Skip to main content
Log in

Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Reactive oxygen species (ROS) are constantly produced in plants, as the metabolic by-products or as the signaling components in stress responses. High levels of ROS are harmful to plants. In contrast, ROS play important roles in plant physiology, including abiotic and biotic tolerance, development, and cellular signaling. Therefore, ROS production needs to be tightly regulated to balance their function. Respiratory burst oxidase homologue (RBOH) proteins, also known as plant nicotinamide adenine dinucleotide phosphate oxidases, are well studied enzymatic ROS-generating systems in plants. The regulatory mechanisms of RBOH-dependent ROS production in stress responses have been intensively studied. This has greatly advanced our knowledge of the mechanisms that regulate plant ROS production. This review attempts to integrate the regulatory mechanisms of RBOHD-dependent ROS production by discussing the recent advance. AtRBOHD-dependent ROS production could provide a valuable reference for studying ROS production in plant stress responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

BIK1:

Botrytis-induced kinase 1

CPK:

Calcium-dependent protein kinase

DAMPs:

Damage-associated molecular patterns

EFR:

EF-Tu receptor

ETI:

Effector triggered immunity

FAD:

Flavin adenine dinucleotide

FLS2:

Flagellin-sensing 2

GFP:

Green fluorescent protein

MAPK or MPK:

Mitogen-activated protein kinase

NADPH:

Nicotinamide adenine dinucleotide phosphate

PAMPs:

Pathogen-associated molecular patterns

PEPRs:

PEP receptors

PRRs:

Pattern recognition receptors

PTI:

PAMP triggered immunity

RBOH:

Respiratory burst oxidase homologue

ROS:

Reactive oxygen species

SAA:

Systemic acquired acclimation

SAR:

Systemic acquired resistance

References

  • Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27:2645–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson JC, Bartels S, Gonzalez Besteiro MA, Shahollari B, Ulm R, Peck SC (2011) Arabidopsis MAP kinase phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant J 67:258–268

    Article  CAS  PubMed  Google Scholar 

  • Aranda-Sicilia MN, Trusov Y, Maruta N, Chakravorty D, Zhang Y, Botella JR (2015) Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. J Plant Physiol 188:44–48

    Article  CAS  PubMed  Google Scholar 

  • Astier J, Kulik A, Koen E, Besson-Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D (2012) Protein S-nitrosylation: what’s going on in plants? Free Radic Biol Med 53:1101–1110

    Article  CAS  PubMed  Google Scholar 

  • Ben Rejeb K, Benzarti M, Debez A, Bailly C, Savoure A, Abdelly C (2015a) NADPH oxidase-dependent H2O2 production is required for salt-induced antioxidant defense in Arabidopsis thaliana. J Plant Physiol 174:5–15

    Article  CAS  PubMed  Google Scholar 

  • Ben Rejeb K, Lefebvre-De Vos D, Le Disquet I, Leprince AS, Bordenave M, Maldiney R, Jdey A, Abdelly C, Savoure A (2015b) Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol 208:1138–1148

    Article  CAS  PubMed  Google Scholar 

  • Benschop JJ, Mohammed S, O’Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214

    Article  CAS  PubMed  Google Scholar 

  • Berriri S, Garcia AV, Freidit Frey N, Rozhon W, Pateyron S, Leonhardt N, Montillet JL, Leung J, Hirt H, Colcombet J (2012) Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. Plant Cell 24:4281–4293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berrocal-Lobo M, Stone S, Yang X, Antico J, Callis J, Ramonell KM, Somerville S (2010) ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin- and NADPH oxidase-mediated defense responses. PLoS One 5:e14426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  CAS  PubMed  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  PubMed  Google Scholar 

  • Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502–14507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  CAS  PubMed  Google Scholar 

  • Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111:6497–6502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110:8744–8749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fagard M, Dellagi A, Roux C, Perino C, Rigault M, Boucher V, Shevchik VE, Expert D (2007) Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. Mol Plant Microbe Interact 20:794–805

    Article  CAS  PubMed  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng F, Yang F, Rong W, Wu X, Zhang J, Chen S, He C, Zhou JM (2012) A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–118

    Article  CAS  PubMed  Google Scholar 

  • Flury P, Klauser D, Schulze B, Boller T, Bartels S (2013) The anticipation of danger: microbe-associated molecular pattern perception enhances AtPep-triggered oxidative burst. Plant Physiol 161:2023–2035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 148:1695–1706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galletti R, Ferrari S, De Lorenzo G (2011) Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiol 157:804–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, Li L, Cheng C, McCormack M, Sheen J, Shan L, He P (2013) Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog 9:e1003127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamann T, Bennett M, Mansfield J, Somerville C (2009) Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J 57:1015–1026

