Stress-induced reactive oxygen species compartmentalization, perception and signalling
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
R35 GM136402
NIGMS NIH HHS - United States
PubMed
33846592
PubMed Central
PMC8751180
DOI
10.1038/s41477-021-00887-0
PII: 10.1038/s41477-021-00887-0
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis enzymologie fyziologie MeSH
- fyziologický stres * MeSH
- reaktivní formy kyslíku metabolismus MeSH
- signální transdukce * MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- reaktivní formy kyslíku MeSH
Reactive oxygen species (ROS) are essential for life and are involved in the regulation of almost all biological processes. ROS production is critical for plant development, response to abiotic stresses and immune responses. Here, we focus on recent discoveries in ROS biology emphasizing abiotic and biotic stress responses. Recent advancements have resulted in the identification of one of the first sensors for extracellular ROS and highlighted waves of ROS production during stress signalling in Arabidopsis. Enzymes that produce ROS, including NADPH oxidases, exhibit precise regulation through diverse post-translational modifications. Discoveries highlight the importance of both amino- and carboxy-terminal regulation of NADPH oxidases through protein phosphorylation and cysteine oxidation. Here, we discuss advancements in ROS compartmentalization, systemic ROS waves, ROS sensing and post-translational modification of ROS-producing enzymes and identify areas where foundational gaps remain.
Department of Plant Pathology University of California Davis Davis CA USA
Ritsumeikan Global Innovation Research Organization Ritsumeikan University Kusatsu Japan
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Mhamdi A, Van Breusegem F. Reactive oxygen species in plant development. Development 145, (2018). PubMed
Mittler R ROS Are Good. Trends Plant Sci 22, 11–19 (2017). PubMed
Dietz KJ, Turkan I, Krieger-Liszkay A. Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast. Plant Physiol 171, 1541–1550 (2016). PubMed PMC
Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH. The Roles of Mitochondrial Reactive Oxygen Species in Cellular Signaling and Stress Response in Plants. Plant Physiol 171, 1551–1559 (2016). PubMed PMC
Sandalio LM, Romero-Puertas MC. Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann Bot 116, 475–485 (2015). PubMed PMC
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y. Mechanisms of ROS Regulation of Plant Development and Stress Responses. Front Plant Sci 10, 800 (2019). PubMed PMC
Zhao C, Zhang H, Song C, Zhu J-K, Shabala S. Mechanisms of Plant Responses and Adaptation to Soil Salinity. The Innovation 1, 100017 (2020). PubMed PMC
El-Shetehy M, Wang C, Shine MB, Yu K, Kachroo A, Kachroo P. Nitric oxide and reactive oxygen species are required for systemic acquired resistance in plants. Plant Signal Behav 10, e998544 (2015). PubMed PMC
Schmidt R, Kunkowska AB, Schippers JH. Role of Reactive Oxygen Species during Cell Expansion in Leaves. Plant Physiol 172, 2098–2106 (2016). PubMed PMC
Kaya H, et al. Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26, 1069–1080 (2014). PubMed PMC
Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241–1244 (2008). PubMed
Mangano S, et al. Molecular link between auxin and ROS-mediated polar growth. Proc Natl Acad Sci U S A 114, 5289–5294 (2017). PubMed PMC
Lee Y, Rubio MC, Alassimone J, Geldner N. A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412 (2013). PubMed
Cheval C, et al. Chitin perception in plasmodesmata characterizes submembrane immune-signaling specificity in plants. Proc Natl Acad Sci U S A 117, 9621–9629 (2020). PubMed PMC
Han JP, et al. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca. New Phytol 221, 1935–1949 (2019). PubMed
Smirnoff N, Arnaud D. Hydrogen peroxide metabolism and functions in plants. New Phytol 221, 1197–1214 (2019). PubMed
