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Submission: On June 03 via api from US — Scanned from DE
Submission: On June 03 via api from US — Scanned from DE
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<option value="acoustics"> Acoustics </option>
<option value="amh"> Acta Microbiologica Hellenica (AMH) </option>
<option value="actuators"> Actuators </option>
<option value="admsci"> Administrative Sciences </option>
<option value="adolescents"> Adolescents </option>
<option value="arm"> Advances in Respiratory Medicine (ARM) </option>
<option value="aerobiology"> Aerobiology </option>
<option value="aerospace"> Aerospace </option>
<option value="agriculture"> Agriculture </option>
<option value="agriengineering"> AgriEngineering </option>
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<option value="agronomy"> Agronomy </option>
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<option value="algorithms"> Algorithms </option>
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<option value="analytics"> Analytics </option>
<option value="anatomia"> Anatomia </option>
<option value="anesthres"> Anesthesia Research </option>
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<option value="antibiotics"> Antibiotics </option>
<option value="antibodies"> Antibodies </option>
<option value="antioxidants" selected="selected"> Antioxidants </option>
<option value="applbiosci"> Applied Biosciences </option>
<option value="applmech"> Applied Mechanics </option>
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<option value="applnano"> Applied Nano </option>
<option value="applsci"> Applied Sciences </option>
<option value="asi"> Applied System Innovation (ASI) </option>
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<option value="aquacj"> Aquaculture Journal </option>
<option value="architecture"> Architecture </option>
<option value="arthropoda"> Arthropoda </option>
<option value="arts"> Arts </option>
<option value="astronomy"> Astronomy </option>
<option value="atmosphere"> Atmosphere </option>
<option value="atoms"> Atoms </option>
<option value="audiolres"> Audiology Research </option>
<option value="automation"> Automation </option>
<option value="axioms"> Axioms </option>
<option value="bacteria"> Bacteria </option>
<option value="batteries"> Batteries </option>
<option value="behavsci"> Behavioral Sciences </option>
<option value="beverages"> Beverages </option>
<option value="BDCC"> Big Data and Cognitive Computing (BDCC) </option>
<option value="biochem"> BioChem </option>
<option value="bioengineering"> Bioengineering </option>
<option value="biologics"> Biologics </option>
<option value="biology"> Biology </option>
<option value="blsf"> Biology and Life Sciences Forum </option>
<option value="biomass"> Biomass </option>
<option value="biomechanics"> Biomechanics </option>
<option value="biomed"> BioMed </option>
<option value="biomedicines"> Biomedicines </option>
<option value="biomedinformatics"> BioMedInformatics </option>
<option value="biomimetics"> Biomimetics </option>
<option value="biomolecules"> Biomolecules </option>
<option value="biophysica"> Biophysica </option>
<option value="biosensors"> Biosensors </option>
<option value="biotech"> BioTech </option>
<option value="birds"> Birds </option>
<option value="blockchains"> Blockchains </option>
<option value="brainsci"> Brain Sciences </option>
<option value="buildings"> Buildings </option>
<option value="businesses"> Businesses </option>
<option value="carbon"> C </option>
<option value="cancers"> Cancers </option>
<option value="cardiogenetics"> Cardiogenetics </option>
<option value="catalysts"> Catalysts </option>
<option value="cells"> Cells </option>
<option value="ceramics"> Ceramics </option>
<option value="challenges"> Challenges </option>
<option value="ChemEngineering"> ChemEngineering </option>
<option value="chemistry"> Chemistry </option>
<option value="chemproc"> Chemistry Proceedings </option>
<option value="chemosensors"> Chemosensors </option>
<option value="children"> Children </option>
<option value="chips"> Chips </option>
<option value="civileng"> CivilEng </option>
<option value="cleantechnol"> Clean Technologies (Clean Technol.) </option>
<option value="climate"> Climate </option>
<option value="ctn"> Clinical and Translational Neuroscience (CTN) </option>
<option value="clinpract"> Clinics and Practice </option>
<option value="clockssleep"> Clocks & Sleep </option>
<option value="coasts"> Coasts </option>
<option value="coatings"> Coatings </option>
<option value="colloids"> Colloids and Interfaces </option>
<option value="colorants"> Colorants </option>
<option value="commodities"> Commodities </option>
<option value="complications"> Complications </option>
<option value="compounds"> Compounds </option>
<option value="computation"> Computation </option>
<option value="csmf"> Computer Sciences & Mathematics Forum </option>
<option value="computers"> Computers </option>
<option value="condensedmatter"> Condensed Matter </option>
<option value="conservation"> Conservation </option>
<option value="constrmater"> Construction Materials </option>
<option value="cmd"> Corrosion and Materials Degradation (CMD) </option>
<option value="cosmetics"> Cosmetics </option>
<option value="covid"> COVID </option>
<option value="crops"> Crops </option>
<option value="cryptography"> Cryptography </option>
<option value="crystals"> Crystals </option>
<option value="cimb"> Current Issues in Molecular Biology (CIMB) </option>
<option value="curroncol"> Current Oncology </option>
<option value="dairy"> Dairy </option>
<option value="data"> Data </option>
<option value="dentistry"> Dentistry Journal </option>
<option value="dermato"> Dermato </option>
<option value="dermatopathology"> Dermatopathology </option>
<option value="designs"> Designs </option>
<option value="diabetology"> Diabetology </option>
<option value="diagnostics"> Diagnostics </option>
<option value="dietetics"> Dietetics </option>
<option value="digital"> Digital </option>
<option value="disabilities"> Disabilities </option>
<option value="diseases"> Diseases </option>
<option value="diversity"> Diversity </option>
<option value="dna"> DNA </option>
<option value="drones"> Drones </option>
<option value="ddc"> Drugs and Drug Candidates (DDC) </option>
<option value="dynamics"> Dynamics </option>
<option value="earth"> Earth </option>
<option value="ecologies"> Ecologies </option>
<option value="econometrics"> Econometrics </option>
<option value="economies"> Economies </option>
<option value="education"> Education Sciences </option>
<option value="electricity"> Electricity </option>
<option value="electrochem"> Electrochem </option>
<option value="electronicmat"> Electronic Materials </option>
<option value="electronics"> Electronics </option>
<option value="ecm"> Emergency Care and Medicine </option>
<option value="encyclopedia"> Encyclopedia </option>
<option value="endocrines"> Endocrines </option>
<option value="energies"> Energies </option>
<option value="eng"> Eng </option>
<option value="engproc"> Engineering Proceedings </option>
<option value="entropy"> Entropy </option>
<option value="environsciproc"> Environmental Sciences Proceedings </option>
<option value="environments"> Environments </option>
<option value="epidemiologia"> Epidemiologia </option>
<option value="epigenomes"> Epigenomes </option>
<option value="ebj"> European Burn Journal (EBJ) </option>
<option value="ejihpe"> European Journal of Investigation in Health, Psychology and Education (EJIHPE) </option>
<option value="fermentation"> Fermentation </option>
<option value="fibers"> Fibers </option>
<option value="fintech"> FinTech </option>
<option value="fire"> Fire </option>
<option value="fishes"> Fishes </option>
<option value="fluids"> Fluids </option>
<option value="foods"> Foods </option>
<option value="forecasting"> Forecasting </option>
<option value="forensicsci"> Forensic Sciences </option>
<option value="forests"> Forests </option>
<option value="fossstud"> Fossil Studies </option>
<option value="foundations"> Foundations </option>
<option value="fractalfract"> Fractal and Fractional (Fractal Fract) </option>
<option value="fuels"> Fuels </option>
<option value="future"> Future </option>
<option value="futureinternet"> Future Internet </option>
<option value="futurepharmacol"> Future Pharmacology </option>
<option value="futuretransp"> Future Transportation </option>
<option value="galaxies"> Galaxies </option>
<option value="games"> Games </option>
<option value="gases"> Gases </option>
<option value="gastroent"> Gastroenterology Insights </option>
<option value="gastrointestdisord"> Gastrointestinal Disorders </option>
<option value="gastronomy"> Gastronomy </option>
<option value="gels"> Gels </option>
<option value="genealogy"> Genealogy </option>
<option value="genes"> Genes </option>
<option value="geographies"> Geographies </option>
<option value="geohazards"> GeoHazards </option>
<option value="geomatics"> Geomatics </option>
<option value="geometry"> Geometry </option>
<option value="geosciences"> Geosciences </option>
<option value="geotechnics"> Geotechnics </option>
<option value="geriatrics"> Geriatrics </option>
<option value="glacies"> Glacies </option>
<option value="gucdd"> Gout, Urate, and Crystal Deposition Disease (GUCDD) </option>
<option value="grasses"> Grasses </option>
<option value="hardware"> Hardware </option>
<option value="healthcare"> Healthcare </option>
<option value="hearts"> Hearts </option>
<option value="hemato"> Hemato </option>
<option value="hematolrep"> Hematology Reports </option>
<option value="heritage"> Heritage </option>
<option value="histories"> Histories </option>
<option value="horticulturae"> Horticulturae </option>
<option value="hospitals"> Hospitals </option>
<option value="humanities"> Humanities </option>
<option value="humans"> Humans </option>
<option value="hydrobiology"> Hydrobiology </option>
<option value="hydrogen"> Hydrogen </option>
<option value="hydrology"> Hydrology </option>
<option value="hygiene"> Hygiene </option>
<option value="immuno"> Immuno </option>
<option value="idr"> Infectious Disease Reports </option>
<option value="informatics"> Informatics </option>
<option value="information"> Information </option>
<option value="infrastructures"> Infrastructures </option>
<option value="inorganics"> Inorganics </option>
<option value="insects"> Insects </option>
<option value="instruments"> Instruments </option>
<option value="ijerph"> International Journal of Environmental Research and Public Health (IJERPH) </option>
<option value="ijfs"> International Journal of Financial Studies (IJFS) </option>
<option value="ijms"> International Journal of Molecular Sciences (IJMS) </option>
<option value="IJNS"> International Journal of Neonatal Screening (IJNS) </option>
<option value="ijpb"> International Journal of Plant Biology (IJPB) </option>
<option value="ijt"> International Journal of Topology </option>
<option value="ijtm"> International Journal of Translational Medicine (IJTM) </option>
<option value="ijtpp"> International Journal of Turbomachinery, Propulsion and Power (IJTPP) </option>
<option value="ime"> International Medical Education (IME) </option>
<option value="inventions"> Inventions </option>
<option value="IoT"> IoT </option>
<option value="ijgi"> ISPRS International Journal of Geo-Information (IJGI) </option>
<option value="J"> J </option>
<option value="jal"> Journal of Ageing and Longevity (JAL) </option>
<option value="jcdd"> Journal of Cardiovascular Development and Disease (JCDD) </option>
<option value="jcto"> Journal of Clinical & Translational Ophthalmology (JCTO) </option>
<option value="jcm"> Journal of Clinical Medicine (JCM) </option>
<option value="jcs"> Journal of Composites Science (J. Compos. Sci.) </option>
<option value="jcp"> Journal of Cybersecurity and Privacy (JCP) </option>
<option value="jdb"> Journal of Developmental Biology (JDB) </option>
<option value="jeta"> Journal of Experimental and Theoretical Analyses (JETA) </option>
<option value="jfb"> Journal of Functional Biomaterials (JFB) </option>
<option value="jfmk"> Journal of Functional Morphology and Kinesiology (JFMK) </option>
<option value="jof"> Journal of Fungi (JoF) </option>
<option value="jimaging"> Journal of Imaging (J. Imaging) </option>
<option value="jintelligence"> Journal of Intelligence (J. Intell.) </option>
<option value="jlpea"> Journal of Low Power Electronics and Applications (JLPEA) </option>
<option value="jmmp"> Journal of Manufacturing and Materials Processing (JMMP) </option>
<option value="jmse"> Journal of Marine Science and Engineering (JMSE) </option>
<option value="jmahp"> Journal of Market Access & Health Policy (JMAHP) </option>
<option value="jmp"> Journal of Molecular Pathology (JMP) </option>
<option value="jnt"> Journal of Nanotheranostics (JNT) </option>
<option value="jne"> Journal of Nuclear Engineering (JNE) </option>
<option value="ohbm"> Journal of Otorhinolaryngology, Hearing and Balance Medicine (JOHBM) </option>
<option value="jpm"> Journal of Personalized Medicine (JPM) </option>
<option value="jpbi"> Journal of Pharmaceutical and BioTech Industry (JPBI) </option>
<option value="jor"> Journal of Respiration (JoR) </option>
<option value="jrfm"> Journal of Risk and Financial Management (JRFM) </option>
<option value="jsan"> Journal of Sensor and Actuator Networks (JSAN) </option>
<option value="jtaer"> Journal of Theoretical and Applied Electronic Commerce Research (JTAER) </option>
<option value="jvd"> Journal of Vascular Diseases (JVD) </option>
<option value="jox"> Journal of Xenobiotics (JoX) </option>
<option value="jzbg"> Journal of Zoological and Botanical Gardens (JZBG) </option>
<option value="journalmedia"> Journalism and Media </option>
<option value="kidneydial"> Kidney and Dialysis </option>
<option value="kinasesphosphatases"> Kinases and Phosphatases </option>
<option value="knowledge"> Knowledge </option>
<option value="laboratories"> Laboratories </option>
<option value="land"> Land </option>
<option value="languages"> Languages </option>
<option value="laws"> Laws </option>
<option value="life"> Life </option>
<option value="limnolrev"> Limnological Review </option>
<option value="lipidology"> Lipidology </option>
<option value="liquids"> Liquids </option>
<option value="literature"> Literature </option>
<option value="livers"> Livers </option>
<option value="logics"> Logics </option>
<option value="logistics"> Logistics </option>
<option value="lubricants"> Lubricants </option>
<option value="lymphatics"> Lymphatics </option>
<option value="make"> Machine Learning and Knowledge Extraction (MAKE) </option>
<option value="machines"> Machines </option>
<option value="macromol"> Macromol </option>
<option value="magnetism"> Magnetism </option>
<option value="magnetochemistry"> Magnetochemistry </option>
<option value="marinedrugs"> Marine Drugs </option>
<option value="materials"> Materials </option>
<option value="materproc"> Materials Proceedings </option>
<option value="mca"> Mathematical and Computational Applications (MCA) </option>
<option value="mathematics"> Mathematics </option>
<option value="medsci"> Medical Sciences </option>
<option value="msf"> Medical Sciences Forum </option>
<option value="medicina"> Medicina </option>
<option value="medicines"> Medicines </option>
<option value="membranes"> Membranes </option>
<option value="merits"> Merits </option>
<option value="metabolites"> Metabolites </option>
<option value="metals"> Metals </option>
<option value="meteorology"> Meteorology </option>
<option value="methane"> Methane </option>
<option value="mps"> Methods and Protocols (MPs) </option>
<option value="metrology"> Metrology </option>
<option value="micro"> Micro </option>
<option value="microbiolres"> Microbiology Research </option>
<option value="micromachines"> Micromachines </option>
<option value="microorganisms"> Microorganisms </option>
<option value="microplastics"> Microplastics </option>
<option value="minerals"> Minerals </option>
<option value="mining"> Mining </option>
<option value="modelling"> Modelling </option>
<option value="molbank"> Molbank </option>
<option value="molecules"> Molecules </option>
<option value="mti"> Multimodal Technologies and Interaction (MTI) </option>
<option value="muscles"> Muscles </option>
<option value="nanoenergyadv"> Nanoenergy Advances </option>
<option value="nanomanufacturing"> Nanomanufacturing </option>
<option value="nanomaterials"> Nanomaterials </option>
<option value="ndt"> NDT </option>
<option value="network"> Network </option>
<option value="neuroglia"> Neuroglia </option>
<option value="neurolint"> Neurology International </option>
<option value="neurosci"> NeuroSci </option>
<option value="nitrogen"> Nitrogen </option>
<option value="ncrna"> Non-Coding RNA (ncRNA) </option>
<option value="nursrep"> Nursing Reports </option>
<option value="nutraceuticals"> Nutraceuticals </option>
<option value="nutrients"> Nutrients </option>
<option value="obesities"> Obesities </option>
<option value="oceans"> Oceans </option>
<option value="onco"> Onco </option>
<option value="optics"> Optics </option>
<option value="oral"> Oral </option>
<option value="organics"> Organics </option>
<option value="organoids"> Organoids </option>
<option value="osteology"> Osteology </option>
<option value="oxygen"> Oxygen </option>
<option value="parasitologia"> Parasitologia </option>