    Article  CAS  PubMed  Google Scholar 

  • Hao LH, Wang WX, Chen C, Wang YF, Liu T, Li X, Shang ZL (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein alpha subunit and reactive oxygen species. Mol Plant 5:852–864

    Article  CAS  PubMed  Google Scholar 

  • Hao H, Fan L, Chen T, Li R, Li X, He Q, Botella MA, Lin J (2014) Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26:1729–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hettenhausen C, Schuman MC, Wu J (2015) MAPK signaling: a key element in plant defense response to insects. Insect Sci 22:157–164

    Article  CAS  PubMed  Google Scholar 

  • Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J, Mott R, Smith JA, Harberd NP (2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31:4359–4370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JD, Shirasu K, Menke F, Jones A, Zipfel C (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M, Kuchitsu K (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405

    Article  CAS  PubMed  Google Scholar 

  • Klauser D, Flury P, Boller T, Bartels S (2013) Several MAMPs, including chitin fragments, enhance AtPep-triggered oxidative burst independently of wounding. Plant Signal Behav 8(9):e25346

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong Q, Qu N, Gao M, Zhang Z, Ding X, Yang F, Li Y, Dong OX, Chen S, Li X, Zhang Y (2012) The MEKK1–MKK1/MKK2–MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24:2225–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) 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

    Article  CAS  PubMed  Google Scholar 

  • Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhao-Hui C, Batoux M, Nekrasov V, Roux M, Chinchilla D, Zipfel C, Jones JD (2009) Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc Natl Acad Sci USA 106:15973–15978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–338

    Article  CAS  PubMed  Google Scholar 

  • Liu Y (2012) Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep 31:1–12

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Kong X, Pan J, Li D (2010) VIP1: linking Agrobacterium-mediated transformation to plant immunity? Plant Cell Rep 29:805–812

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Ding P, Sun T, Nitta Y, Dong O, Huang X, Yang W, Li X, Botella JR, Zhang Y (2013a) Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol 161:2146–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wang L, Zhang D, Li D (2013b) Expression analysis of segmentally duplicated ZmMPK3-1 and ZmMPK3-2 genes in maize. Plant Mol Biol Rep 31:457–463

    Article  CAS  Google Scholar 

  • Liu Y, Zhang D, Wang L, Li D (2013c) Genome-wide analysis of mitogen-activated protein kinase gene family in maize. Plant Mol Biol Rep 31:1446–1460

    Article  CAS  Google Scholar 

  • Liu Z, Wu Y, Yang F, Zhang Y, Chen S, Xie Q, Tian X, Zhou JM (2013d) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci USA 110:6205–6210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorek J, Griebel T, Jones AM, Kuhn H, Panstruga R (2013) The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity. Mol Plant Microbe Interact 26:991–1003

    Article  CAS  PubMed  Google Scholar 

  • Lozano-Duran R, Bourdais G, He SY, Robatzek S (2014) The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol 202:259–269

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Tintor N, Mentzel T, Kombrink E, Boller T, Robatzek S, Schulze-Lefert P, Saijo Y (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci USA 106:22522–22527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact 24:183–193

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Zhao Y, Walker RK, Berkowitz GA (2013) Molecular steps in the immune signaling pathway evoked by plant elicitor peptides: Ca2+-dependent protein kinases, nitric oxide, and reactive oxygen species are downstream from the early Ca2+ signal. Plant Physiol 163:1459–1471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macho AP, Boutrot F, Rathjen JP, Zipfel C (2012) ASPARTATE OXIDASE plays an important role in Arabidopsis stomatal immunity. Plant Physiol 159:1845–1856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  CAS  PubMed  Google Scholar 

  • Maruta T, Inoue T, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2011) Arabidopsis NADPH oxidases, AtrbohD and AtrbohF, are essential for jasmonic acid-induced expression of genes regulated by MYC2 transcription factor. Plant Sci 180:655–660

    Article  CAS  PubMed  Google Scholar 

  • Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR (2015) Membrane-localized extra-large G proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 167:1004–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mersmann S, Bourdais G, Rietz S, Robatzek S (2010) Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45

    PubMed  Google Scholar 

  • Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  CAS  Google Scholar 

  • Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T, Zipfel C (2014) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605–615