Waszczak C, Carmody M, Kangasjärvi J. Reactive Oxygen Species in Plant Signaling. Annu Rev Plant Biol 69, 209–236 (2018). PubMed
Kadota Y, Shirasu K, Zipfel C. Regulation of the NADPH Oxidase RBOHD During Plant Immunity. Plant Cell Physiol 56, 1472–1480 (2015). PubMed
Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J. Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21, 1422–1441 (2014). PubMed PMC
Willems P, et al. The ROS Wheel: Refining ROS Transcriptional Footprints. Plant Physiol 171, 1720–1733 (2016). PubMed PMC
Mielecki J, Gawroński P, Karpiński S. Retrograde Signaling: Understanding the Communication between Organelles. Int J Mol Sci 21, (2020). PubMed PMC
Ng S, et al. A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25, 3450–3471 (2013). PubMed PMC
Shapiguzov A, et al. Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors. Elife 8, (2019). PubMed PMC
Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ. Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond. Annu Rev Plant Biol 67, 25–53 (2016). PubMed
op den Camp RG, et al. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320–2332 (2003). PubMed PMC
Daudi A, et al. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24, 275–287 (2012). PubMed PMC
Fujita S, et al. SCHENGEN receptor module drives localized ROS production and lignification in plant roots. EMBO J 39, e103894 (2020). PubMed PMC
Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T. Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78, 94–106 (2014). PubMed
Müller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol 184, 885–897 (2009). PubMed
Lolle S, Stevens D, Coaker G. Plant NLR-triggered immunity: from receptor activation to downstream signaling. Curr Opin Immunol 62, 99–105 (2020). PubMed PMC
O’Brien JA, et al. A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiol 158, 2013–2027 (2012). PubMed PMC
Wang C, et al. Pipecolic acid confers systemic immunity by regulating free radicals. Sci Adv 4, eaar4509–eaar4509 (2018). PubMed PMC
Li X, et al. Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress. Front Plant Sci 6, 463 (2015). PubMed PMC
Wong HL, et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19, 4022–4034 (2007). PubMed PMC
Tian S, et al. Plant Aquaporin AtPIP1;4 Links Apoplastic H2O2 Induction to Disease Immunity Pathways. Plant Physiol 171, 1635–1650 (2016). PubMed PMC
Bienert GP, Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1840, 1596–1604 (2014). PubMed
Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C. Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation. Plant Cell 27, 1945–1954 (2015). PubMed PMC
Möller MN, Cuevasanta E, Orrico F, Lopez AC, Thomson L, Denicola A. Diffusion and Transport of Reactive Species Across Cell Membranes. Adv Exp Med Biol 1127, 3–19 (2019). PubMed
Lynch RE, Fridovich I. Permeation of the erythrocyte stroma by superoxide radical. J Biol Chem 253, 4697–4699 (1978). PubMed
Reithmeier RA, Casey JR, Kalli AC, Sansom MS, Alguel Y, Iwata S. Band 3, the human red cell chloride/bicarbonate anion exchanger (AE1, SLC4A1), in a structural context. Biochim Biophys Acta 1858, 1507–1532 (2016). PubMed
de Rezende FF, et al. Integrin α7β1 is a redox-regulated target of hydrogen peroxide in vascular smooth muscle cell adhesion. Free Radic Biol Med 53, 521–531 (2012). PubMed
Noctor G, Foyer CH. Intracellular Redox Compartmentation and ROS-Related Communication in Regulation and Signaling. Plant Physiol 171, 1581–1592 (2016). PubMed PMC
Bononi A, et al. Mitochondria-associated membranes (MAMs) as hotspot Ca(2+) signaling units. Adv Exp Med Biol 740, 411–437 (2012). PubMed
Hancock JT. Considerations of the importance of redox state for reactive nitrogen species action. J Exp Bot 70, 4323–4331 (2019). PubMed
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction.) (1997).