<option value="particles"> Particles </option>
<option value="pathogens"> Pathogens </option>
<option value="pathophysiology"> Pathophysiology </option>
<option value="pediatrrep"> Pediatric Reports </option>
<option value="pets"> Pets </option>
<option value="pharmaceuticals"> Pharmaceuticals </option>
<option value="pharmaceutics"> Pharmaceutics </option>
<option value="pharmacoepidemiology"> Pharmacoepidemiology </option>
<option value="pharmacy"> Pharmacy </option>
<option value="philosophies"> Philosophies </option>
<option value="photochem"> Photochem </option>
<option value="photonics"> Photonics </option>
<option value="phycology"> Phycology </option>
<option value="physchem"> Physchem </option>
<option value="psf"> Physical Sciences Forum </option>
<option value="physics"> Physics </option>
<option value="physiologia"> Physiologia </option>
<option value="plants"> Plants </option>
<option value="plasma"> Plasma </option>
<option value="platforms"> Platforms </option>
<option value="pollutants"> Pollutants </option>
<option value="polymers"> Polymers </option>
<option value="polysaccharides"> Polysaccharides </option>
<option value="poultry"> Poultry </option>
<option value="powders"> Powders </option>
<option value="proceedings"> Proceedings </option>
<option value="processes"> Processes </option>
<option value="prosthesis"> Prosthesis </option>
<option value="proteomes"> Proteomes </option>
<option value="psychiatryint"> Psychiatry International </option>
<option value="psychoactives"> Psychoactives </option>
<option value="psycholint"> Psychology International </option>
<option value="publications"> Publications </option>
<option value="qubs"> Quantum Beam Science (QuBS) </option>
<option value="quantumrep"> Quantum Reports </option>
<option value="quaternary"> Quaternary </option>
<option value="radiation"> Radiation </option>
<option value="reactions"> Reactions </option>
<option value="realestate"> Real Estate </option>
<option value="receptors"> Receptors </option>
<option value="recycling"> Recycling </option>
<option value="religions"> Religions </option>
<option value="remotesensing"> Remote Sensing </option>
<option value="reports"> Reports </option>
<option value="reprodmed"> Reproductive Medicine (Reprod. Med.) </option>
<option value="resources"> Resources </option>
<option value="rheumato"> Rheumato </option>
<option value="risks"> Risks </option>
<option value="robotics"> Robotics </option>
<option value="ruminants"> Ruminants </option>
<option value="safety"> Safety </option>
<option value="sci"> Sci </option>
<option value="scipharm"> Scientia Pharmaceutica (Sci. Pharm.) </option>
<option value="sclerosis"> Sclerosis </option>
<option value="seeds"> Seeds </option>
<option value="sensors"> Sensors </option>
<option value="separations"> Separations </option>
<option value="sexes"> Sexes </option>
<option value="signals"> Signals </option>
<option value="sinusitis"> Sinusitis </option>
<option value="smartcities"> Smart Cities </option>
<option value="socsci"> Social Sciences </option>
<option value="siuj"> Société Internationale d’Urologie Journal (SIUJ) </option>
<option value="societies"> Societies </option>
<option value="software"> Software </option>
<option value="soilsystems"> Soil Systems </option>
<option value="solar"> Solar </option>
<option value="solids"> Solids </option>
<option value="spectroscj"> Spectroscopy Journal </option>
<option value="sports"> Sports </option>
<option value="standards"> Standards </option>
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<option value="84276">Reaction Mechanism of the Ferredoxin–Ferredoxin NAD(P)+/H Oxidoreductase System</option>
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<option value="94989">The 10th Anniversary of Antioxidants: Past, Present and Future</option>
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<option value="195792">Use of Antioxidant Supplementation in Aquaculture: Impact on Growth, Health, and Product Quality</option>
<option value="20736">When the Anticancer Strategies Modulating Oxidative Stress Meet Nanomedicine: New Perspectives</option>
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<select multiple="" id="newsletter-journal" class="foundation-select jqmsLoaded" name="journals[]" style="display: none;">
<option value="acoustics">Acoustics</option>
<option value="amh">Acta Microbiologica Hellenica</option>
<option value="actuators">Actuators</option>
<option value="admsci">Administrative Sciences</option>
<option value="adolescents">Adolescents</option>
<option value="arm">Advances in Respiratory Medicine</option>
<option value="aerobiology">Aerobiology</option>
<option value="aerospace">Aerospace</option>
<option value="agriculture">Agriculture</option>
<option value="agriengineering">AgriEngineering</option>
<option value="agrochemicals">Agrochemicals</option>
<option value="agronomy">Agronomy</option>
<option value="ai">AI</option>
<option value="air">Air</option>
<option value="algorithms">Algorithms</option>
<option value="allergies">Allergies</option>
<option value="alloys">Alloys</option>
<option value="analytica">Analytica</option>
<option value="analytics">Analytics</option>
<option value="anatomia">Anatomia</option>
<option value="anesthres">Anesthesia Research</option>
<option value="animals">Animals</option>
<option value="antibiotics">Antibiotics</option>
<option value="antibodies">Antibodies</option>
<option value="antioxidants">Antioxidants</option>
<option value="applbiosci">Applied Biosciences</option>
<option value="applmech">Applied Mechanics</option>
<option value="applmicrobiol">Applied Microbiology</option>
<option value="applnano">Applied Nano</option>
<option value="applsci">Applied Sciences</option>
<option value="asi">Applied System Innovation</option>
<option value="appliedchem">AppliedChem</option>
<option value="appliedmath">AppliedMath</option>
<option value="aquacj">Aquaculture Journal</option>
<option value="architecture">Architecture</option>
<option value="arthropoda">Arthropoda</option>
<option value="arts">Arts</option>
<option value="astronomy">Astronomy</option>
<option value="atmosphere">Atmosphere</option>
<option value="atoms">Atoms</option>
<option value="audiolres">Audiology Research</option>
<option value="automation">Automation</option>
<option value="axioms">Axioms</option>
<option value="bacteria">Bacteria</option>
<option value="batteries">Batteries</option>
<option value="behavsci">Behavioral Sciences</option>
<option value="beverages">Beverages</option>
<option value="BDCC">Big Data and Cognitive Computing</option>
<option value="biochem">BioChem</option>
<option value="bioengineering">Bioengineering</option>
<option value="biologics">Biologics</option>
<option value="biology">Biology</option>
<option value="blsf">Biology and Life Sciences Forum</option>
<option value="biomass">Biomass</option>
<option value="biomechanics">Biomechanics</option>
<option value="biomed">BioMed</option>
<option value="biomedicines">Biomedicines</option>
<option value="biomedinformatics">BioMedInformatics</option>
<option value="biomimetics">Biomimetics</option>
<option value="biomolecules">Biomolecules</option>
<option value="biophysica">Biophysica</option>
<option value="biosensors">Biosensors</option>
<option value="biotech">BioTech</option>
<option value="birds">Birds</option>
<option value="blockchains">Blockchains</option>
<option value="brainsci">Brain Sciences</option>
<option value="buildings">Buildings</option>
<option value="businesses">Businesses</option>
<option value="carbon">C</option>
<option value="cancers">Cancers</option>
<option value="cardiogenetics">Cardiogenetics</option>
<option value="catalysts">Catalysts</option>
<option value="cells">Cells</option>
<option value="ceramics">Ceramics</option>
<option value="challenges">Challenges</option>
<option value="ChemEngineering">ChemEngineering</option>
<option value="chemistry">Chemistry</option>
<option value="chemproc">Chemistry Proceedings</option>
<option value="chemosensors">Chemosensors</option>
<option value="children">Children</option>
<option value="chips">Chips</option>
<option value="civileng">CivilEng</option>
<option value="cleantechnol">Clean Technologies</option>
<option value="climate">Climate</option>
<option value="ctn">Clinical and Translational Neuroscience</option>
<option value="clinpract">Clinics and Practice</option>
<option value="clockssleep">Clocks & Sleep</option>
<option value="coasts">Coasts</option>
<option value="coatings">Coatings</option>
<option value="colloids">Colloids and Interfaces</option>
<option value="colorants">Colorants</option>
<option value="commodities">Commodities</option>
<option value="complications">Complications</option>
<option value="compounds">Compounds</option>
<option value="computation">Computation</option>
<option value="csmf">Computer Sciences & Mathematics Forum</option>
<option value="computers">Computers</option>
<option value="condensedmatter">Condensed Matter</option>
<option value="conservation">Conservation</option>
<option value="constrmater">Construction Materials</option>
<option value="cmd">Corrosion and Materials Degradation</option>
<option value="cosmetics">Cosmetics</option>
<option value="covid">COVID</option>
<option value="crops">Crops</option>
<option value="cryptography">Cryptography</option>
<option value="crystals">Crystals</option>
<option value="cimb">Current Issues in Molecular Biology</option>
<option value="curroncol">Current Oncology</option>
<option value="dairy">Dairy</option>
<option value="data">Data</option>
<option value="dentistry">Dentistry Journal</option>
<option value="dermato">Dermato</option>
<option value="dermatopathology">Dermatopathology</option>
<option value="designs">Designs</option>
<option value="diabetology">Diabetology</option>
<option value="diagnostics">Diagnostics</option>
<option value="dietetics">Dietetics</option>
<option value="digital">Digital</option>
<option value="disabilities">Disabilities</option>
<option value="diseases">Diseases</option>
<option value="diversity">Diversity</option>
<option value="dna">DNA</option>
<option value="drones">Drones</option>
<option value="ddc">Drugs and Drug Candidates</option>
<option value="dynamics">Dynamics</option>
<option value="earth">Earth</option>
<option value="ecologies">Ecologies</option>
<option value="econometrics">Econometrics</option>
<option value="economies">Economies</option>
<option value="education">Education Sciences</option>
<option value="electricity">Electricity</option>
<option value="electrochem">Electrochem</option>
<option value="electronicmat">Electronic Materials</option>
<option value="electronics">Electronics</option>
<option value="ecm">Emergency Care and Medicine</option>
<option value="encyclopedia">Encyclopedia</option>
<option value="endocrines">Endocrines</option>
<option value="energies">Energies</option>
<option value="eng">Eng</option>
<option value="engproc">Engineering Proceedings</option>
<option value="entropy">Entropy</option>
<option value="environsciproc">Environmental Sciences Proceedings</option>
<option value="environments">Environments</option>
<option value="epidemiologia">Epidemiologia</option>
<option value="epigenomes">Epigenomes</option>
<option value="ebj">European Burn Journal</option>
<option value="ejihpe">European Journal of Investigation in Health, Psychology and Education</option>
<option value="fermentation">Fermentation</option>
<option value="fibers">Fibers</option>
<option value="fintech">FinTech</option>
<option value="fire">Fire</option>
<option value="fishes">Fishes</option>
<option value="fluids">Fluids</option>
<option value="foods">Foods</option>
<option value="forecasting">Forecasting</option>
<option value="forensicsci">Forensic Sciences</option>
<option value="forests">Forests</option>
<option value="fossstud">Fossil Studies</option>
<option value="foundations">Foundations</option>
<option value="fractalfract">Fractal and Fractional</option>
<option value="fuels">Fuels</option>
<option value="future">Future</option>
<option value="futureinternet">Future Internet</option>
<option value="futurepharmacol">Future Pharmacology</option>
<option value="futuretransp">Future Transportation</option>
<option value="galaxies">Galaxies</option>
<option value="games">Games</option>
<option value="gases">Gases</option>
<option value="gastroent">Gastroenterology Insights</option>
<option value="gastrointestdisord">Gastrointestinal Disorders</option>
<option value="gastronomy">Gastronomy</option>
<option value="gels">Gels</option>
<option value="genealogy">Genealogy</option>
<option value="genes">Genes</option>
<option value="geographies">Geographies</option>
<option value="geohazards">GeoHazards</option>
<option value="geomatics">Geomatics</option>
<option value="geometry">Geometry</option>
<option value="geosciences">Geosciences</option>
<option value="geotechnics">Geotechnics</option>
<option value="geriatrics">Geriatrics</option>
<option value="glacies">Glacies</option>
<option value="gucdd">Gout, Urate, and Crystal Deposition Disease</option>
<option value="grasses">Grasses</option>
<option value="hardware">Hardware</option>
<option value="healthcare">Healthcare</option>
<option value="hearts">Hearts</option>
<option value="hemato">Hemato</option>
<option value="hematolrep">Hematology Reports</option>
<option value="heritage">Heritage</option>
<option value="histories">Histories</option>
<option value="horticulturae">Horticulturae</option>
<option value="hospitals">Hospitals</option>
<option value="humanities">Humanities</option>
<option value="humans">Humans</option>
<option value="hydrobiology">Hydrobiology</option>
<option value="hydrogen">Hydrogen</option>
<option value="hydrology">Hydrology</option>
<option value="hygiene">Hygiene</option>
<option value="immuno">Immuno</option>
<option value="idr">Infectious Disease Reports</option>
<option value="informatics">Informatics</option>
<option value="information">Information</option>
<option value="infrastructures">Infrastructures</option>
<option value="inorganics">Inorganics</option>
<option value="insects">Insects</option>
<option value="instruments">Instruments</option>
<option value="ijerph">International Journal of Environmental Research and Public Health</option>
<option value="ijfs">International Journal of Financial Studies</option>
<option value="ijms">International Journal of Molecular Sciences</option>
<option value="IJNS">International Journal of Neonatal Screening</option>
<option value="ijpb">International Journal of Plant Biology</option>
<option value="ijt">International Journal of Topology</option>
<option value="ijtm">International Journal of Translational Medicine</option>
<option value="ijtpp">International Journal of Turbomachinery, Propulsion and Power</option>
<option value="ime">International Medical Education</option>
<option value="inventions">Inventions</option>
<option value="IoT">IoT</option>
<option value="ijgi">ISPRS International Journal of Geo-Information</option>
<option value="J">J</option>
<option value="jal">Journal of Ageing and Longevity</option>
<option value="jcdd">Journal of Cardiovascular Development and Disease</option>
<option value="jcto">Journal of Clinical & Translational Ophthalmology</option>
<option value="jcm">Journal of Clinical Medicine</option>
<option value="jcs">Journal of Composites Science</option>
<option value="jcp">Journal of Cybersecurity and Privacy</option>
<option value="jdb">Journal of Developmental Biology</option>
<option value="jeta">Journal of Experimental and Theoretical Analyses</option>
<option value="jfb">Journal of Functional Biomaterials</option>
<option value="jfmk">Journal of Functional Morphology and Kinesiology</option>
<option value="jof">Journal of Fungi</option>
<option value="jimaging">Journal of Imaging</option>
<option value="jintelligence">Journal of Intelligence</option>
<option value="jlpea">Journal of Low Power Electronics and Applications</option>
<option value="jmmp">Journal of Manufacturing and Materials Processing</option>
<option value="jmse">Journal of Marine Science and Engineering</option>
<option value="jmahp">Journal of Market Access & Health Policy</option>
<option value="jmp">Journal of Molecular Pathology</option>
<option value="jnt">Journal of Nanotheranostics</option>
<option value="jne">Journal of Nuclear Engineering</option>
<option value="ohbm">Journal of Otorhinolaryngology, Hearing and Balance Medicine</option>
<option value="jpm">Journal of Personalized Medicine</option>
<option value="jpbi">Journal of Pharmaceutical and BioTech Industry</option>
<option value="jor">Journal of Respiration</option>
<option value="jrfm">Journal of Risk and Financial Management</option>
<option value="jsan">Journal of Sensor and Actuator Networks</option>
<option value="jtaer">Journal of Theoretical and Applied Electronic Commerce Research</option>
<option value="jvd">Journal of Vascular Diseases</option>
<option value="jox">Journal of Xenobiotics</option>
<option value="jzbg">Journal of Zoological and Botanical Gardens</option>
<option value="journalmedia">Journalism and Media</option>
<option value="kidneydial">Kidney and Dialysis</option>
<option value="kinasesphosphatases">Kinases and Phosphatases</option>
<option value="knowledge">Knowledge</option>
<option value="laboratories">Laboratories</option>
<option value="land">Land</option>
<option value="languages">Languages</option>
<option value="laws">Laws</option>
