Nitric oxide (NO) emerged as a key signal molecule in plants. During the last two decades impressive progress has been made in plant NO research. This small, redox-active molecule is now known to play an important role in plant immunity, stress responses, environmental interactions, plant growth and development. To more accurately and robustly establish the full spectrum of NO bioactivity in plants, it will be essential to apply methodological best practice. In addition, there are some instances of conflicting nomenclature within the field, which would benefit from standardization. In this context, we attempt to provide some helpful guidance for best practice associated with NO research and also suggestions for the cognate terminology.

Agroécologie AgroSup Dijon CNRS INRA Université Bourgogne Franche Comté 21000 Dijon France

Department of Applied Sciences University of the West of England Bristol BS16 1QY UK

Department of Biochemistry and Cell and Molecular Biology of Plants Estación Experimental del Zaidín Consejo Superior de Investigaciones Científicas Granada Spain

Department of Biochemistry Faculty of Science Palacký University Šlechtitelů 27 CZ 783 71 Olomouc Czech Republic

Department of Plant Biology University of Szeged Szeged 6726 Hungary

Group of Biochemistry and Cell Signalling in Nitric Oxide Department of Experimental Biology Centre for Advanced Studies in Olive Grove and Olive Oils Faculty of Experimental Sciences University of Jaén Campus Universitario 'Las Lagunillas' s n 23071 Jaén Spain

INRA CNRS Institut Sophia Agrobiotech Université Côte d'Azur 06903 Sophia Antipolis Cedex France

Institute of Biochemical Plant Pathology Helmholtz Zentrum München German Research Centre for Environmental Health München Neuherberg 85764 Germany

Institute of Molecular Plant Sciences School of Biological Sciences University of Edinburgh Edinburgh EH9 3JH UK

National Institute of Plant Genome Research Aruna Asaf Ali Marg 110067 New Delhi India

Zobrazit více v PubMed

Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kosmala A. 2011. Are nitric oxide donors a valuable tool to study the functional role of nitric oxide in plant metabolism? Plant Biology 13: 747-756.

Arita NO, Cohen M, Tokuda G, Yamasaki H. 2006. Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. In: Lamattina L, Polacco JC, eds. Nitric oxide in plant growth, development and stress physiology. Berlin, Germany: Springer, 269-280.

Balcerczyk A, Soszynski M, Bartosz G. 2005. On the specificity of 4-amino-5-methylamino-2′, 7′-difluorofluorescein as a probe for nitric oxide. Free Radical Biology and Medicine 39: 327-335.

Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL. 2002. Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiology 129: 1642-1650.

Besson-Bard A, Griveau S, Bedioui F, Wendehenne D. 2008. Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses. Journal of Experimental Botany 59: 3407-3414.

Bethke PC, Libourel IG, Reinöhl V, Jones RL. 2006. Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223: 805-812.

Calvo-Begueria L, Rubio MC, Martínez JI, Pérez-Rontomé C, Delgado MJ, Bedmar EJ, Becana M. 2018. Redefining nitric oxide production in legume nodules through complementary insights from electron paramagnetic resonance spectroscopy and specific fluorescent probes. Journal of Experimental Botany 69: 3703-3714.

Cao BJ, Reith ME. 2002. Nitric oxide scavenger carboxy-PTIO potentiates the inhibition of dopamine uptake by nitric oxide donors. European Journal of Pharmacology 448: 27-30.

Caro A, Puntarulo S. 1999. Nitric oxide generation by soybean embryonic axes. Possible effect on mitochondrial function. Free Radical Research 31: 205-212.

Chamizo-Ampudia A, Sanz-Luque E, Llamas A, Galvan A, Fernandez E. 2017. Nitrate reductase regulates plant nitric oxide homeostasis. Trends in Plant Science 22: 163-174.

Corpas FJ, Barroso JB. 2017. Nitric oxide synthase-like activity in higher plants. Nitric Oxide: Biology and Chemistry 68: 5.

Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM et al. 2004. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology 136: 2722-2733.

Corpas FJ, del Río LA, Barroso JB. 2007. Need of biomarkers of nitrosative stress in plants. Trends in Plant Science 12: 436-438.

Corpas FJ, Palma JM, Del Río LA, Barroso JB. 2009. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytologist 184: 9-14.