Dikalov SI, Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal 20, 372–382 (2014). PubMed PMC
Kauffman ME, et al. MitoSOX-Based Flow Cytometry for Detecting Mitochondrial ROS. React Oxyg Species (Apex) 2, 361–370 (2016). PubMed PMC
Fichman Y, Miller G, Mittler R. Whole-Plant Live Imaging of Reactive Oxygen Species. Molecular Plant 12, 1203–1210 (2019). PubMed
Nietzel T, et al. The fluorescent protein sensor roGFP2-Orp1 monitors in vivo H. New Phytol 221, 1649–1664 (2019). PubMed
Fichman Y, Mittler R. Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades? Plant J 102, 887–896 (2020). PubMed
Gilroy S, et al. ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants. Plant Physiol 171, 1606–1615 (2016). PubMed PMC
Wu F, et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581 (2020). PubMed
Cheval C, Faulkner C. Plasmodesmal regulation during plant-pathogen interactions. New Phytol 217, 62–67 (2018). PubMed
Mittler R, Blumwald E. The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27, 64–70 (2015). PubMed PMC
Zandalinas SI, Fichman Y, Mittler R. Vascular Bundles Mediate Systemic Reactive Oxygen Signaling during Light Stress. The Plant Cell 32, 3425–3435 (2020). PubMed PMC
Chen YC, et al. -hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in. Proc Natl Acad Sci U S A 115, E4920–E4929 (2018). PubMed PMC
Návarová H, Bernsdorff F, Döring AC, Zeier J. Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24, 5123–5141 (2012). PubMed PMC
Wu J, et al. Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species. Cell Research 25, 621–633 (2015). PubMed PMC
Gilroy S, et al. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19, 623–630 (2014). PubMed
Yuan M, et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. bioRxiv, 2020.2004.2010.031294 (2020). PubMed PMC
McConnell EW, et al. Proteome-Wide Analysis of Cysteine Reactivity during Effector-Triggered Immunity. Plant Physiology 179, 1248–1264 (2019). PubMed PMC
Ngou BPM, Ahn H-K, Ding P, Jones JDG. Mutual Potentiation of Plant Immunity by Cell-surface and Intracellular Receptors. bioRxiv, 2020.2004.2010.034173 (2020). PubMed
Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51, 941–954 (2007). PubMed
Rossi FR, Krapp AR, Bisaro F, Maiale SJ, Pieckenstain FL, Carrillo N. Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J 92, 761–773 (2017). PubMed
Zurbriggen MD, et al. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J 60, 962–973 (2009). PubMed
Moreau M, et al. The Arabidopsis oligopeptidases TOP1 and TOP2 are salicylic acid targets that modulate SA-mediated signaling and the immune response. Plant J 76, 603–614 (2013). PubMed
Westlake TJ, Ricci WA, Popescu GV, Popescu SC. Dimerization and thiol sensitivity of the salicylic acid binding thimet oligopeptidases TOP1 and TOP2 define their functions in redox-sensitive cellular pathways. Frontiers in Plant Sciences 6, 327 (2015). PubMed PMC
Kimura S, Waszczak C, Hunter K, Wrzaczek M. Bound by Fate: The Role of Reactive Oxygen Species in Receptor-Like Kinase Signaling. Plant Cell 29, 638–654 (2017). PubMed PMC
Akter S, et al. Cysteines under ROS attack in plants: a proteomics view. J Exp Bot 66, 2935–2944 (2015). PubMed
Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F. Oxidative post-translational modifications of cysteine residues in plant signal transduction. J Exp Bot 66, 2923–2934 (2015). PubMed
Jacques S, et al. Protein Methionine Sulfoxide Dynamics in Arabidopsis thaliana under Oxidative Stress. Mol Cell Proteomics 14, 1217–1229 (2015). PubMed PMC
Jacques S, Ghesquière B, Van Breusegem F, Gevaert K. Plant proteins under oxidative attack. Proteomics 13, 932–940 (2013). PubMed
Felle HH. pH: Signal and Messenger in Plant Cells. Plant Biology 3, 577–591 (2001).