<option value="life">Life</option>
<option value="limnolrev">Limnological Review</option>
<option value="lipidology">Lipidology</option>
<option value="liquids">Liquids</option>
<option value="literature">Literature</option>
<option value="livers">Livers</option>
<option value="logics">Logics</option>
<option value="logistics">Logistics</option>
<option value="lubricants">Lubricants</option>
<option value="lymphatics">Lymphatics</option>
<option value="make">Machine Learning and Knowledge Extraction</option>
<option value="machines">Machines</option>
<option value="macromol">Macromol</option>
<option value="magnetism">Magnetism</option>
<option value="magnetochemistry">Magnetochemistry</option>
<option value="marinedrugs">Marine Drugs</option>
<option value="materials">Materials</option>
<option value="materproc">Materials Proceedings</option>
<option value="mca">Mathematical and Computational Applications</option>
<option value="mathematics">Mathematics</option>
<option value="medsci">Medical Sciences</option>
<option value="msf">Medical Sciences Forum</option>
<option value="medicina">Medicina</option>
<option value="medicines">Medicines</option>
<option value="membranes">Membranes</option>
<option value="merits">Merits</option>
<option value="metabolites">Metabolites</option>
<option value="metals">Metals</option>
<option value="meteorology">Meteorology</option>
<option value="methane">Methane</option>
<option value="mps">Methods and Protocols</option>
<option value="metrology">Metrology</option>
<option value="micro">Micro</option>
<option value="microbiolres">Microbiology Research</option>
<option value="micromachines">Micromachines</option>
<option value="microorganisms">Microorganisms</option>
<option value="microplastics">Microplastics</option>
<option value="minerals">Minerals</option>
<option value="mining">Mining</option>
<option value="modelling">Modelling</option>
<option value="molbank">Molbank</option>
<option value="molecules">Molecules</option>
<option value="mti">Multimodal Technologies and Interaction</option>
<option value="muscles">Muscles</option>
<option value="nanoenergyadv">Nanoenergy Advances</option>
<option value="nanomanufacturing">Nanomanufacturing</option>
<option value="nanomaterials">Nanomaterials</option>
<option value="ndt">NDT</option>
<option value="network">Network</option>
<option value="neuroglia">Neuroglia</option>
<option value="neurolint">Neurology International</option>
<option value="neurosci">NeuroSci</option>
<option value="nitrogen">Nitrogen</option>
<option value="ncrna">Non-Coding RNA</option>
<option value="nursrep">Nursing Reports</option>
<option value="nutraceuticals">Nutraceuticals</option>
<option value="nutrients">Nutrients</option>
<option value="obesities">Obesities</option>
<option value="oceans">Oceans</option>
<option value="onco">Onco</option>
<option value="optics">Optics</option>
<option value="oral">Oral</option>
<option value="organics">Organics</option>
<option value="organoids">Organoids</option>
<option value="osteology">Osteology</option>
<option value="oxygen">Oxygen</option>
<option value="parasitologia">Parasitologia</option>
<option value="particles">Particles</option>
<option value="pathogens">Pathogens</option>
<option value="pathophysiology">Pathophysiology</option>
<option value="pediatrrep">Pediatric Reports</option>
<option value="pets">Pets</option>
<option value="pharmaceuticals">Pharmaceuticals</option>
<option value="pharmaceutics">Pharmaceutics</option>
<option value="pharmacoepidemiology">Pharmacoepidemiology</option>
<option value="pharmacy">Pharmacy</option>
<option value="philosophies">Philosophies</option>
<option value="photochem">Photochem</option>
<option value="photonics">Photonics</option>
<option value="phycology">Phycology</option>
<option value="physchem">Physchem</option>
<option value="psf">Physical Sciences Forum</option>
<option value="physics">Physics</option>
<option value="physiologia">Physiologia</option>
<option value="plants">Plants</option>
<option value="plasma">Plasma</option>
<option value="platforms">Platforms</option>
<option value="pollutants">Pollutants</option>
<option value="polymers">Polymers</option>
<option value="polysaccharides">Polysaccharides</option>
<option value="poultry">Poultry</option>
<option value="powders">Powders</option>
<option value="proceedings">Proceedings</option>
<option value="processes">Processes</option>
<option value="prosthesis">Prosthesis</option>
<option value="proteomes">Proteomes</option>
<option value="psychiatryint">Psychiatry International</option>
<option value="psychoactives">Psychoactives</option>
<option value="psycholint">Psychology International</option>
<option value="publications">Publications</option>
<option value="qubs">Quantum Beam Science</option>
<option value="quantumrep">Quantum Reports</option>
<option value="quaternary">Quaternary</option>
<option value="radiation">Radiation</option>
<option value="reactions">Reactions</option>
<option value="realestate">Real Estate</option>
<option value="receptors">Receptors</option>
<option value="recycling">Recycling</option>
<option value="religions">Religions</option>
<option value="remotesensing">Remote Sensing</option>
<option value="reports">Reports</option>
<option value="reprodmed">Reproductive Medicine</option>
<option value="resources">Resources</option>
<option value="rheumato">Rheumato</option>
<option value="risks">Risks</option>
<option value="robotics">Robotics</option>
<option value="ruminants">Ruminants</option>
<option value="safety">Safety</option>
<option value="sci">Sci</option>
<option value="scipharm">Scientia Pharmaceutica</option>
<option value="sclerosis">Sclerosis</option>
<option value="seeds">Seeds</option>
<option value="sensors">Sensors</option>
<option value="separations">Separations</option>
<option value="sexes">Sexes</option>
<option value="signals">Signals</option>
<option value="sinusitis">Sinusitis</option>
<option value="smartcities">Smart Cities</option>
<option value="socsci">Social Sciences</option>
<option value="siuj">Société Internationale d’Urologie Journal</option>
<option value="societies">Societies</option>
<option value="software">Software</option>
<option value="soilsystems">Soil Systems</option>
<option value="solar">Solar</option>
<option value="solids">Solids</option>
<option value="spectroscj">Spectroscopy Journal</option>
<option value="sports">Sports</option>
<option value="standards">Standards</option>
<option value="stats">Stats</option>
<option value="stresses">Stresses</option>
<option value="surfaces">Surfaces</option>
<option value="surgeries">Surgeries</option>
<option value="std">Surgical Techniques Development</option>
<option value="sustainability">Sustainability</option>
<option value="suschem">Sustainable Chemistry</option>
<option value="symmetry">Symmetry</option>
<option value="synbio">SynBio</option>
<option value="systems">Systems</option>
<option value="targets">Targets</option>
<option value="taxonomy">Taxonomy</option>
<option value="technologies">Technologies</option>
<option value="telecom">Telecom</option>
<option value="textiles">Textiles</option>
<option value="thalassrep">Thalassemia Reports</option>
<option value="therapeutics">Therapeutics</option>
<option value="thermo">Thermo</option>
<option value="timespace">Time and Space</option>
<option value="tomography">Tomography</option>
<option value="tourismhosp">Tourism and Hospitality</option>
<option value="toxics">Toxics</option>
<option value="toxins">Toxins</option>
<option value="transplantology">Transplantology</option>
<option value="traumacare">Trauma Care</option>
<option value="higheredu">Trends in Higher Education</option>
<option value="tropicalmed">Tropical Medicine and Infectious Disease</option>
<option value="universe">Universe</option>
<option value="urbansci">Urban Science</option>
<option value="uro">Uro</option>
<option value="vaccines">Vaccines</option>
<option value="vehicles">Vehicles</option>
<option value="venereology">Venereology</option>
<option value="vetsci">Veterinary Sciences</option>
<option value="vibration">Vibration</option>
<option value="virtualworlds">Virtual Worlds</option>
<option value="viruses">Viruses</option>
<option value="vision">Vision</option>
<option value="waste">Waste</option>
<option value="water">Water</option>
<option value="wind">Wind</option>
<option value="women">Women</option>
<option value="world">World</option>
<option value="wevj">World Electric Vehicle Journal</option>
<option value="youth">Youth</option>
<option value="zoonoticdis">Zoonotic Diseases</option>
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<li class=""><label for="ms-opt-298" style="padding-left: 23px;"><input type="checkbox" value="modelling" title="Modelling" id="ms-opt-298">Modelling</label></li>
<li class=""><label for="ms-opt-299" style="padding-left: 23px;"><input type="checkbox" value="molbank" title="Molbank" id="ms-opt-299">Molbank</label></li>
<li class=""><label for="ms-opt-300" style="padding-left: 23px;"><input type="checkbox" value="molecules" title="Molecules" id="ms-opt-300">Molecules</label></li>
<li class=""><label for="ms-opt-301" style="padding-left: 23px;"><input type="checkbox" value="mti" title="Multimodal Technologies and Interaction" id="ms-opt-301">Multimodal Technologies and Interaction</label></li>
<li class=""><label for="ms-opt-302" style="padding-left: 23px;"><input type="checkbox" value="muscles" title="Muscles" id="ms-opt-302">Muscles</label></li>
<li class=""><label for="ms-opt-303" style="padding-left: 23px;"><input type="checkbox" value="nanoenergyadv" title="Nanoenergy Advances" id="ms-opt-303">Nanoenergy Advances</label></li>
<li class=""><label for="ms-opt-304" style="padding-left: 23px;"><input type="checkbox" value="nanomanufacturing" title="Nanomanufacturing" id="ms-opt-304">Nanomanufacturing</label></li>
<li class=""><label for="ms-opt-305" style="padding-left: 23px;"><input type="checkbox" value="nanomaterials" title="Nanomaterials" id="ms-opt-305">Nanomaterials</label></li>
<li class=""><label for="ms-opt-306" style="padding-left: 23px;"><input type="checkbox" value="ndt" title="NDT" id="ms-opt-306">NDT</label></li>
<li class=""><label for="ms-opt-307" style="padding-left: 23px;"><input type="checkbox" value="network" title="Network" id="ms-opt-307">Network</label></li>
<li class=""><label for="ms-opt-308" style="padding-left: 23px;"><input type="checkbox" value="neuroglia" title="Neuroglia" id="ms-opt-308">Neuroglia</label></li>
<li class=""><label for="ms-opt-309" style="padding-left: 23px;"><input type="checkbox" value="neurolint" title="Neurology International" id="ms-opt-309">Neurology International</label></li>
<li class=""><label for="ms-opt-310" style="padding-left: 23px;"><input type="checkbox" value="neurosci" title="NeuroSci" id="ms-opt-310">NeuroSci</label></li>
<li class=""><label for="ms-opt-311" style="padding-left: 23px;"><input type="checkbox" value="nitrogen" title="Nitrogen" id="ms-opt-311">Nitrogen</label></li>
<li class=""><label for="ms-opt-312" style="padding-left: 23px;"><input type="checkbox" value="ncrna" title="Non-Coding RNA" id="ms-opt-312">Non-Coding RNA</label></li>
<li class=""><label for="ms-opt-313" style="padding-left: 23px;"><input type="checkbox" value="nursrep" title="Nursing Reports" id="ms-opt-313">Nursing Reports</label></li>
<li class=""><label for="ms-opt-314" style="padding-left: 23px;"><input type="checkbox" value="nutraceuticals" title="Nutraceuticals" id="ms-opt-314">Nutraceuticals</label></li>
<li class=""><label for="ms-opt-315" style="padding-left: 23px;"><input type="checkbox" value="nutrients" title="Nutrients" id="ms-opt-315">Nutrients</label></li>
<li class=""><label for="ms-opt-316" style="padding-left: 23px;"><input type="checkbox" value="obesities" title="Obesities" id="ms-opt-316">Obesities</label></li>
<li class=""><label for="ms-opt-317" style="padding-left: 23px;"><input type="checkbox" value="oceans" title="Oceans" id="ms-opt-317">Oceans</label></li>
<li class=""><label for="ms-opt-318" style="padding-left: 23px;"><input type="checkbox" value="onco" title="Onco" id="ms-opt-318">Onco</label></li>
<li class=""><label for="ms-opt-319" style="padding-left: 23px;"><input type="checkbox" value="optics" title="Optics" id="ms-opt-319">Optics</label></li>
<li class=""><label for="ms-opt-320" style="padding-left: 23px;"><input type="checkbox" value="oral" title="Oral" id="ms-opt-320">Oral</label></li>
<li class=""><label for="ms-opt-321" style="padding-left: 23px;"><input type="checkbox" value="organics" title="Organics" id="ms-opt-321">Organics</label></li>
<li class=""><label for="ms-opt-322" style="padding-left: 23px;"><input type="checkbox" value="organoids" title="Organoids" id="ms-opt-322">Organoids</label></li>
<li class=""><label for="ms-opt-323" style="padding-left: 23px;"><input type="checkbox" value="osteology" title="Osteology" id="ms-opt-323">Osteology</label></li>
<li class=""><label for="ms-opt-324" style="padding-left: 23px;"><input type="checkbox" value="oxygen" title="Oxygen" id="ms-opt-324">Oxygen</label></li>
<li class=""><label for="ms-opt-325" style="padding-left: 23px;"><input type="checkbox" value="parasitologia" title="Parasitologia" id="ms-opt-325">Parasitologia</label></li>
<li class=""><label for="ms-opt-326" style="padding-left: 23px;"><input type="checkbox" value="particles" title="Particles" id="ms-opt-326">Particles</label></li>
<li class=""><label for="ms-opt-327" style="padding-left: 23px;"><input type="checkbox" value="pathogens" title="Pathogens" id="ms-opt-327">Pathogens</label></li>
<li class=""><label for="ms-opt-328" style="padding-left: 23px;"><input type="checkbox" value="pathophysiology" title="Pathophysiology" id="ms-opt-328">Pathophysiology</label></li>
<li class=""><label for="ms-opt-329" style="padding-left: 23px;"><input type="checkbox" value="pediatrrep" title="Pediatric Reports" id="ms-opt-329">Pediatric Reports</label></li>
<li class=""><label for="ms-opt-330" style="padding-left: 23px;"><input type="checkbox" value="pets" title="Pets" id="ms-opt-330">Pets</label></li>
<li class=""><label for="ms-opt-331" style="padding-left: 23px;"><input type="checkbox" value="pharmaceuticals" title="Pharmaceuticals" id="ms-opt-331">Pharmaceuticals</label></li>
<li class=""><label for="ms-opt-332" style="padding-left: 23px;"><input type="checkbox" value="pharmaceutics" title="Pharmaceutics" id="ms-opt-332">Pharmaceutics</label></li>
<li class=""><label for="ms-opt-333" style="padding-left: 23px;"><input type="checkbox" value="pharmacoepidemiology" title="Pharmacoepidemiology" id="ms-opt-333">Pharmacoepidemiology</label></li>
<li class=""><label for="ms-opt-334" style="padding-left: 23px;"><input type="checkbox" value="pharmacy" title="Pharmacy" id="ms-opt-334">Pharmacy</label></li>
<li class=""><label for="ms-opt-335" style="padding-left: 23px;"><input type="checkbox" value="philosophies" title="Philosophies" id="ms-opt-335">Philosophies</label></li>
<li class=""><label for="ms-opt-336" style="padding-left: 23px;"><input type="checkbox" value="photochem" title="Photochem" id="ms-opt-336">Photochem</label></li>
<li class=""><label for="ms-opt-337" style="padding-left: 23px;"><input type="checkbox" value="photonics" title="Photonics" id="ms-opt-337">Photonics</label></li>
<li class=""><label for="ms-opt-338" style="padding-left: 23px;"><input type="checkbox" value="phycology" title="Phycology" id="ms-opt-338">Phycology</label></li>
<li class=""><label for="ms-opt-339" style="padding-left: 23px;"><input type="checkbox" value="physchem" title="Physchem" id="ms-opt-339">Physchem</label></li>
<li class=""><label for="ms-opt-340" style="padding-left: 23px;"><input type="checkbox" value="psf" title="Physical Sciences Forum" id="ms-opt-340">Physical Sciences Forum</label></li>
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<li class=""><label for="ms-opt-343" style="padding-left: 23px;"><input type="checkbox" value="plants" title="Plants" id="ms-opt-343">Plants</label></li>
<li class=""><label for="ms-opt-344" style="padding-left: 23px;"><input type="checkbox" value="plasma" title="Plasma" id="ms-opt-344">Plasma</label></li>
<li class=""><label for="ms-opt-345" style="padding-left: 23px;"><input type="checkbox" value="platforms" title="Platforms" id="ms-opt-345">Platforms</label></li>
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<li class=""><label for="ms-opt-347" style="padding-left: 23px;"><input type="checkbox" value="polymers" title="Polymers" id="ms-opt-347">Polymers</label></li>
<li class=""><label for="ms-opt-348" style="padding-left: 23px;"><input type="checkbox" value="polysaccharides" title="Polysaccharides" id="ms-opt-348">Polysaccharides</label></li>
<li class=""><label for="ms-opt-349" style="padding-left: 23px;"><input type="checkbox" value="poultry" title="Poultry" id="ms-opt-349">Poultry</label></li>
<li class=""><label for="ms-opt-350" style="padding-left: 23px;"><input type="checkbox" value="powders" title="Powders" id="ms-opt-350">Powders</label></li>
<li class=""><label for="ms-opt-351" style="padding-left: 23px;"><input type="checkbox" value="proceedings" title="Proceedings" id="ms-opt-351">Proceedings</label></li>
<li class=""><label for="ms-opt-352" style="padding-left: 23px;"><input type="checkbox" value="processes" title="Processes" id="ms-opt-352">Processes</label></li>
<li class=""><label for="ms-opt-353" style="padding-left: 23px;"><input type="checkbox" value="prosthesis" title="Prosthesis" id="ms-opt-353">Prosthesis</label></li>