D'Alessandro S, Posocco B, Costa A, Zahariou G, Schiavo FL, Carbonera D, Zottini M. 2013. Limits in the use of cPTIO as nitric oxide scavenger and EPR probe in plant cells and seedlings. Frontiers in Plant Science 4: 340.

Del Castello F, Nejamkin A, Cassia R, Correa-Aragunde N, Fernández B, Foresi N, Lombardo C, Ramirez L, Lamattina L. 2019. The era of nitric oxide in plant biology: twenty years tying up loose ends. Nitric Oxide 85: 17-27.

Deng M, Moureaux T, Caboche M. 1989. Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiology 91: 304-309.

Denicola A, Souza JM, Radi R. 1998. Diffusion of peroxynitrite across erythrocyte membranes. Proceedings of the National Academy of Sciences, USA 95: 3566-3571.

Düppe PM, Talbierski PM, Hornig FS, Rauen U, Korth HG, Wille T, Boese R, Omlor T, de Groot H, Sustmann R. 2010. Pyrene-based Fluorescent Nitric Oxide Cheletropic Traps (FNOCTs) for the detection of nitric oxide in cell cultures and tissues. Chemistry - A European Journal 16: 11121-11132.

Ederli L, Reale L, Madeo L, Ferranti F, Gehring C, Fornaciari M, Romano B, Pasqualini S. 2009. NO release by nitric oxide donors in vitro and in planta. Plant Physiology and Biochemistry 47: 42-48.

Eroglu E, Gottschalk B, Charoensin S, Blass S, Bischof H, Rost R, Madreiter-Sokolowski CT, Pelzmann B, Bernhart E, Sattler W et al. 2016. Development of novel FP-based probes for live-cell imaging of nitric oxide dynamics. Nature Communications 7: 10623.

Fedorova M, Bollineni RC, Hoffmann R. 2014. Protein carbonylation as a major hallmark of oxidative damage: update of analytical strategies. Mass Spectrometry Reviews 33: 79-97.

Floryszak-Wieczorek J, Milczarek G, Arasimowicz M, Ciszewski A. 2006. Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224: 1363-1372.

Ford PC. 2010. Reactions of NO and nitrite with heme models and proteins. Inorganic Chemistry 49: 6226-6239.

Ford PC, Fernandez BO, Lim MD. 2005. Mechanisms of reductive nitrosylation in iron and copper models relevant to biological systems. Chemical Reviews 105: 2439-2456.

Gardner PR, Gardner AM, Martin LA, Salzman AL. 1998. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proceedings of the National Academy of Sciences, USA 95: 10378-11038.

Goldstein S, Russo A, Samuni A. 2003. Reactions of PTIO and carboxy-PTIO with ·NO,·NO2, and O2˙−. Journal of Biological Chemistry 278: 50949-50955.

Griveau S, Besson-Bard A, Bedioui F, Wendehenne D. 2016. Electrochemical detection of nitric oxide in plant cell suspensions. In: Gupta K, ed. Plant nitric oxide. New York, NY, USA: Humana Press, 127-137.

Gupta KJ, Igamberdiev AU. 2013. Recommendations of using at least two different methods for measuring NO. Frontiers in Plant Science 4: 58.

Heinrich TA, Da Silva RS, Miranda KM, Switzer CH, Wink DA, Fukuto JM. 2013. Biological nitric oxide signalling: chemistry and terminology. British Journal of Pharmacology 169: 1417-1429.

Hill R, Hargrove M, Arredondo-Peter R. 2016. Phytoglobin: a novel nomenclature for plant globins accepted by the globin community at the 2014 XVIII conference on oxygen-binding and sensing proteins. F1000Research 5: 212.

Hill RD. 2012. Non-symbiotic haemoglobins-what's happening beyond nitric oxide scavenging? AoB Plants 2012: pls004.

Hu J, Huang X, Chen L, Sun X, Lu C, Zhang L, Wang Y, Zuo J. 2015. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiology 167: 1731-1746.

Jasid S, Simontacchi M, Bartoli CG, Puntarulo S. 2006. Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiology 142: 1246-1255.

Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GK, Wendehenne D. 2016. Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Science Signaling 9: re2.

Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ, Ischiropoulos H. 2012. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radical Biology Medicine 52: 1-6.

Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH. 2014. Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Molecular Cell 56: 153-162.

Kojima H, Hirotani M, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, Hirata Y, Nagano T. 2001. Bioimaging of nitric oxide with fluorescent indicators based on the rhodamine chromophore. Analytical Chemistry 73: 1967-1973.

Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JV, Snowman AM, Law L, Hester LD, Snyder SH. 2010. GAPDH mediates nitrosylation of nuclear proteins. Nature Cell Biology 12: 1094.

Li H, Wan A. 2015. Fluorescent probes for real-time measurement of nitric oxide in living cells. Analyst 140: 7129-7141.

Lim MH, Xu D, Lippard SJ. 2006. Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nature Chemical Biology 2: 375.

Maskall CS, Gibson JF, Dart PJ. 1977. Electron-paramagnetic-resonance studies of leghaemoglobins from soya-bean and cowpea root nodules. Identification of nitrosyl-leghaemoglobin in crude leghaemoglobin preparations. Biochemical Journal 167: 435-445.

Mur LA, Mandon J, Cristescu SM, Harren FJ, Prats E. 2011. Methods of nitric oxide detection in plants: a commentary. Plant Science 181: 509-519.

Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ. 2013. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5: pls052.

Murgia I, de Pinto MC, Delledonne M, Soave C, De Gara L. 2004. Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells. Journal of Plant Physiology 161: 777-783.

Palma JM, Ruiz C, Corpas FJ. 2018. A simple and useful method to apply exogenous NO gas to plant systems: bell pepper fruits as a model. In: Mengel A, Lindermayr C, eds. Nitric oxide: methods and protocols. New York, NY, USA: Humana Press, 3-11.

Peterson DA, Peterson DC, Archer S, Weir EK. 1992. The non specificity of specific nitric oxide synthase inhibitors. Biochemical and Biophysical Research Communications 187: 797-801.

Planchet E, Kaiser WM. 2006. Nitric oxide production in plants: facts and fictions. Plant Signaling & Behavior 1: 46-51.

Planchet E, Sonoda M, Zeier J, Kaiser WM. 2006. Nitric oxide (NO) as an intermediate in the cryptogein-induced hypersensitive response - a critical re-evaluation. Plant, Cell & Environment 29: 59-69.

Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S. 2012. Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant, Cell & Environment 35: 1483-1499.

Reisser D, Onier-Cherix N, Jeannin JF. 2002. Arginase activity is inhibited by L-NAME, both in vitro and in vivo. Journal of Enzyme Inhibition and Medicinal Chemistry 17: 267-270.

Rubio MC, Calvo-Begueria L, Diaz-Mendoza M, Elhiti M, Moore M, Matamoros MA, James EK, Diaz I, Perez-Rontome C, Villar I et al. 2019. Phytoglobins in the nuclei, cytoplasm, and chloroplasts modulate nitric oxide signaling and interact with abscisic acid. The Plant Journal 100: 38-54.

Seth D, Hess DT, Hausladen A, Wang L, Wang YJ, Stamler JS. 2018. A multiplex enzymatic machinery for cellular protein S-nitrosylation. Molecular Cell 69: 451-464.

Shishido SM, de Oliveira MG. 2001. Photosensitivity of aqueous sodium nitroprusside solutions: nitric oxide release versus cyanide toxicity. Progress in Reaction Kinetics and Mechanism 26: 239-261.

Singh N, Bhatla SC. 2019. Hemoglobin as a probe for estimation of nitric oxide emission from plant tissues. Plant Methods 5: 39.

Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB. 2007. Nitrosative stress in plants. FEBS Letters 58: 453-461.

Vishwakarma A, Wany A, Pandey S, Bulle M, Kumari A, Kishorekumar R, Igamberdiev AU, Mur LA, Gupta KJ. 2019. Current approaches to measure nitric oxide in plants. Journal of Experimental Botany 70: 4333-4343.

Vitecek J, Reinohl V, Jones RL. 2008. Measuring NO production by plant tissues and suspension cultured cells. Molecular Plant 1: 270-284.

Wu C, Parrott AM, Fu C, Liu T, Marino SM, Gladyshev VN, Jain MR, Baykal AT, Li Q, Oka S et al. 2011. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxidants & Redox Signaling 15: 2565-2604.

Xiong J, Fu G, Yang Y, Zhu C, Tao L. 2012. Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? Journal of Experimental Botany 63: 33-41.

Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH et al. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264.

Progress in Plant Nitric Oxide Studies: Implications for Phytopathology and Plant Protection

Stress-induced reactive oxygen species compartmentalization, perception and signalling