Geilfus CM. The pH of the Apoplast: Dynamic Factor with Functional Impact Under Stress. Mol Plant 10, 1371–1386 (2017). PubMed
Wojtkowiak JW, Verduzco D, Schramm KJ, Gillies RJ. Drug resistance and cellular adaptation to tumor acidic pH microenvironment. Mol Pharm 8, 2032–2038 (2011). PubMed PMC
Toledano MB, Kullik I, Trinh F, Baird PT, Schneider TD, Storz G. Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78, 897–909 (1994). PubMed
Gaudu P, Moon N, Weiss B. Regulation of the soxRS oxidative stress regulon reversible oxidation of the Fe-S centers of SoxR in vivo. Journal of Biological Chemistry 272, 5082–5086 (1997). PubMed
Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471–481 (2002). PubMed
Miao Y, et al. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18, 2749–2766 (2006). PubMed PMC
Ding Y, Sun T, Ao K, Peng Y, Zhang Y, Li X. Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity. Cell 173, 1454–1467.e1415 (2018). PubMed
Dong X NPR1, all things considered. Curr Opin Plant Biol 7, 547–552 (2004). PubMed
Mou Z, Fan W, Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935–944 (2003). PubMed
Tada Y, et al. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952–956 (2008). PubMed PMC
Kinkema M, Fan W, Dong X. Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12, 2339–2350 (2000). PubMed PMC
Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P. Plant cytoplasmic GAPDH: redox post-translational modifications and moonlighting properties. Front Plant Sci 4, 450 (2013). PubMed PMC
Hancock JT, et al. Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. Plant Physiol Biochem 43, 828–835 (2005). PubMed
Schneider M, Knuesting J, Birkholz O, Heinisch JJ, Scheibe R. Cytosolic GAPDH as a redox-dependent regulator of energy metabolism. BMC Plant Biol 18, 184 (2018). PubMed PMC
Uraji M, et al. Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 159, 450–460 (2012). PubMed PMC
Bourdais G, et al. Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress. PLoS Genet 11, e1005373 (2015). PubMed PMC
Kimura S, et al. CRK2 and C-terminal Phosphorylation of NADPH Oxidase RBOHD Regulate Reactive Oxygen Species Production in Arabidopsis. Plant Cell 32, 1063–1080 (2020). PubMed PMC
Vaattovaara A, et al. Mechanistic insights into the evolution of DUF26-containing proteins in land plants. Commun Biol 2, 56 (2019). PubMed PMC
Tian W, et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572, 131–135 (2019). PubMed
Byrne DP, et al. Aurora A regulation by reversible cysteine oxidation reveals evolutionarily conserved redox control of Ser/Thr protein kinase activity. Sci Signal 13, (2020). PubMed
Behring JB, et al. Spatial and temporal alterations in protein structure by EGF regulate cryptic cysteine oxidation. Science Signaling 13, eaay7315 (2020). PubMed PMC
Zhang T, Zhu M, Song WY, Harmon AC, Chen S. Oxidation and phosphorylation of MAP kinase 4 cause protein aggregation. Biochim Biophys Acta 1854, 156–165 (2015). PubMed
Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97, 2940–2945 (2000). PubMed PMC
Xie G, Sasaki K, Imai R, Xie D. A redox-sensitive cysteine residue regulates the kinase activities of OsMPK3 and OsMPK6 in vitro. Plant Sci 227, 69–75 (2014). PubMed
Ueoka-Nakanishi H, Sazuka T, Nakanishi Y, Maeshima M, Mori H, Hisabori T. Thioredoxin h regulates calcium dependent protein kinases in plasma membranes. FEBS J 280, 3220–3231 (2013). PubMed
Kaya H, et al. Comparative analysis of the reactive oxygen species-producing enzymatic activity of Arabidopsis NADPH oxidases. The Plant Journal 98, 291–300 (2019). PubMed
Pandey D, Gratton JP, Rafikov R, Black SM, Fulton DJ. Calcium/calmodulin-dependent kinase II mediates the phosphorylation and activation of NADPH oxidase 5. Mol Pharmacol 80, 407–415 (2011). PubMed PMC
Streller S, Krömer S, Wingsle G. Isolation and purification of mitochondrial Mn-superoxide dismutase from the gymnosperm Pinus sylvestris L. Plant Cell Physiol 35, 859–867 (1994). PubMed
Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341 (2002). PubMed