<li class=""><label for="ms-opt-354" style="padding-left: 23px;"><input type="checkbox" value="proteomes" title="Proteomes" id="ms-opt-354">Proteomes</label></li>
<li class=""><label for="ms-opt-355" style="padding-left: 23px;"><input type="checkbox" value="psychiatryint" title="Psychiatry International" id="ms-opt-355">Psychiatry International</label></li>
<li class=""><label for="ms-opt-356" style="padding-left: 23px;"><input type="checkbox" value="psychoactives" title="Psychoactives" id="ms-opt-356">Psychoactives</label></li>
<li class=""><label for="ms-opt-357" style="padding-left: 23px;"><input type="checkbox" value="psycholint" title="Psychology International" id="ms-opt-357">Psychology International</label></li>
<li class=""><label for="ms-opt-358" style="padding-left: 23px;"><input type="checkbox" value="publications" title="Publications" id="ms-opt-358">Publications</label></li>
<li class=""><label for="ms-opt-359" style="padding-left: 23px;"><input type="checkbox" value="qubs" title="Quantum Beam Science" id="ms-opt-359">Quantum Beam Science</label></li>
<li class=""><label for="ms-opt-360" style="padding-left: 23px;"><input type="checkbox" value="quantumrep" title="Quantum Reports" id="ms-opt-360">Quantum Reports</label></li>
<li class=""><label for="ms-opt-361" style="padding-left: 23px;"><input type="checkbox" value="quaternary" title="Quaternary" id="ms-opt-361">Quaternary</label></li>
<li class=""><label for="ms-opt-362" style="padding-left: 23px;"><input type="checkbox" value="radiation" title="Radiation" id="ms-opt-362">Radiation</label></li>
<li class=""><label for="ms-opt-363" style="padding-left: 23px;"><input type="checkbox" value="reactions" title="Reactions" id="ms-opt-363">Reactions</label></li>
<li class=""><label for="ms-opt-364" style="padding-left: 23px;"><input type="checkbox" value="realestate" title="Real Estate" id="ms-opt-364">Real Estate</label></li>
<li class=""><label for="ms-opt-365" style="padding-left: 23px;"><input type="checkbox" value="receptors" title="Receptors" id="ms-opt-365">Receptors</label></li>
<li class=""><label for="ms-opt-366" style="padding-left: 23px;"><input type="checkbox" value="recycling" title="Recycling" id="ms-opt-366">Recycling</label></li>
<li class=""><label for="ms-opt-367" style="padding-left: 23px;"><input type="checkbox" value="religions" title="Religions" id="ms-opt-367">Religions</label></li>
<li class=""><label for="ms-opt-368" style="padding-left: 23px;"><input type="checkbox" value="remotesensing" title="Remote Sensing" id="ms-opt-368">Remote Sensing</label></li>
<li class=""><label for="ms-opt-369" style="padding-left: 23px;"><input type="checkbox" value="reports" title="Reports" id="ms-opt-369">Reports</label></li>
<li class=""><label for="ms-opt-370" style="padding-left: 23px;"><input type="checkbox" value="reprodmed" title="Reproductive Medicine" id="ms-opt-370">Reproductive Medicine</label></li>
<li class=""><label for="ms-opt-371" style="padding-left: 23px;"><input type="checkbox" value="resources" title="Resources" id="ms-opt-371">Resources</label></li>
<li class=""><label for="ms-opt-372" style="padding-left: 23px;"><input type="checkbox" value="rheumato" title="Rheumato" id="ms-opt-372">Rheumato</label></li>
<li class=""><label for="ms-opt-373" style="padding-left: 23px;"><input type="checkbox" value="risks" title="Risks" id="ms-opt-373">Risks</label></li>
<li class=""><label for="ms-opt-374" style="padding-left: 23px;"><input type="checkbox" value="robotics" title="Robotics" id="ms-opt-374">Robotics</label></li>
<li class=""><label for="ms-opt-375" style="padding-left: 23px;"><input type="checkbox" value="ruminants" title="Ruminants" id="ms-opt-375">Ruminants</label></li>
<li class=""><label for="ms-opt-376" style="padding-left: 23px;"><input type="checkbox" value="safety" title="Safety" id="ms-opt-376">Safety</label></li>
<li class=""><label for="ms-opt-377" style="padding-left: 23px;"><input type="checkbox" value="sci" title="Sci" id="ms-opt-377">Sci</label></li>
<li class=""><label for="ms-opt-378" style="padding-left: 23px;"><input type="checkbox" value="scipharm" title="Scientia Pharmaceutica" id="ms-opt-378">Scientia Pharmaceutica</label></li>
<li class=""><label for="ms-opt-379" style="padding-left: 23px;"><input type="checkbox" value="sclerosis" title="Sclerosis" id="ms-opt-379">Sclerosis</label></li>
<li class=""><label for="ms-opt-380" style="padding-left: 23px;"><input type="checkbox" value="seeds" title="Seeds" id="ms-opt-380">Seeds</label></li>
<li class=""><label for="ms-opt-381" style="padding-left: 23px;"><input type="checkbox" value="sensors" title="Sensors" id="ms-opt-381">Sensors</label></li>
<li class=""><label for="ms-opt-382" style="padding-left: 23px;"><input type="checkbox" value="separations" title="Separations" id="ms-opt-382">Separations</label></li>
<li class=""><label for="ms-opt-383" style="padding-left: 23px;"><input type="checkbox" value="sexes" title="Sexes" id="ms-opt-383">Sexes</label></li>
<li class=""><label for="ms-opt-384" style="padding-left: 23px;"><input type="checkbox" value="signals" title="Signals" id="ms-opt-384">Signals</label></li>
<li class=""><label for="ms-opt-385" style="padding-left: 23px;"><input type="checkbox" value="sinusitis" title="Sinusitis" id="ms-opt-385">Sinusitis</label></li>
<li class=""><label for="ms-opt-386" style="padding-left: 23px;"><input type="checkbox" value="smartcities" title="Smart Cities" id="ms-opt-386">Smart Cities</label></li>
<li class=""><label for="ms-opt-387" style="padding-left: 23px;"><input type="checkbox" value="socsci" title="Social Sciences" id="ms-opt-387">Social Sciences</label></li>
<li class=""><label for="ms-opt-388" style="padding-left: 23px;"><input type="checkbox" value="siuj" title="Société Internationale d’Urologie Journal" id="ms-opt-388">Société Internationale d’Urologie Journal</label></li>
<li class=""><label for="ms-opt-389" style="padding-left: 23px;"><input type="checkbox" value="societies" title="Societies" id="ms-opt-389">Societies</label></li>
<li class=""><label for="ms-opt-390" style="padding-left: 23px;"><input type="checkbox" value="software" title="Software" id="ms-opt-390">Software</label></li>
<li class=""><label for="ms-opt-391" style="padding-left: 23px;"><input type="checkbox" value="soilsystems" title="Soil Systems" id="ms-opt-391">Soil Systems</label></li>
<li class=""><label for="ms-opt-392" style="padding-left: 23px;"><input type="checkbox" value="solar" title="Solar" id="ms-opt-392">Solar</label></li>
<li class=""><label for="ms-opt-393" style="padding-left: 23px;"><input type="checkbox" value="solids" title="Solids" id="ms-opt-393">Solids</label></li>
<li class=""><label for="ms-opt-394" style="padding-left: 23px;"><input type="checkbox" value="spectroscj" title="Spectroscopy Journal" id="ms-opt-394">Spectroscopy Journal</label></li>
<li class=""><label for="ms-opt-395" style="padding-left: 23px;"><input type="checkbox" value="sports" title="Sports" id="ms-opt-395">Sports</label></li>
<li class=""><label for="ms-opt-396" style="padding-left: 23px;"><input type="checkbox" value="standards" title="Standards" id="ms-opt-396">Standards</label></li>
<li class=""><label for="ms-opt-397" style="padding-left: 23px;"><input type="checkbox" value="stats" title="Stats" id="ms-opt-397">Stats</label></li>
<li class=""><label for="ms-opt-398" style="padding-left: 23px;"><input type="checkbox" value="stresses" title="Stresses" id="ms-opt-398">Stresses</label></li>
<li class=""><label for="ms-opt-399" style="padding-left: 23px;"><input type="checkbox" value="surfaces" title="Surfaces" id="ms-opt-399">Surfaces</label></li>
<li class=""><label for="ms-opt-400" style="padding-left: 23px;"><input type="checkbox" value="surgeries" title="Surgeries" id="ms-opt-400">Surgeries</label></li>
<li class=""><label for="ms-opt-401" style="padding-left: 23px;"><input type="checkbox" value="std" title="Surgical Techniques Development" id="ms-opt-401">Surgical Techniques Development</label></li>
<li class=""><label for="ms-opt-402" style="padding-left: 23px;"><input type="checkbox" value="sustainability" title="Sustainability" id="ms-opt-402">Sustainability</label></li>
<li class=""><label for="ms-opt-403" style="padding-left: 23px;"><input type="checkbox" value="suschem" title="Sustainable Chemistry" id="ms-opt-403">Sustainable Chemistry</label></li>
<li class=""><label for="ms-opt-404" style="padding-left: 23px;"><input type="checkbox" value="symmetry" title="Symmetry" id="ms-opt-404">Symmetry</label></li>
<li class=""><label for="ms-opt-405" style="padding-left: 23px;"><input type="checkbox" value="synbio" title="SynBio" id="ms-opt-405">SynBio</label></li>
<li class=""><label for="ms-opt-406" style="padding-left: 23px;"><input type="checkbox" value="systems" title="Systems" id="ms-opt-406">Systems</label></li>
<li class=""><label for="ms-opt-407" style="padding-left: 23px;"><input type="checkbox" value="targets" title="Targets" id="ms-opt-407">Targets</label></li>
<li class=""><label for="ms-opt-408" style="padding-left: 23px;"><input type="checkbox" value="taxonomy" title="Taxonomy" id="ms-opt-408">Taxonomy</label></li>
<li class=""><label for="ms-opt-409" style="padding-left: 23px;"><input type="checkbox" value="technologies" title="Technologies" id="ms-opt-409">Technologies</label></li>
<li class=""><label for="ms-opt-410" style="padding-left: 23px;"><input type="checkbox" value="telecom" title="Telecom" id="ms-opt-410">Telecom</label></li>
<li class=""><label for="ms-opt-411" style="padding-left: 23px;"><input type="checkbox" value="textiles" title="Textiles" id="ms-opt-411">Textiles</label></li>
<li class=""><label for="ms-opt-412" style="padding-left: 23px;"><input type="checkbox" value="thalassrep" title="Thalassemia Reports" id="ms-opt-412">Thalassemia Reports</label></li>
<li class=""><label for="ms-opt-413" style="padding-left: 23px;"><input type="checkbox" value="therapeutics" title="Therapeutics" id="ms-opt-413">Therapeutics</label></li>
<li class=""><label for="ms-opt-414" style="padding-left: 23px;"><input type="checkbox" value="thermo" title="Thermo" id="ms-opt-414">Thermo</label></li>
<li class=""><label for="ms-opt-415" style="padding-left: 23px;"><input type="checkbox" value="timespace" title="Time and Space" id="ms-opt-415">Time and Space</label></li>
<li class=""><label for="ms-opt-416" style="padding-left: 23px;"><input type="checkbox" value="tomography" title="Tomography" id="ms-opt-416">Tomography</label></li>
<li class=""><label for="ms-opt-417" style="padding-left: 23px;"><input type="checkbox" value="tourismhosp" title="Tourism and Hospitality" id="ms-opt-417">Tourism and Hospitality</label></li>
<li class=""><label for="ms-opt-418" style="padding-left: 23px;"><input type="checkbox" value="toxics" title="Toxics" id="ms-opt-418">Toxics</label></li>
<li class=""><label for="ms-opt-419" style="padding-left: 23px;"><input type="checkbox" value="toxins" title="Toxins" id="ms-opt-419">Toxins</label></li>
<li class=""><label for="ms-opt-420" style="padding-left: 23px;"><input type="checkbox" value="transplantology" title="Transplantology" id="ms-opt-420">Transplantology</label></li>
<li class=""><label for="ms-opt-421" style="padding-left: 23px;"><input type="checkbox" value="traumacare" title="Trauma Care" id="ms-opt-421">Trauma Care</label></li>
<li class=""><label for="ms-opt-422" style="padding-left: 23px;"><input type="checkbox" value="higheredu" title="Trends in Higher Education" id="ms-opt-422">Trends in Higher Education</label></li>
<li class=""><label for="ms-opt-423" style="padding-left: 23px;"><input type="checkbox" value="tropicalmed" title="Tropical Medicine and Infectious Disease" id="ms-opt-423">Tropical Medicine and Infectious Disease</label></li>
<li class=""><label for="ms-opt-424" style="padding-left: 23px;"><input type="checkbox" value="universe" title="Universe" id="ms-opt-424">Universe</label></li>
<li class=""><label for="ms-opt-425" style="padding-left: 23px;"><input type="checkbox" value="urbansci" title="Urban Science" id="ms-opt-425">Urban Science</label></li>
<li class=""><label for="ms-opt-426" style="padding-left: 23px;"><input type="checkbox" value="uro" title="Uro" id="ms-opt-426">Uro</label></li>
<li class=""><label for="ms-opt-427" style="padding-left: 23px;"><input type="checkbox" value="vaccines" title="Vaccines" id="ms-opt-427">Vaccines</label></li>
<li class=""><label for="ms-opt-428" style="padding-left: 23px;"><input type="checkbox" value="vehicles" title="Vehicles" id="ms-opt-428">Vehicles</label></li>
<li class=""><label for="ms-opt-429" style="padding-left: 23px;"><input type="checkbox" value="venereology" title="Venereology" id="ms-opt-429">Venereology</label></li>
<li class=""><label for="ms-opt-430" style="padding-left: 23px;"><input type="checkbox" value="vetsci" title="Veterinary Sciences" id="ms-opt-430">Veterinary Sciences</label></li>
<li class=""><label for="ms-opt-431" style="padding-left: 23px;"><input type="checkbox" value="vibration" title="Vibration" id="ms-opt-431">Vibration</label></li>
<li class=""><label for="ms-opt-432" style="padding-left: 23px;"><input type="checkbox" value="virtualworlds" title="Virtual Worlds" id="ms-opt-432">Virtual Worlds</label></li>
<li class=""><label for="ms-opt-433" style="padding-left: 23px;"><input type="checkbox" value="viruses" title="Viruses" id="ms-opt-433">Viruses</label></li>
<li class=""><label for="ms-opt-434" style="padding-left: 23px;"><input type="checkbox" value="vision" title="Vision" id="ms-opt-434">Vision</label></li>
<li class=""><label for="ms-opt-435" style="padding-left: 23px;"><input type="checkbox" value="waste" title="Waste" id="ms-opt-435">Waste</label></li>
<li class=""><label for="ms-opt-436" style="padding-left: 23px;"><input type="checkbox" value="water" title="Water" id="ms-opt-436">Water</label></li>
<li class=""><label for="ms-opt-437" style="padding-left: 23px;"><input type="checkbox" value="wind" title="Wind" id="ms-opt-437">Wind</label></li>
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* Table of Contents
* Abstract
* Introduction
* Types of ROS
* ROS Production Locations
* ROS Plays a Significant Role in Plant–Microbe Interactions
* Plants Antioxidant Defense System
* RNS Production in Plants
* Role of RNS in Plant–Microbe Interactions
* Cross-Talk of ROS and RNS
* Role of ROS and RNS in Protein Modifications
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THE KEY ROLES OF ROS AND RNS AS A SIGNALING MOLECULE IN PLANT–MICROBE
INTERACTIONS
by
Murtaza Khan
Murtaza Khan
SciProfiles Scilit Preprints.org Google Scholar
1,†,
Sajid Ali
Sajid Ali
SciProfiles Scilit Preprints.org Google Scholar
1,†,
Tiba Nazar Ibrahim Al Azzawi
Tiba Nazar Ibrahim Al Azzawi
SciProfiles Scilit Preprints.org Google Scholar
2,†,
Saddam Saqib
Saddam Saqib
SciProfiles Scilit Preprints.org Google Scholar
3,4,
Fazal Ullah
Fazal Ullah
SciProfiles Scilit Preprints.org Google Scholar
5,
Asma Ayaz
Asma Ayaz
SciProfiles Scilit Preprints.org Google Scholar
6 and
Wajid Zaman
Wajid Zaman
SciProfiles Scilit Preprints.org Google Scholar
7,*
1
Department of Horticulture and Life Science, Yeungnam University, Gyeongsan
38541, Republic of Korea
2
Department of Applied Biosciences, Kyungpook National University, Daegu 41566,
Republic of Korea
3
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany,
Chinese Academy of Sciences, Beijing 100093, China
4
University of Chinese Academy of Sciences, Beijing 100049, China
5
State Key Laboratory of Grassland Agro-Ecosystems, School of Life Sciences,
Lanzhou University, Lanzhou 730000, China
6
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life
Sciences, Hubei University, Wuhan 430062, China
7
Department of Life Sciences, Yeungnam University, Gyeongsan 38541, Republic of
Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Antioxidants 2023, 12(2), 268; https://doi.org/10.3390/antiox12020268
Submission received: 23 November 2022 / Revised: 13 January 2023 / Accepted: 24
January 2023 / Published: 25 January 2023
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ABSTRACT
Reactive oxygen species (ROS) and reactive nitrogen species (RNS) play a pivotal
role in the dynamic cell signaling systems in plants, even under biotic and
abiotic stress conditions. Over the past two decades, various studies have
endorsed the notion that these molecules can act as intracellular and
intercellular signaling molecules at a very low concentration to control plant
growth and development, symbiotic association, and defense mechanisms in
response to biotic and abiotic stress conditions. However, the upsurge of ROS
and RNS under stressful conditions can lead to cell damage, retarded growth, and
delayed development of plants. As signaling molecules, ROS and RNS have gained
great attention from plant scientists and have been studied under different
developmental stages of plants. However, the role of RNS and RNS signaling in
plant–microbe interactions is still unknown. Different organelles of plant cells
contain the enzymes necessary for the formation of ROS and RNS as well as their
scavengers, and the spatial and temporal positions of these enzymes determine
the signaling pathways. In the present review, we aimed to report the production
of ROS and RNS, their role as signaling molecules during plant–microbe
interactions, and the antioxidant system as a balancing system in the synthesis
and elimination of these species.