    Article  CAS  PubMed  Google Scholar 

  • Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, Lacombe S, Rougon A, Bittel P, Kiss-Papp M, Chinchilla D, van Esse HP, Jorda L, Schwessinger B, Nicaise V, Thomma BP, Molina A, Jones JD, Zipfel C (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J 28:3428–3438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitta Y, Ding P, Zhang Y (2015) Heterotrimeric G proteins in plant defense against pathogens and ABA signaling. Environ Exp Bot 114:153–158

    Article  CAS  Google Scholar 

  • Nuhse TS, Bottrill AR, Jones AM, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892

    Article  CAS  PubMed  Google Scholar 

  • Pastor V, Luna E, Ton J, Cerezo M, Garcia-Agustin P, Flors V (2013) Fine tuning of reactive oxygen species homeostasis regulates primed immune responses in Arabidopsis. Mol Plant Microbe Interact 26:1334–1344

    Article  CAS  PubMed  Google Scholar 

  • Peer M, Bach M, Mueller MJ, Waller F (2011) Free sphingobases induce RBOHD-dependent reactive oxygen species production in Arabidopsis leaves. FEBS Lett 585:3006–3010

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Hirt H (2006) Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol 141:351–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pogany M, von Rad U, Grun S, Dongo A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J (2009) Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an ArabidopsisAlternaria pathosystem. Plant Physiol 151:1459–1475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poovaiah CR, Nageswara-Rao M, Soneji JR, Baxter HL, Stewart CN Jr (2014) Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks. Plant Biotechnol J 12:1163–1173

    Article  CAS  PubMed  Google Scholar 

  • Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68:100–113

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, Haweker H, Dong X, Robatzek S, Schulze-Lefert P (2009) Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J 28:3439–3449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto H, Matsuda O, Iba K (2008) ITN1, a novel gene encoding an ankyrin-repeat protein that affects the ABA-mediated production of reactive oxygen species and is involved in salt-stress tolerance in Arabidopsis thaliana. Plant J 56:411–422

    Article  CAS  PubMed  Google Scholar 

  • Sewelam N, Kazan K, Thomas-Hall SR, Kidd BN, Manners JM, Schenk PM (2013) Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS One 8:e70289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  CAS  PubMed  Google Scholar 

  • Smith JM, Heese A (2014) Rapid bioassay to measure early reactive oxygen species production in Arabidopsis leave tissue in response to living Pseudomonas syringae. Plant Methods 10:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song CJ, Steinebrunner I, Wang X, Stout SC, Roux SJ (2006) Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis. Plant Physiol 140:1222–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, Shulaev V, Mittler R (2013) Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553–3569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi F, Mizoguchi T, Yoshida R, Ichimura K, Shinozaki K (2011) Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol Cell 41:649–660

    Article  CAS  PubMed  Google Scholar 

  • Tateda C, Zhang Z, Shrestha J, Jelenska J, Chinchilla D, Greenberg JT (2014) Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26:4171–4187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Morales J, Sanchez-Rodriguez C, Molina A, Dangl JL (2013) Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Mol Plant Microbe Interact 26:686–694

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Du Y, Zhao X, Miao Y, Song CP (2013) The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol 161:1392–1408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Guo Y, Jia L, Chu H, Zhou S, Chen K, Wu D, Zhao L (2014) Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol 164:2184–2196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wrzaczek M, Brosche M, Kangasjarvi J (2013) ROS signaling loops—production, perception, regulation. Curr Opin Plant Biol 16:575–582

    Article  CAS  PubMed  Google Scholar 

  • Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292

    Article  CAS  PubMed  Google Scholar 

  • Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26:2007–2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S (2014) A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant J 77:222–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C-Y, Hong C-P (2015) The NADPH oxidase Rboh D is involved in primary hypoxia signalling and modulates expression of hypoxia-inducible genes under hypoxic stress. Environ Exp Bot 115:63–72

    Article  CAS  Google Scholar 

  • Yi SY, Shirasu K, Moon JS, Lee SG, Kwon SY (2014) The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PLoS One 9:e88951

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang A, Zhang J, Ye N, Cao J, Tan M, Zhang J, Jiang M (2010) ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroid-induced antioxidant defence in leaves of maize. J Exp Bot 61:4399–4411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work in our laboratory is supported by the Nation Natural Science Foundation of China (Nos. 31360166, 31360184, and 31560198) and the China Scholarship Council (No. 201408530515). We thank Prof. Neal Stewart for comments on the manuscript. We thank the anonymous reviewers for their careful reading of our manuscript and their many insightful comments and suggestions. We apologize to all investigators whose results could not be cited due to space limitations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yukun Liu.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by N. Stewart.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., He, C. Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Rep 35, 995–1007 (2016). https://doi.org/10.1007/s00299-016-1950-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1950-x

Keywords

Navigation