Winterbourn CC, Parsons-Mair HN, Gebicki S, Gebicki JM, Davies MJ. Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides. Biochem J 381, 241–248 (2004). PubMed PMC
Zhang Y, et al. Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21, 2357–2377 (2009). PubMed PMC
Hu CH, et al. NADPH Oxidases: The Vital Performers and Center Hubs during Plant Growth and Signaling. Cells 9, (2020). PubMed PMC
Morales J, Kadota Y, Zipfel C, Molina A, Torres MA. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J Exp Bot 67, 1663–1676 (2016). PubMed
Chen D, et al. Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture. Nat Commun 8, 2265 (2017). PubMed PMC
Kadota Y, et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54, 43–55 (2014). PubMed
Li L, et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329–338 (2014). PubMed
Dubiella U, et al. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proceedings of the National Academy of Sciences 110, 8744–8749 (2013). PubMed PMC
Gao X, et al. Bifurcation of Arabidopsis NLR immune signaling via Ca 2+-dependent protein kinases. PLoS Pathog 9, e1003127 (2013). PubMed PMC
Zhang M, et al. The MAP4 Kinase SIK1 Ensures Robust Extracellular ROS Burst and Antibacterial Immunity in Plants. Cell Host Microbe 24, 379–391.e375 (2018). PubMed PMC
Kadota Y, et al. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol 221, 2160–2175 (2019). PubMed PMC
Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proc Natl Acad Sci U S A 112, 12211–12216 (2015). PubMed PMC
Fernando V, Zheng X, Walia Y, Sharma V, Letson J, Furuta S. S-Nitrosylation: An Emerging Paradigm of Redox Signaling. Antioxidants (Basel) 8, (2019). PubMed PMC
Heinrich TA, da Silva RS, Miranda KM, Switzer CH, Wink DA, Fukuto JM. Biological nitric oxide signalling: chemistry and terminology. Br J Pharmacol 169, 1417–1429 (2013). PubMed PMC
Astier J, Gross I, Durner J. Nitric oxide production in plants: an update. Journal of Experimental Botany 69, 3401–3411 (2017). PubMed
Gupta KJ, et al. Recommendations on terminology and experimental best practice associated with plant nitric oxide research. New Phytol 225, 1828–1834 (2020). PubMed
Lindermayr C, Durner J. S-Nitrosylation in plants: pattern and function. J Proteomics 73, 1–9 (2009). PubMed
Yun BW, et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264–268 (2011). PubMed
Beaumel S, et al. Down-regulation of NOX2 activity in phagocytes mediated by ATM-kinase dependent phosphorylation. Free Radic Biol Med 113, 1–15 (2017). PubMed PMC
Qian J, et al. Nitric oxide reduces NADPH oxidase 5 (Nox5) activity by reversible S-nitrosylation. Free Radic Biol Med 52, 1806–1819 (2012). PubMed PMC
Shen J, et al. Persulfidation-based Modification of Cysteine Desulfhydrase and the NADPH Oxidase RBOHD Controls Guard Cell Abscisic Acid Signaling. Plant Cell 32, 1000–1017 (2020). PubMed PMC
Lee D, et al. Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nat Commun 11, 1838 (2020). PubMed PMC
Swatek KN, Komander D. Ubiquitin modifications. Cell Res 26, 399–422 (2016). PubMed PMC
Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 67, 425–479 (1998). PubMed
Mithoe SC, Menke FL. Regulation of pattern recognition receptor signalling by phosphorylation and ubiquitination. Curr Opin Plant Biol 45, 162–170 (2018). PubMed
Lu D, et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332, 1439–1442 (2011). PubMed PMC
Ma X, et al. Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581, 199–203 (2020). PubMed PMC
Liao D, et al. Arabidopsis E3 ubiquitin ligase PLANT U-BOX13 (PUB13) regulates chitin receptor LYSIN MOTIF RECEPTOR KINASE5 (LYK5) protein abundance. New Phytol 214, 1646–1656 (2017). PubMed
Li QY, Li P, Myint Phyu Sin Htwe N, Shangguan KK, Liang Y. Antepenultimate residue at the C-terminus of NADPH oxidase RBOHD is critical for its function in the production of reactive oxygen species in Arabidopsis. J Zhejiang Univ Sci B 20, 713–727 (2019). PubMed PMC
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