Keywords:
ROS; RNS; signaling; plant–microbe interactions; antioxidant system
Graphical Abstract
1. INTRODUCTION
Due to their immobile nature, plants are constantly exposed to biotic and
abiotic stressors [1,2]. In response to these stressors, different signaling
molecules are produced in plants, including melatonin, ROS, and RNS [3,4]. ROS
and RNS are key signaling molecules and play a pivotal role in the regulation of
different processes, including plant growth and development, metabolism, and the
response to stressful (biotic and abiotic) conditions [5,6]. In plants, ROS are
produced in a variety of cellular compartments, including chloroplasts,
mitochondria, and peroxisomes [7]. In addition to causing irreversible DNA
damage and cell death, ROS are significant signaling molecules that control
healthy plant growth and responses to stress [7]. This shows that ROS have a
dual role in vivo with various levels of reactivity, generation locations, and
capabilities to penetrate biological membranes. RNS in plants were first
identified in the 1960s, but until the 1990s, they did not receive the same
level of attention as their oxygen equivalents (ROS). Among RNS, nitric oxide
(NO), acting as a signaling molecule in plant disease, rekindled interest among
researchers to understand the physiological roles of RNS in plants [8]. RNS were
initially recognized through their signaling role, in contrast to ROS, which
were first recognized as harmful chemicals and then signals [5]. The importance
of ROS and RNS as signals and significant regulators of a number of activities
in plants, such as metabolism, growth and development, and response to biotic
and abiotic stressors, is now well documented [6]. Various biotic and abiotic
stress factors, including intense light, extreme temperature, salt, drought,
waterlogging, and plant pathogens, cause the induction of ROS and RNS in plants
[9,10,11].
Broadly, ROS are divided into two classes: radicals and non-radicals [12].
Radical ROS include superoxide anions (O2−), hydroxyl radicals (−OH), alkoxyl
(RO−), hydroperoxyl (HO2−), peroxyl (ROO−), carbonate (CO3−), and semiquinone
(SQ−). Non-radical ROS include hypobromous acid (HOBr), singlet oxygen (1O2−),
ozone (O3), hydrogen peroxide (H2O2), hypoiodous acid (HOI), hypoperoxides
(ROOH), and hypochlorous acid (HOCl). It has been established that under both
normal and stressful circumstances, ROS can be formed in numerous locations,
including the cell wall, mitochondria, chloroplasts, plasma membranes,
peroxisomes, and endoplasmic reticulum. When light is present, peroxisomes and
chloroplasts are the main sources of ROS production; however, when light is
absent, mitochondria are the main source. ROS, which have been identified as the
second messenger in intracellular signaling cascades, have been correlated with
a range of plant responses, including programmed cell death, stomatal closure,
gravitropism, and the development of abiotic and biotic stress tolerance. The
activity of numerous signaling molecules, including protein phosphatases,
transcription factors, and protein kinases, can also be affected by ROS, in
addition to how they interact with other signaling molecules and regulate the
response given downstream. The quantity, potency, and size of the ROS signaling
pool is all dependent on the equilibrium between the production and the
elimination of ROS [13].
Similarly, RNS are also divided into two classes: free radicals and non-radicals
[14]. Free radical RNS include nitric oxide (NO), nitric dioxide (NO2), and
nitric oxide (NO3). Non-radical RNS include nitrous acid (HNO2), nitroxyl anion
(NO−), nitrosonium cation (NO+), peroxynitrite (NOOO−), dinitrogen tetroxide
(N2O4), and dinitrogen trioxide (N2O3). NO, a main source of RNS, is produced in
plants through numerous enzymatic and non-enzymatic mechanisms. Because the
process of NO generation in plant cells is less understood than that of ROS, it
presents one of the biggest difficulties in the research of NO as a signaling
molecule. For instance, in animals, NO is produced mostly by the action of
nitric oxide synthase (NOS), but in higher plants, NOS has not been discovered
yet. However, the proposed pathways for NO production in plants are oxidative
and reductive pathways. The substrates for NO production in oxidative pathways
are arginine, hydroxylamine, and polyamines, while the substrates for NO
production in reductive pathways are xanthine oxidoreductase (XOR), and
nitrite:NO-reductase (NiNOR) reductase. RNS are produced in different organelles
of plants, including the chloroplast, cell wall, cell membrane, mitochondria,
cytoplasm, and peroxisome [15]. Under biotic and abiotic stress situations,
plants’ nitric oxide (NO) functions as a signaling molecule in plant growth and
development [8,9].
Moreover, the recognition of a pathogen leads to “oxidative burst”, which
results in ROS and RNS generation and accumulation in higher quantities; by
triggering callose deposition, cross-linking of glycoproteins in cell walls, and
localized programmed cell death to stop the spread of infection, ROS/RNS can
directly affect the pathogen [16]. On the other hand, inoculation with
beneficial microbial flora such as plant-growth-promoting rhizobacteria (PGPR)
reduces oxidative stress via scavenging overproduced ROS, enhances the
antioxidant system of the host plant, and mitigates the adverse effects of
stressful conditions [10,17].
In this overview, we report the biosynthesis of ROS and RNS, their function as
signaling molecules during plant–microbe interactions, and the antioxidant
system’s involvement as a balancing mechanism in the synthesis and elimination
of these species. The present review covers the research gaps and basic
information regarding ROS, RNS generation, and their signaling during plant and
microbe interactions.
2. TYPES OF ROS
In general, ROS are molecules of oxygen (O2) that have undergone incomplete
activation or reduction, as well as being the main product or an O2-containing
molecule byproduct that is more reactive than ambient O2. O2 molecules’
electrons or energy transfer forms ROS. In plants, −OH, O2−, 1O2−, and H2O2 are
the most common cellular ROS. ROS are produced by cells in both radical and
non-radical forms. Radical ROS include superoxide anions (O2−), hydroxyl
radicals (−OH), alkoxyl (RO−), hydroperoxyl (HO2−), peroxyl (ROO−), carbonate
(CO3−), and semiquinone (SQ−). Non-radical ROS include hypobromous acid (HOBr),
singlet oxygen (1O2−), ozone (O3), hydrogen peroxide (H2O2), hypoiodous acid
(HOI), hypoperoxides (ROOH), and hypochlorous acid (HOCl). Each form of ROS
influences various physiological and biochemical processes in plants that are
controlled by various genes and has a distinct oxidative capacity [18].
Different kinds of ROS are shown in Figure 1A, and some of the important ROS are
discussed below.
2.1. SUPEROXIDE ANIONS (O2−)
ROS are continuously generated in the chloroplasts as a result of partial O2
reduction or energy transfer to O2. O2− is mostly produced in the
thylakoid-localized photosystem I (PSI) and other cellular compartments during
the noncyclic electron transport chain (ETC). In a typical reaction between O2
and cytochrome c oxidase, H2O is produced. O2− is occasionally created when O2
reacts with the various ETC constituents. Typically, it develops first among
ROS. O2− may undergo another reaction that could result in the production of
more ROS [19]. In an investigation by [20], it was found that O2− plays a key
role in breaking seed dormancy. These anions, together with ROS, are accountable
for the alteration of thiol groups that leads to a decrease in the total
glutathione pool, which is crucial for the mobilization of nitrogen and
carbohydrate needed for seed germination and development [21]. Furthermore, it
has been shown that O2− makes antioxidant enzymes such as catalase, peroxidases,
and pseudocatalases inactive, leaving cells open to other downstream oxidants,
such as H2O2 [22].
2.2. SINGLET OXYGEN (1O2−)
In contrast to electron transfer to O2, this ROS is created by the chlorophyll
reaction (in the antenna system, in the triplet state). Stomatal closure is
brought on by heavy metals, salt, and dryness, which results in low
intracellular CO2 concentration. The entire photosynthetic apparatus is put in
danger due to significant damage to both photosystems (PSI and PSII) and the
facilitated generation of 1O2−, which harms a variety of targets. Furthermore,
ROS also harm plant pigments, proteins, lipids, and nucleic acids, which leads
to cellular death [23]. In addition to its well-known harmful effects, 1O2−
appears to stimulate various stress responses by activating specific retrograde
signaling pathways through the oxidative alteration of carotenoids, proteins,
and lipids at sub-lethal levels [24].
2.3. HYDROGEN PEROXIDE (H2O2)
Hydrogen peroxide is produced in plant cells both naturally and in response to
biotic and abiotic stressors. Both univalent protonation and the reduction of
O2− result in the production of moderately reactive H2O2. The main sources of
H2O2 production in plant cells are the endoplasmic reticulum (ER), mitochondria,
ETC in the chloroplast, oxidation of fatty acids, photorespiration, and the cell
membrane. Low concentrations of H2O2 are beneficial to plants, but higher
concentrations are toxic. At optimum concentration inside the cell, it serves as
a regulatory signal for critical physiological processes, such senescence,
stomatal movement, photosynthesis and photorespiration, growth, and development
[25]. Furthermore, H2O2 directly kills the microbe at the infection sites,
induces cell walls’ lignification, induces phytoalexin’s production, triggers
PCD and the HR, and induces SAR [26].
2.4. HYDROXYL RADICAL (−OH)
The most reactive and harmful ROS is −OH. It is created at neutral pH levels by
the Fenton reaction of H2O2 and O2−, which is aided by transition metals such as
Fe. By inducing lipid peroxidation (LPO), protein degradation, and membrane
disintegration, it can affect a number of biological components. The excessive
accumulation of −OH leads to cellular death because there is no enzymatic
machinery able to remove this harmful radical [27]. Similar to how H2O2 was
formerly thought to be just a harmful byproduct of oxidative metabolism but is
now recognized to play signaling roles in plant cells, there is growing evidence
that the −OH radical is more than just a destructive agent. Its oxidative
capacity aids in germination, growth, stomatal closure, reproduction, the
immunological response, and stress adaption [28].
2.5. PEROXYL RADICAL (ROO−)
The primary chain propagation step in lipid peroxidation and non-lipid systems
is the creation of RO2- and RO- radicals, which can be triggered by the
heating-induced breakdown of protein and lipid peroxides or by the addition of
transition-metal ions. The oxidation of lipids, DNA damage, modifications to the
structure of proteins, and food breakdown are all significantly influenced by
the peroxyl radical [27].
2.6. ALKOXY RADICAL (RO−)
Alkoxyl radicals are produced during lipid oxidative degradation or
peroxidization without the aid of enzymes through the Fenton reaction, electron
reductions, or the fusion of two peroxyl radicals. Alkoxyl radicals can damage
DNA and trigger apoptosis since they are potent oxidizers [27].
3. ROS PRODUCTION LOCATIONS
It has been demonstrated that ROS can be created both normally and under
stressful circumstances in a variety of locations, including the mitochondria,
chloroplasts, plasma membranes, peroxisomes, endoplasmic reticulum, and cell
wall. When light is present, ROS are largely created by peroxisomes and
chloroplasts; however, when light is absent, ROS are produced by mitochondria.
3.1. CHLOROPLAST
The most prominent site of ROS synthesis is in chloroplasts, where light and
chlorophyll (chl) combine to form ROS. In chloroplasts, triplet chl and ETC,
including PSI and PSII, create ROS. In the Mehler reaction, in the PSI, SOD
changes O2− into H2O2 [29]. When O2− and H2O2 are mixed with metal ions such as
Fe2+, they produce more highly reactive −OH. Numerous environmental stresses
promote stomatal closure, which lowers CO2 levels and leads to the production of
chloroplastic ROS [30].
3.2. MITOCHONDRIA
Mitochondria are also in charge of producing harmful ROS, such as O2− and H2O2,
but on a lower scale. This is caused by the mitochondrial ETC’s (mt ETC)
abundance of energetic electrons, which can decrease O2 and generate ROS.
Complexes I and III are the two main mt ETC elements in charge of producing ROS
[31]. In addition, the mitochondrial matrix is home to a large number of
ROS-producing enzymes. In mitochondria, Mn-SOD and APX reduce O2 into H2O2. ROS
generation increases noticeably when mitochondria are under abiotic stress [32].
3.3. APOPLAST
Incoming CO2 appears to be transformed into a soluble, diffusible form that may
be carried into the cytoplasm to carry out photosynthesis via the diffusible
region surrounding the plant cell membrane. Stress signals and abscisic acid
work together to make the apoplast a prominent site for H2O2 generation under
adverse environmental conditions. Other compounds that produce ROS include
cell-wall-linked oxidases, polyamine oxidases, and pH-dependent peroxidases
(POXs) [33].
3.4. PLASMA MEMBRANES
A plasma membrane encircles each plant cell, continually interacting with the
environment to provide vital information for the cells’ survival. Dismutase is
either spontaneously transformed into H2O2 or is catalyzed by NADPH oxidase
during the transport of electrons from cytosolic NADPH to O2, and SOD creates
O2−. It is widely known that NADPH oxidase plays a crucial role in plants’
defense mechanisms against pathogenic infection and abiotic stress [34].
3.5. CELL WALL AND ENDOPLASMIC RETICULUM
Polyunsaturated fatty acid (PUFA) hydroperoxidation is produced by the
cell-wall-localized lipoxygenase (LOX), making it an active producer of reactive
oxygen species (ROS) such as O2−, −OH, 1O2, and H2O2. Using diamines or
polyamines, cell-wall-localized diamine oxidases produce ROS in the cell wall.
Recombinant lignin is produced as a result of the extensive cross-linking that
occurs during the pathogenic attack on lignin precursors via H2O2-mediated
pathways [35]. Through NADPH-mediated electron transport, Cyt P450, which is
found in the ER, produces O2−.
The total amount of ROS produced is the sum of the ROS produced in these
cellular organelles. The overproduction of ROS is known as oxidative burst, and
it may cause oxidative stress. The cites of ROS production are shown in Figure
1B.
Figure 1. (A) All types of reactive oxygen species (ROS) in plants and (B) sites
of ROS production in the plant cell.
4. ROS PLAYS A SIGNIFICANT ROLE IN PLANT–MICROBE INTERACTIONS
The development of abiotic and biotic stress tolerance in plants, programmed
cell death, stomatal closure, gravitropism, and other responses have all been
correlated with ROS, which have been identified as the second messengers in
intracellular signaling cascades [36]. Additionally, ROS can interact with
protein phosphatases, transcription factors, and protein kinases to alter their
activity. The quantity, potency, and size of the ROS signaling pool are all
dependent on the equilibrium between oxidant generation and antioxidant
clearance [34,35].
4.1. ROLE OF ROS IN PTI
Innate defense mechanisms in plants rely on plasma-membrane-localized pattern
recognition receptors (PRRs) to defend against a variety of pathogens [37].
Pattern-triggered immunity (PTI) is the result of PRRs recognizing conserved
microbial features known as pathogen-associated molecular patterns (PAMPs) [8].
Through the activation of NADPH oxidases and peroxidases caused by PAMP
perception by plants through PRRs, ROS are produced, which in turn induce
PTI-dependent basal defenses that thwart encroaching pathogens. Following the
perception of PAMP, the produced ROS act as toxic molecules to kill the
pathogens [38]. In addition to being signaling molecules, ROS also cause plant
immunological and cell death responses [39]. Therefore, pathogens must take
precautions to limit their exposure to hazardous ROS. In response to pathogens
infection, ROS are produced by the action of NADPH oxidases, also known as
respiratory burst oxidase homologs (RBOHs) [39]. The PRR-associated kinase BIK1
has been proposed to be crucial for PAMP-triggered ROS generation via
phosphorylating NADPH oxidase (RBOHD) [40]. Additionally, the Arabidopsis PTI is
significantly influenced by the apoplastic peroxidase-dependent ROS burst, which
is mediated by the detection of PAMPs [41]. The extracellular peroxidase CaPO2,
found in peppers, also produces bursts of ROS, which activate local and systemic
cell death as well as the body’s reaction to bacterial infections [42]. Systemic
acquired resistance (SAR) and PTI pathways are activated in response to
Pseudomonas syringae pv. tomato DC3000 and two common PAMPs (flagellin and
chitin), respectively, by the plant aquaporin AtPIP;4, which has been shown to
cause cytoplasmic import of apoplastic H2O2 into plant cells [43]. This shows
that aquaporins play a crucial part in the signaling of apocytoplastic ROS in
disease immune pathways.
Through the fortification of their cell walls, plants protect themselves from
invasive infections. An apoplastic H2O2 burst, cell wall cross-linking, and
callose deposition at the site of infection are all factors that aid in cell
wall fortifications [44]. For cell maturation and wall toughening during the
early phases of plant defense, effector (elicitor)-induced oxidative
cross-linking of structural proteins in plant cells is crucial [45]. Callose, a
(1,3)-b-glucan, is a key ingredient in the thickening of plant cell walls at the
sites of fungal penetration [46]. In order to improve PMR4-dependent callose
production and finally confer total penetration resistance to powdery mildew,
the Arabidopsis GTPase RabA4c physically interacts with its effector PMR4 [47].
In order to reinforce the cell wall, hydroxyproline-rich glycoproteins (HRGPs)
generate intra- and intermolecular cross-links [48]. H2O2, when exogenously
applied to peroxidase knockdown Arabidopsis lines treated with the bacterial
flagellin Flg22, restores the callose deposition-deficient phenotype [41]. This
shows that PAMP-triggered immunological responses, such as callose deposition,
depend on cell wall peroxidase-dependent H2O2 generation.
4.2. ROLE OF ROS IN ETI
Plants have developed a cell-based surveillance system that uses intracellular
nucleotide-binding leucine-rich repeat (NLR) receptors to identify certain
pathogen effectors, resulting in resistance (R) gene-mediated effector-triggered
immunity (ETI). In response to avirulent pathogens, plants overproduce ROS. A
powerful ROS burst and the HR cell death response, two essential elements of
ETI, are induced as a result of interactions between pathogen avirulence (Avr)
effectors and NLR proteins [49]. However, uncertainty exists about the
activation of HR cell death and immunological responses by NLR-mediated ROS. By
preventing the buildup of apoplastic ROS, even in the presence of the R gene,
rice resistance to incompatible rice blast fungus isolates is inhibited [50].
Although the Avr effector and cognate NLR proteins remain unaffected, cell death
and immunological responses are significantly inhibited in the absence of normal
ROS generation [50]. NLR-mediated cell death, immunity, and disease-associated
cell death are all dependent on increased ROS generation during infection
[51,52]. Although the two stages of plant immunity are spatially and temporally
separate, they are closely linked to the burst of ROS. The successful
identification of plant pathogens and the activation of plant defenses are both
characterized by ROS’s production in plant cells [44]. Furthermore, it is well
established that pathogen-induced ROS production in chloroplasts is essential
for signaling and/or carrying out hypersensitive response (HR) cell death in
plants [44]. H2O2 activates PTI and systemic acquired resistance (SAR) pathways
[44].
4.3. ROLE OF ROS IN SYMBIOTIC ASSOCIATION
Although the synthesis of ROS is mostly associated with pathogen invasion, their
production has also been noticed in other biotic interactions, such as symbiosis
between bacteria or mycorrhiza, indicating that ROS synthesis is a common
feature of different biotic interactions [39]. The previous results also
indicate that after the exposure of plants to beneficial microbes, the synthesis
of ROS is low and the level of the antioxidant system is high [53]. Therefore,
for ROS to act as signaling molecules, a proper balance between the producers
and the scavengers of ROS is crucial, and any disturbance in the equilibrium
between them can cause oxidative burst, leading to lipid peroxidation, damage to
nucleic acids and proteins, alteration of the metabolism of carbohydrates, and
eventually cell death [54].
As a summary, the role of ROS in PTI, ETI, and symbiotic association is shown in
Figure 2.
Figure 2. Schematic representation of ROS in PTI, ETI, and symbiotic
association.
Plants protect themselves from the attack of pathogens and their infection by
the activation of hypersensitive response (HR)-mediated cell death, programmed
cell death (PCD), lignin biosynthesis, PTI, ETI, expression of defense-related
genes, etc. Therefore, both ROS and RNS, as signaling molecules, significantly
induce these processes to protect themselves from the attack and infection of
pathogens. The overproduction of ROS and RNS, primarily O2−, H2O2, and NO,
during the oxidative burst may directly contribute to the killing of pathogens,
the strengthening of plant cell walls, the induction of the HR, and the
production of systemic resistance signaling [8,55]. An essential component of a
successful defense mechanism for plants against biotrophic infections feeding on
living host tissues has been thought to be the death of assaulted cells during
the HR, preceded by an oxidative burst [55,56]. Furthermore, both ROS and NO
significantly contribute to the induction of stress-related genes and PCD to
protect plants from the adverse effects of the pathogens [55,57]. For instance,
in response to different pathogens, ROS induce hypersensitive response
(HR)-mediated cell death in tobacco, programmed cell death (PCD) in barley and
Nicotiana benthamiana, expression of defense-related genes in N. benthamiana,
lignin biosynthesis and plant immunity in Arabidopsis, and PCD and the HR in
tobacco to protect these plants from the infection of pathogenic organisms
[58,59,60,61,62,63,64,65,66,67,68,69]. Interestingly, ROS also act as signaling
molecules to improve the symbiotic association of beneficial microbes with
different plants, including Medicago truncatula, Phaseolus vulgaris, and
Castanea sativa, to improve plant growth and development under normal and
stressful conditions [69,70,71].
Similarly, RNS also act as signaling molecules to induce the defense system of
plants to protect them from pathogenic attacks. For instance, in response to
different pathogens, RNS induce PTI, ETI, and SAR (different modes of plant
defense) in Arabidopsis, resistance to viral infection in rice, resistance
against tobacco mosaic virus infection in tobacco, and resistance against
powdery mildew invasion in wheat [5,8,37,72,73,74]. Interestingly, RNS such as
ROS also act as signaling molecules to improve the symbiotic association of
beneficial microbes with different plants, including Medicago truncatula, Lotus
japonicus, Medicago truncatula, and Legumes [75,76,77,78]. Furthermore, NO, in
particular, directs the development of PCD, phytoalexin accumulation, and SA
production and signaling in plants [79]. NO differentially regulates the
activity of the zinc finger proteins S-Nitrosothiols (SNO) Regulated (SRG) SRG2
and SRG3 in Arabidopsis, which are positive regulators of plant immunity [79].
The roles of ROS and RNS as signaling molecules in plant interaction with
harmful and beneficial microbes are given in Table 1.
Table 1. Roles of ROS and RNS in plant–microbe interaction.
5. PLANTS ANTIOXIDANT DEFENSE SYSTEM
ROS play a dual role in living organisms, acting as signaling molecules at
optimum concentration and toxic molecules at higher concentrations [83].
Therefore, plants have a complex and multilayered network of the antioxidative
system (AOS) to protect them from injurious ROS. The cooperation and involvement
of AOS in redox processes, which improves safety and promotes regeneration of
the active reduced forms, is particularly crucial for the existence of stressed
plants [84]. Some of the enzymatic and non-enzymatic antioxidants are discussed
below.
5.1. ENZYMATIC ANTIOXIDANTS
5.1.1. SUPEROXIDE DISMUTASE
SOD (EC 1.15.1.1) significantly reduces oxidative damage by catalyzing the quick
dismutation of O2− to lower the risk of −OH production in plants. Under stress
conditions, SOD eliminates O2− and converts it into O2 and H2O2. In a biological
system, dismutation reactions occur when oxidation and reduction events occur
simultaneously on the same reactant (in this case, O2−), ultimately resulting in
the formation of two compounds: one with a higher oxidation state (such as O2)
and another with a lower oxidation state (H2O2 in this case). This enzyme is
regarded as one of the primary enzymatic systems responsible for removing free
radicals (O2−) produced by plants under stress [85]. Through a Haber–Weiss
reaction, additional enzymes such as CAT and POX cooperate closely with SOD to
stop the production of more toxic ROS by both O2− and H2O2. In response to
drought and Pb stress, SOD activity was dramatically increased in different
cultivars of Phaseolus vulgaris and Oryza sativa [9,86]. In comparison to
spontaneous processes, SOD-catalyzed dismutation is 10,000 times faster. SOD is
present in all aerobic cells as well as oxidative-stress-sensitive subcellular
compartments. Plants have three different varieties of SOD metalloenzymes
depending on the type of metal cofactor that is present in the active center.
The most prevalent isoenzyme is Cu/Zn-SOD, which is abundant in the chloroplast
stroma, cytosol, peroxisomes, and apoplast [84]. Mn-SOD is expressed in
mitochondria and peroxisomes, the apoplast, and the cell wall, whereas Fe-SOD is
only mildly detectable in these structures. However, only the chloroplast stroma
of a few plant species can use this isoenzyme [87].
5.1.2. CATALASE AND PEROXIDASE
The most crucial enzymes in the fine regulation of ROS concentration within the
cell are catalases (CATs; EC 1.11.1.6) and peroxidases, which control the
intracellular amount of H2O2 in the cell [2]. According to reports, the CAT
enzyme exists in a variety of forms and is expressed in various plant tissues at
various developmental stages [88]. Given cellular compartmentalization, it is
possible that peroxisomes have substantial amounts of CATs, but chloroplasts do
not contain this enzyme [84]. The catalases are very efficient in the removal of
H2O2 and split two H2O2 molecules into water and oxygen. Catalase does not need
a reductant to perform its catalytic function because, in this two-step process,
H2O2 first oxidizes the iron in the CAT to produce an intermediate iron peroxide
known as compound I. However, at greater H2O2 concentrations, the second
molecule of H2O2 acts as a reductant for this intermediate chemical I, which
results in the regeneration of the enzyme and the release of water and oxygen in
the subsequent step [86]. During drought, salinity, and Pb stress, CAT’s
activity was significantly enhanced in Triticum aestivum, Cicer arietinum, and
O. sativa. Furthermore, the application of melatonin and sodium nitroprusside
(SNP) enhanced the activity of the CAT during drought and under Pb stress
[9,89].
Peroxidases (POXs; EC 1.11.1.7) are made in the endoplasmic reticulum and Golgi
apparatus, where they are then secreted into the vacuoles or extracellular
environment. Most plants use POX in its original form, which consists of a
single polypeptide with 300–350 amino acid residues and a molecular weight (MW)
of 33–55 kDa. Ascorbate and glutathione are the major components in the
antioxidant system that regulate redox homeostasis through the
Foyer–Halliwell–Asada pathway, while flavonoids, phenolic compounds, and POX act
as the second line of defense for plants in dealing with excessive H2O2 [90,91].
However, POX plays a variety of roles in the growth and development of plants.
This family of enzymes is also engaged in cell wall cross-linking, cell wall
loosening, lignification, saucerization, and auxin catabolism in addition to its
roles in the catabolism of H2O2 and redox homeostasis. By catalyzing the
oxidation of phenolic substrates with H2O2 acting as an electron acceptor, POX
removes the H2O2. MDA (mono-dehydro-ascorbyl radical), ascorbate, and DHA
(de-hydro-ascorbate) were produced as a result of subsequent reactions, as well
as the cross-linking product of phenolic compounds such as lignin or suberin. In
a recently completed study, POX from Z. mays and P. vulgaris roots were
extracted and found to be functional for cross-linking the globular protein
patatin from Solanum tuberosum. Such types of enzymatic cross-linking reactions
are important for examining protein–protein interactions. It has been discovered
that phenolic chemicals facilitate the cross-linking reaction [92]. This study
sheds light on the value of POX for comprehending the biophysical structure of
the target protein.
Together with the non-enzymatic components of the antioxidant system, the
enzymatic components provide a complex and multi-faceted protective mechanism to
maintain ROS homeostasis in order to both avoid oxidative-induced damages in
plant cells and support plant development. SOD (EC 1.15.1.1) and peroxidases
such as CAT (EC 1.11.1.6) and POX (EC 1.11.1.7) constitute the enzymatic
antioxidant components. Considering their role as ROS scavengers, variations in
their activity and/or transcript accumulation are a common feature in plants
under biotic and abiotic stresses [93].
5.2. NON-ENZYMATIC ANTIOXIDANTS
5.2.1. ASCORBIC ACID
The most prevalent AOX metabolite in plant cells is ascorbic acid (AsA), also
known as vitamin C. (Smirnoff, 2008). Ascorbate peroxidase’s (APX; EC 1.11.1.11)
activity enables it to directly interact with various ROS, neutralize the
harmful effects of O2−, −OH, and 1O2, and act as an electron donor in enzymatic
activities that decrease the amount of H2O2 [94]. Chloroplasts make up 30–40% of
a cell’s overall AsA content and are home to this water-soluble AOX, which can
accumulate to a concentration of 300mM in plant cells [95]. However, Castro et
al. [96] found that AsA, when at enhanced levels, may operate as a prooxidant in
the presence of high H2O2 levels, activating the Fenton reaction and boosting
oxidative stress in rice leaves when exposed to intense UV radiation. In terms
of its biosynthesis, L-galactono—lactone dehydrogenase (EC 1.3.2.3)—generates
AsA in the mitochondria, where it is later transferred to other organelles by
active transport or facilitated diffusion [94]. Under normal circumstances, AsA
is mostly found in its reduced form, and its pool is kept constant by the
activities of monodehydroascorbate reductase (MDHAR; EC 1.6.5.4) and DHAR [95].
Aside from that, AsA actively contributes to the regulation of mitosis, cellular
elongation, senescence, and cell death, in addition to stabilizing enzymes with
artificial metallic ions [96].
5.2.2. GLUTATHIONE
Tripeptide glutathione (GSH), a non-protein thiol, can chemically react with
O2−, −OH, and H2O2, acting as a powerful radical scavenger [94]. In addition,
during normal and stressful conditions, GSH acts as a substrate for
dehydroascorbate reductase to synthesize AsA [97]. GSH’s reducing capability
also influences protein synthesis, enzymatic control, and the expression of
genes that respond to stress [94,95]. The ratio of reduced GSH to oxidized
glutathione (GSSG) in this context is an important indicator of the redox status
of the cell. According to Gill and Tuteja [95], glutathione reductase (GR; EC
1.6.4.2) increases GSH biosynthesis and/or GSSG degradation or, alternatively,
their long-distance transport to achieve enhanced levels of GSH compared to
GSSG. According to Castro, Lima-Melo, Carvalho, Feitosa, Lima Neto, Caverzan,
Margis-Pinheiro, and Silveira [96], specific enzymes called glutamyl cysteine
ligase and glutathione synthetase synthesize glutathione in the cytosol and
chloroplasts. However, glutathione has also been found in vacuoles, the
endoplasmic reticulum, and mitochondria [96].
5.2.3. CAROTENOIDS
As one of the most prevalent naturally occurring pigments, carotenoids are
produced by both photosynthetic and non-photosynthetic organisms. They belong to
a class of lipophilic chemicals with over 700 species [98]. They can be divided
into two groups: the carotenes, which are oxygen-free carotenoids (e.g.,
β-carotene and lycopene), and the xanthophylls, which are their
oxygen-containing counterparts (e.g., lutein and zeaxanthin) [99]. These
low-molecular-weight metabolites can prevent the synthesis of 1O2 in
photosynthetic organs by quenching excited chlorophyll and triplet sensitizer,
safeguarding the photosynthetic apparatus, and lowering lipid peroxidation [96].
According to Havaux [99], because β-carotene is close to the main location of
1O2 production in chloroplasts, its oxidation can be thought of as an early
event during photo stress. As a result, metabolites from β-carotene oxidation
may serve as the primary sensors of light stress in plants. Carotenoids and
their byproducts are essential for the construction of photosystems as well as
for the regulation of developmental processes by directly regulating the
production of two plant hormones, strigolactones and abscisic acid (ABA), since
carotenoids serve as their precursors. Carotenoids also play a crucial role in
the assembly of antenna complexes as accessory pigments responsible for
absorbing light at 400 and 550 nm [93].
5.2.4. Α-TOCOPHEROLS
A unique quantity and placement of methyl groups in the 2-methyl-6-cromanol ring
distinguish the four isomers of tocopherols (α-, β-, γ-, and δ-tocopherol).
However, the most prevalent isomer is α-tocopherol, having the highest AOX
activity [100]. Tocopherols are located in plastids, plastoglobuli, and in close
proximity to the envelope and thylakoid membranes. Since it may directly
interact with 1O2, −OH, and certain lipid radicals produced by the oxidation of
polyunsaturated fatty acids, α-tocopherol is especially active in the thylakoid
membranes, where it can stop lipid peroxidation. Through an energy transfer
process, α-tocopherol can neutralize 1O2, resulting in the synthesis of various
quinones and epoxides. One of these compounds, α-tocopherol quinone,
demonstrates antioxidant characteristics similar to those of α-tocopherol and
appears to be involved in PSII energy dissipation [101].
Because quinones and other oxidized derivatives cannot be converted back into
α-tocopherol, the AOX characteristics may be compromised. Contrarily, when
α-tocopherol reacts with alkoxy or peroxyl radicals, it creates tocopheroxy
radicals, which allow the intervention of AsA, GSH, and coenzyme Q to regenerate
α-tocopherol [102]. α-tocopherol preserves the membrane’s integrity in
chloroplasts and makes these structures stiffer, which affects their fluidity
and permeability for ions and small molecules [101]. Because of the role of
α-tocopherol in membrane stability, its contribution to chloroplast redox
homeostasis, and its ability to control the concentration of some phytohormones,
such as jasmonic acid, it is assumed that α-tocopherol may interact with key
players in signal transduction pathways, indicating that tocopherol has
functions beyond its antioxidant activity [96].
5.2.5. PHENOLIC COMPOUNDS
Flavonoids, tannins, hydroxycinnamate esters, lignin, and other secondary
metabolites, collectively referred to as phenols, are found in plant tissue
[103]. The ability of phenols to act as antioxidants is due to the fact that
they have an aromatic ring structure with −OH or −OCH3 substituents, which is
excellent for trapping free radicals. Phenolic compounds directly absorb 1O2 and
prevent peroxidation of the lipid by seizing lipid alkoxy radicals [94]. The
capacity of phenols to affect the kinetics of peroxidation by changing the lipid
package and decreasing membrane fluidity is another mechanism correlated with
their antioxidant effects. These modifications may restrict free radicals’
ability to diffuse and may lessen the peroxidation process. Additionally, it has
been demonstrated that phenolic compounds may play a role in the H2O2 capture
cascade [84].
Non-enzymatic antioxidants, including AsA, GSH, α-tocopherol, phenolic
compounds, flavonoids, alkaloids, and non-protein amino acids, cooperate with
antioxidant enzymes including SOD, CAT, POX, polyphenol oxidase (PPO), APX,
MDHAR, DHAR, GR, GPX, GST, TRX, and PRX in order to control the rapid production
of ROS [104].
The efficiency and behavior of the non-enzymatic antioxidant system under stress
depend on diverse factors, such as the type of stress, time of exposure and its
intensity, plant species and their genotypes, organ or tissue, among others.
Therefore, distinct responses and outcomes from the non-enzymatic antioxidant
system have been largely reported in plants under exposure to different biotic
and abiotic stresses [93].
6. RNS PRODUCTION IN PLANTS
RNS is a collective term that includes radicals such as a nitric oxide (NO−) and
nitric dioxide (NO2−) and non-radicals such as nitrous acid (HNO2) and
dinitrogen tetroxide (N2O4) [105]. All types of RNS are shown in Figure 3A.
Among the above, the most important RNS is nitrogen oxide, which acts as a
significant signaling molecule in all living organisms and was proclaimed the
“molecule of the year” in 1992 by the journal Science. As compared to ROS, the
mechanism of NO production in plant cells is not yet fully explored, which is
one of the main obstacles in the investigation of NO as a signaling molecule. In
animals, NO is produced mostly by nitric oxide synthase (NOS). Furthermore,
though there are many reports of the role of nitric oxide synthase (NOS) in the
synthesis of NO in the extracts of different plant species, its occurrence in
higher plants has not been explored yet [106]. On the other hand, it has been
found in the unicellular alga Ostreococcus tauri [107]. The proposed pathways
for NO production are oxidative and reductive. The substrates in the oxidative
pathway for NO production are arginine, hydroxylamine, and polyamines [108]. The
reductive pathway includes the action of xanthine oxidoreductase (XOR) in the
peroxisomes and nitrite:NO-reductase (NiNOR) reductase attached to the membrane
[15]. In plants, an important source of NO production is cytosolic enzyme
nitrate reductase (NR). It has been suggested that NR plays a vital role in NO
production during bacterial defense, in the presence of other pathogens, under
drought stress, during cold acclimation, in stomatal regulation, in diminishing
the symptoms related to iron deficiency, and in the process related with the
growth of the roots [15]. The previous results also show that under normal
conditions, NR prefers to convert nitrate to nitrite, and it increases NO
production under certain conditions, such as anaerobic conditions, or at a
higher level of nitrate [109]. The pathways of NO production are shown in Figure
3B. The cell organelles involved in the production of NO are the chloroplast,
mitochondria, cytoplasm, cell wall, cell membrane, and peroxisome [15].
Furthermore, S-nitrosothioles such as S-nitrosoglutathione (GSNO) also play a
significant role in the increased NO concentration inside plants, and may act as
an NO donor [110]. The sites of NO production are shown in Figure 3C.
Figure 3. (A) All types of reactive nitrogen species (ROS) in plants, (B)
oxidative and reductive pathways, (C) sites of NO production.
7. ROLE OF RNS IN PLANT–MICROBE INTERACTIONS
The mechanisms that activate a variety of defenses, including the cross-linking
of cell wall proteins, the production of ROS and RNS, localized PCD, and the
activation of pathogenesis-related (PR) genes both at local and systemic sites,
determine a plant’s resistance to disease [8]. This system of defenses involves
unique plant receptors that can detect various signals given out by the
pathogens and guards the whole plant tissues from a wide variety of infections
[37]. NO is produced in response to potential aggressors such as viruses and
microbial pathogens during biotic stress and is involved in a variety of stress
responses. These reactions range from the control of defense genes to the
synthesis of hormones and the emergence of the hypersensitive response (HR)
[72,111]. The role of NO in PTI, ETI, and symbiotic association and the role of
GSNOR and NR in its homeostasis during plant immunity have been discussed in the
following sections in detail.
7.1. ROLE OF NO IN PTI, ETI, AND SYMBIOTIC ASSOCIATION IN PLANTS
It is suggested that plant innate immunity is a two-tiered immune system with
both PTI and ETI. Furthermore, SAR is also an important defense response of the
plants against pathogenic bacteria. In fact, it has been demonstrated that
plants produce NO quickly after being challenged by biotrophic and necrotrophic
diseases, and it is regarded as a key defense activator [56]. It is widely
acknowledged today that NO generated in response to MAMPs/PAMPs and effector
molecules from the pathogens has a significant impact on signaling pathways [6].
As a chemical messenger, after the recognition of pathogens via the interaction
between MAMPs/PAMPs and PRRs, NO significantly enhances the expression of
pathogenesis-related (PR) genes, including PR1 and PR2, and significantly
reduces pathogenic growth. It reveals that NO positively regulates plants’ basal
defense/PTI. For instance, after the inoculation of the virulent bacteria
DC3000, the expression AtPR1 and AtPR2 was more significantly enhanced in
wild-type Col-0 than in atgsnor1-3 and NO-induced mutant line atill6.
Furthermore, symptomless development of severe diseases and increased pathogenic
growth was observed in atgsnor1-3 and the NO-induced mutant line atill6 as
compared to Col-0 WT [8]. Feechan, Kwon, Yun, Wang, Pallas, and Loake [74] also
stated that S-nitrosoglutathione reductase (GSNOR) is required for basal and
R-gene-mediated resistance. NO accumulation is crucial to increase the basal
defense system of the Arabidopsis against Phytophthora parasitica infection
[112]. The same author also suggested that the loss-of-function mutant line of
GSNOR1 was deficient in SA accumulation and the signaling associated with it,
which led to its susceptibility towards infection with Phytophthora parasitica.
Furthermore, Shahid, Imran, Hussain, Khan, Lee, Mun, and Yun [72] also found
that NO-induced AtCL1 and AtCL2 positively regulated plants’ basal defense with
an increase in the transcript accumulation of AtPR genes and lower pathogenic
growth. On the other hand, Nabi, Rolly, Tayade, Khan, Shahid, and Yun [37] and
Khan, Imran, Shahid, Mun, Lee, Khan, Hussain, Lee, and Yun [56] observed that
NO-induced AtbZIP62, AtAO3, and AtNCED3 genes negatively regulated PTI
resistance against virulent bacterial infection.
Similarly, NO also significantly contributes to ETI and R-gene-mediated
resistance. Imran et al. [113] found that the NO-induced AtHMAD1 gene positively
regulated ETI and R-gene-mediated resistance. They observed higher pathogenic
growth and electrolyte leakage and lower transcript accumulation of AtPR genes
in athmad1 and atgsnor1-3 mutant lines as compared to Col-0 WT. These results
show that GSNOR is required for the induction of ETI and R-gene-mediated
resistance against a virulent bacterium (avrB). Khan, Nazar, Pande, Mun, Lee,
Hussain, Lee, and Yun [8] found similar results, and they suggested that the
NO-induced gene AtILL6 positively regulated ETI and R-gene-mediated resistance
against the infection of avrB. In contrast, the NO-induced AtAO3 and AtNCED3
genes from the ABA pathway negatively regulated plants’ ETI with decreased
transcript accumulation of AtPR genes and higher pathogenic growth in Col-0 WT
than the atbzip62, atao3, and atnced3 mutant lines. However, these NO-induced
genes positively regulated the defense system of A. thaliana plants against
drought stress [37,56].
In the past two decades, numerous studies have been conducted on the mechanisms
driving plant–microbe interaction in the rhizosphere [17]. Interaction between
plants and microbes takes place through a highly complicated communication
network that uses cutting-edge technology on both sides to identify friends and
enemies. The role of NO during recognition, root hair curling, the formation of
infection threads, nodule development, and nodule senescence is suggested by
studies on the legume–rhizobia symbiosis [5]. The interaction of plants and
mycorrhizal fungus is also thought to involve a similar role for NO. It is
interesting to note that there have been findings linking silicon to an increase
in nodules, an improvement in nitrogen fixation, and a possible interaction
between silicon and NO in mediating microbial communication underground [5].
7.2. S-NITROSYLATION OF NPR1, SAB3, PAL, AND CHS PROTEINS
According to Durrant and Dong [114], SA is a key signaling molecule in plant
immunity. The non-expresser of pathogenesis-related protein 1 (NPR1) is a
crucial transcription factor (TF) in the SA-mediated pathway. According to Mou,
et al. [115], NPR1 activity is redox-sensitive, and its oxidized oligomeric form
is found in the cytoplasm. When a pathogen infects a cell, a rise in SA causes
Cys residues to be reduced, which causes NPR1 to monomerize and quickly go to
the nucleus. Expression of the defense-related genes is enhanced in the nucleus
by NPR1’s interaction with co-transcriptional factors of the TGA family [114].
Furthermore, NPR1 is also regulated by S-nitrosation, which is controlled by NO
or GSNO concentrations. S-nitrosation induces the oligomerization of NPR1 genes
and thus helps to regulate the level of NPR1 in the cytoplasm [116]. Other
researchers, however, have demonstrated that NO facilitates NPR1 translocation
to the nucleus, where it interacts with S-nitrosylated TGA1, increasing TGA1’s
DNA-binding activity [117]. In considering these contrasting results, it has
been proposed that S-nitrosation-mediated oligomerization might not have an
inhibitory effect on NPR1 activity but may act as an earlier step to monomer
accumulation, supporting the proposition of a positive effect of NO or GSNO on
the resistance of plants to disease. Furthermore, Lindermayr, Sell, Muller,
Leister, and Durnera [117] suggest that a secondary action inducing
S-nitrosation of NPR1 might happen once this protein is already in the nucleus.
Additionally, the SA-binding protein SAB3, which acts as a positive regulator of
plant immunity, is also a target for S-nitrosation. Due to S-nitrosation, the
post-translated modified SAB3 loses its SA-binding potential and strongly
reduces its carbonic anhydrase activity, which is necessary for immune signaling
[118]. Besides this, NO also induces the expression of defense-related genes,
such as encoding phenylalanine ammonia-lyase (PAL) and chalcone synthase (CHS),
two important enzymes of the phenylpropanoid pathway required for the production
of flavonoids with antimicrobial activity. The research, which was conducted on
different plants, including potato, soybean, and wheat plants, also supported
the key role of NO in the synthesis of antimicrobial compounds in plant–pathogen
interaction [119].
7.3. ROLE OF GSNOR AND NR IN NO HOMEOSTASIS AND PLANT IMMUNITY
In response to pathogenic bacteria, NO is produced by the action of NR. This was
confirmed by using the loss-of-function of NR atnia1–atnia2 double mutant, which
showed reduced NO emissions and an impaired HR when inoculated with avirulent
bacteria or Sclerotinia sclerotiorum [120,121]. The amino acid levels in
atnia1–atnia2 mutants are also decreased; treatments with glutamine were able to
restore the WT amino acid levels but not the resistance to avirulent bacteria
[122], disproving the possibility that the plant susceptibility was caused by
problems with nitrogen metabolism. The hypothesis that NR is solely required to
generate the nitrite required for NO synthesis is supported by the fact that the
penetration of atnia1–atnia2 leaves by nitrite results in enhanced NO emissions
and activation of the HR in pathogen-challenged plants [120,123]. Furthermore,
NR-dependent NO production is also observed in response to abiotic stress
conditions and in nitrogen-fixing nodules.
According to [74,124], plants with null or reduced expression of GSNOR have
higher levels of total S-nitrosothiols (SNO), whereas plants with GSNOR
overexpression have lower levels of SNO. The modulation of intracellular SNO
levels by the GSNOR enzyme has significant ramifications for plant immunology.
According to Rustérucci, Espunya, Díaz, Chabannes, and Martínez [124], who used
an antisense approach, plants with decreased GSNOR activity (50%) displayed
improved basal resistance and improved induced SAR, whereas plants with GSNOR
overexpression displayed increased susceptibility to pathogens in comparison to
WT plants. Surprisingly, other researchers demonstrated that AtGSNOR1 null
mutants had reduced basal and pathogen-induced (gene-for-gene) resistance [74].
A striking difference between these two types of mutants was that the content of
SA, which is similarly essential for plant immunity [124,125], was not altered
in the antisense plants but was significantly decreased in GSNOR-null mutants.
Additionally, exogenous SA had no effect on GSNOR-null mutants [74,126]. If the
intricate control of NPR1 is taken into account, the seemingly conflicting
results obtained with null [74] and antisense [124] mutants might be reconciled.
As a result, Espunya, De Michele, Gómez-Cadenas, and Martínez [125] hypothesized
that decreased levels of GSNOR activity in the antisense plants might favor the
existence of the proper ratio of S-nitrosylated/NPR1/TGA1 forms, which would
have a positive impact on plant defense. GSNOR knockout mutants may completely
hinder activation of the NPR1/TGA1 signaling pathway by their inability to
prevent the overaccumulation of GSNO.
Additionally, it has been revealed that GSNOR may play a significant role in
regulating systemic defense responses during pathogenic and wound stress (Figure
4). According to Díaz, et al. [127], wounding, SA, and JA both locally and
systemically affect the transcription of the gene GSNOR. Espunya, De Michele,
Gómez-Cadenas, and Martínez [125] demonstrated that in wounded Arabidopsis
leaves, GSNO levels grew quickly and uniformly, whereas in systemic leaves, GSNO
was initially found in vascular tissues before spreading over the parenchyma.
These findings imply that GSNO participates in the movement of the wound mobile
signal across the vascular tissue. Furthermore, the alternative JA-independent
wound-signaling pathway does not use GSNO, whereas JA-dependent wound responses
need GSNO accumulation to be activated. In response to diverse abiotic stimuli,
GSNOR also modifies SNO levels, which is crucial for resistance and
acclimatization [128].
Figure 4. Proposed model of action for GSNOR and NR in NO homeostasis and plant
immunity. After the exposure to the pathogen, activation of NR at the local site
leads to accumulation of NO2−, which is reduced to NO by the mitochondrial
electron transport system. The new production of NO rapidly increases the
concentration of GSNO and other nitrosothiols; moreover, the transcriptional
inhibition of GSNOR also contributes to maintaining the enhanced GSNO pool.
8. CROSS-TALK OF ROS AND RNS
In response to biotic and abiotic stress conditions, both ROS and RNS are
produced in significant amounts and cause oxidative stress. However, at optimum
concentrations, they act as chemical messengers to regulate growth and
development and induce a defense response against these stressors. In plants,
the production of RNS and ROS is a common requirement for cells to go through
PCD. These tiny molecules can operate either alone or cooperatively [129].
Although the precise role of RNS and ROS in the process of cell death is still
unclear, the mounting evidence suggests that RNS and ROS interact significantly.
ROS and NO can control one another’s production. NO can influence the generation
of ROS during the HR by S-nitrosylating the NADPH oxidase AtRBOHD [126].
However, in the rice noe1 mutant, the loss of OsNOE1/OsCATC function causes the
accumulation of H2O2 to stimulate NO generation by increasing nitrate reductase
expression. Nitrate reductase is also crucial for the H2O2-induced death of leaf
cells through the S-nitrosylation of GAPDH and thioredoxin [130,131]. The HR,
which is characterized by fast cell death around infection sites, is a
well-researched plant PCD. Cross-talk between NO and H2O2 is a key aspect of
these tiny molecules’ activity. Additionally, RNS and ROS are crucial in
controlling the activity of target proteins. The HR procedure is under the
jurisdiction of both RNS and ROS. The balance between intracellular NO and ROS
levels is one of the major factors affecting the HR [132,133]. When a pathogen
is detected, NO builds up concurrently with an oxidative burst, which includes a
phasic synthesis of apoplastic ROS at the location of the attempted invasion
[134]. NO and H2O2 are believed to work together in this context to cause HR
cell death. For example, each of them could trigger the release of cytochrome C
from mitochondria and impact the caspase-like signaling cascade that results in
the HR [129]. Mitogen-activated protein kinases (MAPKs) and phosphatases are
some important defensive signaling cascade elements known to be impacted by ROS
and NO activity. Therefore, altering the core MAPK cascade may result in the
combination of the H2O2 and NO signaling pathways, which are triggered in
response to pathogen infection. Upon xylanase sensing in tomato cell
suspensions, cells activate a protein kinase pathway necessary for NO synthesis
as well as S-nitrosylation-dependent mechanisms that are involved in downstream
signaling, resulting in the production of polyamine and ROS [135]. It is
interesting to note that numerous proteins are both NO and H2O2 targets. For
instance, H2O2 directly targets GAPDH, which is involved in mediating ROS
signaling in plants, and NO-mediated S-nitrosylation targets it as well, which
reduces glyceraldehyde-3-phosphate dehydrogenase’s (GAPDH) activity [136].
Additionally, H2O2 inactivates methionine adenosyl transferase (MAT) in mammals
by oxidizing a Cys residue in a reversible and covalent manner. NO also targets
the same Cys residue, inducing comparable enzyme inactivation [137]. Further,
PrxII E not only reduces H2O2 and alkyl hydroperoxides [129], but also functions
in detoxifying peroxynitrite. During the defensive reaction, PrxII E undergoes
S-nitrosylation, which controls the antioxidant function of this important
enzyme and may be related to the HR [129]. The ability of ozone (O3) to cause
HR-like cell death makes it a powerful instrument for inducing ROS-activated
responses. This suggests that NO is a key signaling molecule in response to O3
exposure because NO accumulation occurred prior to buildup of ET, JA, SA, and
leaf damage [138,139]. Contrary to its intended role in the HR, NO can also
scavenge H2O2 and, in some situations, shield plant cells from harm [140,141].
Both wounding- or JA-induced expression of defense genes and wounding-induced
H2O2 production are impacted by NO donors [142]. GSNOR1 in Arabidopsis is a
significant regulator that indirectly regulates the levels of protein
S-nitrosylation on a global scale. Increased levels of total cellular NO and SNO
were caused by loss-of-function mutations in GSNOR1, which also impaired
resistance (R) gene-mediated defense and hindered basal defensive mechanisms
[74,143]. Additionally, the mutant atgsnor1-3 showed altered thermotolerance and
resistance to paraquat (1,1′-dimethyl-4,4′-bipyridinium dichloride), a chemical
that causes the generation of superoxide and H2O2 in the leaves of the WT [129].
These findings are supported by the fact that WT plants treated with an NO donor
showed paraquat resistance [144]. These investigations demonstrated that the
Arabidopsis GSNOR1/HOT5/PAR-2 gene controls cell death by acting downstream of
superoxide, in addition to regulating SA signaling and thermotolerance. It is
interesting to note that the HR was potentiated in atgsnor1-3 plants by higher
levels of SNOs even in the absence of apoplastic ROS production and the cell
death agonist SA. Unexpectedly, NO S-nitrosylation of the NADPH oxidase,
AtRBOHD, at Cys890, reduces its capacity to produce ROS. Additionally, this
cysteine is preferentially S-nitrosylated in both human and fly NADPH oxidases,
indicating that this mechanism may control immunological responses in both
plants and animals [126]. In order to further manage the onset of cell death
processes, NO may therefore regulate the formation of ROS through protein
S-nitrosylation. Together, these results shed light on the processes underlying
ROS and RNS function in plants and reveal that the ROS/RNS pathway in plant PCD
is extremely complicated is at least partially regulated by cross-talk with a
number of phytohormone signaling networks [129].
Other types of plant cell death are also described in some papers as involving
NO and ROS interplay. Aleurone layer PCD caused by gibberellin (GA) in barley is
mediated by ROS, while NO is a protective antioxidant [129]. While delaying this
PCD process, NO donors do not impair the overall metabolism or the GA-induced
production and release of alpha-amylase. In aleurone layers treated with GA, the
levels of CAT and SOD are significantly decreased. In the presence of NO donors,
treatment with GA slows the depletion of CAT and SOD. Consequently, NO may act
as an endogenous PCD modulator in barley aleurone cells [140]. NO may
potentially support PCD brought on by ROS. Self-incompatibility (SI) causes
relatively quick and temporary increases in ROS and NO during pollen–pistil
interactions. Since ROS/NO scavengers reduced the development of SI-induced
actin punctate foci and the activation of a DEVDase/caspase-3-like activity,
both of these effects were reduced [145]. Sphinganine, or dihydrosphingosine
(d18:0, DHS), induces calcium-dependent PCD and causes H2O2 generation via
activating NADPH oxidase in tobacco BY-2 cells (s). It also encourages the
synthesis of NO, which is necessary to trigger cell death [146]. By encouraging
MPK6-mediated caspase-3-like activation, NO accumulated in Cd-induced PCD and
aided Cd-induced PCD in Arabidopsis [147]. Therefore, the many functions of RNS
in PCD and their interactions with ROS rely on the type of plant, the
environment it grows in, and its redox state.
9. ROLE OF ROS AND RNS IN PROTEIN MODIFICATIONS
Protein oxidation is described as the covalent alteration, a significant class
of post-translational modification, of a protein brought on either directly by
interactions with ROS or indirectly by conjugation with breakdown products of
fatty acid peroxidation. Nitrosylation, carbonylation, disulfide bond formation,
and glutathionylation are all examples of direct modifications that affect a
protein’s activity [94]. The amino acids arginine, histidine, lysine, proline,
threonine, and tryptophan are preferentially targeted by indirect modifications
of proteins, which increases the vulnerability of proteins to proteolytic
disintegration [95]. Since thiol groups and S-containing amino acids, such as
Met and Cys, are more likely to be attacked by ROS and are particularly
susceptible to oxidation, they are the most often changed amino acids [94]. Cys
residues can have a H atom removed by active oxygen, creating a thiyl radical
that then bonds with another thiyl radical to create a disulfide bridge [148].
Sulfenic acid, sulfinic acid, and sulfonic acid derivatives can also be produced
by the oxidation of protein Cys thiol groups [149]. However, Met can also be
subjected to ROS-mediated oxidation, just as Cys. Protein Met residues undergo
oxidation to form methionine-S- and methionine-R-sulfoxides [149]. Methionine
sulfoxide reductase, a group of cytosolic and plastidic enzymes involved in
reducing oxidative damage, quickly reduces the oxidized Met residues back to Met
[93]. However, superoxide radical irreversibly inactivates enzymes that contain
Fe-S centers, resulting in enzyme inactivation [150].
Proteins that have been permanently inactivated cannot be restored; instead,
they must be identified and removed by cellular proteolytic processes [94].
These removal and degradation processes are crucial for the preservation of
cellular metabolism. By preparing for ubiquitination and becoming a target for
proteasome destruction, it has been proposed that oxidized proteins are better
substrates for proteolytic digestion [151]. The most frequent oxidative protein
modification, carbonylation, is an irreversible alteration of proteins that has
a detrimental effect on the structure and functionality of proteins that are
involved in channels, enzymes, and receptors [150]. The cytoplasm, chloroplasts,
peroxisomes, nucleus, and mitochondria of plant cells have all been reported to
have carbonylated proteins. According to Bartoli, et al. [152], wheat leaves had
a larger concentration of carbonylated proteins per mg of protein in the
mitochondria than in the chloroplasts and peroxisomes, which may indicate that
mitochondrial proteins are more vulnerable to oxidative damage. The
carbonylation of proteins is caused by both biotic and abiotic stresses, such as
heat, salinity, drought, and heavy metals. However, the degree of carbonylation
is correlated with the stressor factor’s severity and exposure period [153].
NO mediates its redox functions primarily through S-nitrosation/nitrosylation,
which is the addition of an NO moiety to a Cys sulfhydryl/thiol to form an SNO.
It has been demonstrated that this redox-based alteration controls plants’
immunity, development, and responses to the environment. According to newly
available data, NO orchestrates some of these processes by controlling the use
of various PTMs [154]. The small ubiquitin-like modifier (SUMO), which is
attached covalently to target proteins, is emerging as a crucial regulator of
eukaryotic immunological activity. In plants, it has been suggested that
SUMO1/2-dependent mechanisms regulate the activation of host immunity [155].
S-nitrosation has recently been shown to have a significant role in the
regulation of SUMOylation [156]. Increasing NO levels were shown to cause
S-nitrosation of the Arabidopsis SUMO E2 enzyme SCE1 at Cys139 after a
pathogen-triggered nitrosative burst. Therefore, the accumulation of SUMO1/2
conjugates, impaired immunological responses, and increased vulnerability to
pathogens were caused by the mutation of Cys139 [156]. Taking these results
together, it was determined that S-nitrosation of SCE1 at Cys139 allows NO
bioactivity to increase immunological activation by reducing SUMO1/2-mediated
repression.
According to newly available information, NO plays a significant role in
regulating phosphorylation-dependent signaling cascades. NO buildup has been
shown to activate protein kinases (PKs) and cause the phosphorylation of several
proteins involved in a variety of cellular activities [157]. Ca2+-dependent PKs
(CDPKs), sucrose nonfermenting 1-related PKs (SnRKs), mitogen-activated PKs
(MAPKs), and phosphoinositide-dependent PKs are examples of NO-dependent PKs
(PDKs). However, it is still unknown how NO modifies the activity of these
target PKs. By releasing cytosolic free Ca2+, NO is hypothesized to indirectly
mediate the activation of MAPKs and CDPKs [158]. But it is still unknown what
subtle mechanisms underlie this process. SnRKs, MAPKs, and CDPKs have not been
reported to undergo direct S-nitrosation [159]. However, it was shown that
S-nitrosation of a crucial catalytic Cys residue decreased the action of tomato
cell death regulator PDK1. Additionally, preliminary results suggest that
tyrosine nitration may be used to regulate the activity of MAPKs [160]. In fact,
the dual phosphorylation of the Thr-X-Tyr motif in the activation loop by MAPK
kinases (MAPKKs) causes MAPKs to become active. Consequently, it is tempting to
hypothesize that nitration of the Tyr residue inside the activation loop may
prevent it from being phosphorylated by MAPKKs and, as a result, negatively
affect MAPK activity. Finally, NO may affect phosphorylated PK and
phosphorylated proteins more generally by redox-regulating protein phosphatases
(PPs). Major phosphatases, particularly tyrosine phosphatases, are impacted by
this process, which is well known in mammals [161].
In eukaryotic species, the chromatin structure is extremely dynamic and changes
during growth and development as well as in response to environmental cues.
Histone protein modification triggers chromatin remodeling to regulate
transcription, replication, recombination, and repair [162]. These processes
depend on the modification of histone acetylation or methylation, which is
catalyzed by enzymes called histone acetyltransferases/histone deacetylases
(HDAs) and methyltransferases/demethylases, respectively [154]. NO has recently
been shown to influence histone acetylation by inhibiting histone deacetylase
(HDA) complexes [163]. NO-regulated histone acetylation of genes essential to
immunity, abiotic stress, and chloroplast function was discovered via
genome-wide NO-dependent H3K9/14ac profiling in Arabidopsis seedlings,
indicating that NO bioactivity may regulate gene expression by modulating
chromatin structure [163]. Furthermore, it has been demonstrated that NO buildup
causes worldwide DNA hypomethylation, which changes the expression of
chromatin-remodeling enzymes [164]. This suggests that NO indirectly affects
plant chromatin methylation processes. The current facts collectively imply that
NO bioactivity might play significant functions in the nucleus, but further
research into the molecular specifics is still needed.
10. CONCLUSIONS AND FUTURE PROSPECTS
It is widely understood that ROS and RNS play a key role as signaling molecules
in plant growth and development under normal, biotic, and abiotic stress
conditions. However, the beginning of ROS and RNS signaling, the detection and
response mechanisms, and how the balance between the synthesis and removal of
these species is managed are all areas in which much remains to be discovered.
Although recent approaches such as RNA-seq and proteomics have enabled
discoveries of new TFs and protein–protein interaction that support cellular ROS
and RNS signaling in plants, fundamental knowledge about ROS and RNS synthesis
and their activities inside the plant is still needed. There is still little
information about the role of ROS and RNS in the initiation of the signaling
network, the mechanism required for the perception and specificity of the
general signals, and the regulation between the production and elimination of
ROS and RNS in plants. However, advanced microscopy techniques and in vivo
optical manipulation of intracellular structures are providing new windows into
the synthesis and activities of ROS and RNS inside the plant. Understanding how
the various metabolic pathways regulate the production and elimination of both
ROS and RNS, the post-translational modifications mediated by ROS and RNS, and
their signaling role in different physiological and metabolic processes and
responses to biotic and abiotic stresses in plants should constitute the major
objectives of ROS and RNS research going forward.
In this review, we discussed the vital role of ROS and RNS as key signaling
molecules in plant–microbe interactions and the antioxidant system as a
regulator in the synthesis and elimination of these species. Both ROS and RNS,
as significant signaling molecules, have gained great fame amongst plant
scientists in the last few decades, opening new windows into many aspects of
plant physiology and metabolism, both under normal and harsh environmental
conditions. Our understanding of the role of both ROS and RNS in the defense
mechanism as signaling molecules is still relatively poor, and we still need
some basic information about the enzymatic sources involved in the production of
ROS and RNS in plant–microbe interactions. The attempts of many scientists to
unveil the signaling role and sources of synthesis of ROS and RNS during
plant–microbe interactions have been quite successful, and various reports from
previous research indicate that antioxidants, NR, and GSNOR are important
regulators of these processes. Hence, recognition and a description of the role
of ROS and RNS in synthesizing enzymes during plant–microbe interactions as well
as that of genes contributing to ROS and RNS signaling during the HR is
necessary. To achieve these goals, genetic screening is being investigated as an
interesting approach. Additionally, a functional genomics study is necessary to
understand the mechanism and role of ROS and RNS in plant–microbe interactions.
AUTHOR CONTRIBUTIONS
Conceptualization, methodology, formal analysis, M.K., T.N.I.A.A. and S.A.;
software, W.Z. and A.A.; validation, A.A., F.U. and S.S.; investigation, W.Z.;
resources, S.A.; data curation, A.A. and F.U.; writing—original draft
preparation, M.K., S.A. and W.Z.; writing—review and editing, W.Z., T.N.I.A.A.,
A.A. and S.S.; visualization, S.A., M.K. and W.Z.; supervision, project
administration W.Z. All authors have read and agreed to the published version of
the manuscript.
FUNDING
This research received no external funding.
CONFLICTS OF INTEREST
The authors declare no conflict of interest.
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Figure 1. (A) All types of reactive oxygen species (ROS) in plants and (B) sites
of ROS production in the plant cell.
Figure 2. Schematic representation of ROS in PTI, ETI, and symbiotic
association.
Figure 3. (A) All types of reactive nitrogen species (ROS) in plants, (B)
oxidative and reductive pathways, (C) sites of NO production.
Figure 4. Proposed model of action for GSNOR and NR in NO homeostasis and plant
immunity. After the exposure to the pathogen, activation of NR at the local site
leads to accumulation of NO2−, which is reduced to NO by the mitochondrial
electron transport system. The new production of NO rapidly increases the
concentration of GSNO and other nitrosothiols; moreover, the transcriptional
inhibition of GSNOR also contributes to maintaining the enhanced GSNO pool.
Table 1. Roles of ROS and RNS in plant–microbe interaction.
PlantROS/RNSEffectsReferencesSand pearH2O2 HR-mediated cell
death[80]ArabidopsisH2O2Programmed cell death (PCD)[81] Nicotiana benthamianaSOA
and H2O2Replication of two unrelated RNA viruses[63]ArabidopsisROS- and
JA-dependent processLignin biosynthesis[64]ArabidopsisOxidative
burstPTI[65]ArabidopsisRBOHDPlant immunity[66]TobaccoH2O2PCD and
HR[67,68]Medicago truncatulaROSSymbiosis[69]Phaseolus
vulgarisROSSymbiosis[70]Castanea sativaROSSymbiosis[71]ArabidopsisNOPlant
immunity[8,37,72]ArabidopsisNOPlant immunity, growth, and many
more[5,6,57]ArabidopsisNOPlant immunity[37]Rice NOResistance to viral
infection[73]TobacoNOResistance against tobacco mosaic
virus[82]WheatSNOResistance against powdery mildew invasion[74]Medicago
truncatulaNOSymbiosis[75]Lotus japonicusNOSymbiosis[76]Medicago
truncatulaNOSymbiosis[77]LegumesNOSymbiosis[78]
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Khan, M.; Ali, S.; Al Azzawi, T.N.I.; Saqib, S.; Ullah, F.; Ayaz, A.; Zaman, W.
The Key Roles of ROS and RNS as a Signaling Molecule in Plant–Microbe
Interactions. Antioxidants 2023, 12, 268. https://doi.org/10.3390/antiox12020268
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Khan M, Ali S, Al Azzawi TNI, Saqib S, Ullah F, Ayaz A, Zaman W. The Key Roles
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Khan, M.; Ali, S.; Al Azzawi, T.N.I.; Saqib, S.; Ullah, F.; Ayaz, A.; Zaman, W.
The Key Roles of ROS and RNS as a Signaling Molecule in Plant–Microbe
Interactions. Antioxidants 2023, 12, 268. https://doi.org/10.3390/antiox12020268
AMA Style
Khan M, Ali S, Al Azzawi TNI, Saqib S, Ullah F, Ayaz A, Zaman W. The Key Roles
of ROS and RNS as a Signaling Molecule in Plant–Microbe Interactions.
Antioxidants. 2023; 12(2):268. https://doi.org/10.3390/antiox12020268
Chicago/Turabian Style
Khan, Murtaza, Sajid Ali, Tiba Nazar Ibrahim Al Azzawi, Saddam Saqib, Fazal
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Signaling Molecule in Plant–Microbe Interactions" Antioxidants 12, no. 2: 268.
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