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Signal Function Studies of ROS, Especially RBOH-Dependent ROS, in Plant Growth, Development and Environmental Stress

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Abstract

Reactive oxygen species (ROS) are well known for their dual functions in plants. On the one hand, ROS were once thought to be harmful to plants because their excessive accumulation might lead to oxidative stress and cause cell injury in severe cases. On the other hand, a timely and appropriate burst of ROS acts as an important signal for plant growth, development and defence against environmental stress. ROS are common molecules in various plant metabolic processes and can be generated almost anywhere in plant cells. NADPH oxidase located on the plasma membrane, also known as the RBOH protein, provides a very important ROS synthesis pathway. This article briefly summarizes the signal functions of ROS, especially RBOH-dependent ROS, in plant growth, development and defence against abiotic and biotic stress in Arabidopsis (Arabidopsis thaliana).

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References

  • Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18:656–660

    CAS  PubMed  Google Scholar 

  • Alvarez MA, Pennell RI, Meijer P, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 90:109–116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnaud D, Lee S, Takebayashi Y, Choi D, Choi J, Sakakibarac H, Hwang I (2017) Cytokinin-mediated regulation of reactive oxygen species homeostasis modulates stomatal immunity in arabidopsis. Plant Cell 29:543–559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ayarpadikannan S, Chung E, Cho CW, So HA, Kim SO, Jeon JM, Kwak MH, Lee SW, Lee JH (2012) Exploration for the salt stress tolerance genes from a salt-treated halophyte, Suaeda asparagoides. Plant Cell Rep 31:35–48

    CAS  PubMed  Google Scholar 

  • Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 331:806–814

    CAS  PubMed  Google Scholar 

  • Baker CJ, Orlandi EW, Mock NM (1993) Harpin, an elicitor of the hypersensitive response in tobacco caused by erwinia amylovora, elicits active oxygen production in suspension cells. Plant Physiol 102:1341–1344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beemster GT, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beemster GT, Veylder LD, Vercruysse S, West G, Rombaut D, Hummelen PV, Galichet A, Gruissem W, Inze D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539

    CAS  PubMed  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    CAS  PubMed  Google Scholar 

  • Cao S, Du XH, Li LH, Liu YD, Zhang L, Pan X, Li Y, Li H, Lu H (2017) Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants. Russ J Plant Physiol 64:224–234

    CAS  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    CAS  PubMed  Google Scholar 

  • Chen ZP, Xie YJ, Gu Q, Zhao G, Zhang YH, Cui WT, Xu S, Wang R, Shen WB (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic Biol Med 108:465–477

    CAS  PubMed  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    CAS  PubMed  Google Scholar 

  • Cummins WR, Kende H, Raschke K (1971) Specificity and reversibility of the rapid stomatal response to abscisic acid. Planta 99:347–351

    CAS  PubMed  Google Scholar 

  • Desikan R, Cheung M, Bright J, Henson D, Hancock J, Neill S (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212

    CAS  PubMed  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    CAS  PubMed  Google Scholar 

  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    CAS  Google Scholar 

  • Doke N (1985) NADPH -dependent O·−2 generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiol Plant Pathol 27:311–322

    CAS  Google Scholar 

  • Drerupa MM, Schlückinga K, Hashimotoa K, Manishankara P, Steinhorsta L, Kuchitsub K, Kudlaa J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RbohF. Mol Plant 6:559–569

    Google Scholar 

  • Dreyer A, Dietz KJ (2018) Reactive oxygen species and the redox-regulatory network in cold stress acclimation. Antioxidants 7:169

    PubMed Central  Google Scholar 

  • Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu HM, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Elstner EF (1982) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33:73–96

    CAS  Google Scholar 

  • Ensminger I, Busch F, Huner NP (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    CAS  Google Scholar 

  • Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559

    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

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    CAS  Google Scholar 

  • Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, Lorenzo GD, 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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gechev TS, Van BF, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101

    CAS  PubMed  Google Scholar 

  • Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630

    CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    CAS  PubMed  Google Scholar 

  • Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ, Jones JD (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J 10:515–522

    CAS  PubMed  Google Scholar 

  • Guan B, Yu J, Wang X, Fu Y, Kan X, Lin Q, Han G, Lu Z (2011) Physiological responses of halophyte suaeda salsa to water table and salt stresses in coastal wetland of yellow river delta. Clean-Soil Air Water 39:1029–1035

    CAS  Google Scholar 

  • Halliwell B (1978) Lignin synthesis. The generation of hydrogen peroxide and superoxide by horseradish peroxidase and its stimulation by manganese (II) and phenols. Planta 140:81–88

    CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harkin JM, Obst JR (1973) Lignification in trees: indication of exclusive peroxidase participation. Science 180:296–298

    CAS  PubMed  Google Scholar 

  • Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334

    CAS  PubMed  Google Scholar 

  • Hodgson RA, Raison JK (1991) Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta 183:222–228

    CAS  PubMed  Google Scholar 

  • Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Porée F, Boucherez J, Lebaudy A, Bouchez D, Véry A (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100:5549–5554

    CAS  PubMed  Google Scholar 

  • Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515–533

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Aken OV, Schwarzländer M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol 171:1551–1559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–2159

    CAS  PubMed  Google Scholar 

  • Huner NP, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang C, Belfield EJ, Cao Y, Smith JA, Harberd NP (2013) An Arabidopsis soilsalinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25:3535–3552

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060

    CAS  PubMed  PubMed Central  Google Scholar 

  • Juszczak I, Cvetkovic J, Zuther E, Hincha DK, Baier M (2016) Natural variation of cold deacclimation correlates with variation of cold-acclimation of the plastid antioxidant system in Arabidopsis thaliana Accessions. Front Plant Sci 7:305

    PubMed  PubMed Central  Google Scholar 

  • Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S (2014) Direct regulation of the NADPH oxidase RbohD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55

    CAS  PubMed  Google Scholar 

  • Kadota Y, Shirasu K, Zipfel C (2015) Regulation of the NADPH oxidase RbohD during plant immunity. Plant Cell Physiol 56:1472–1480

    CAS  PubMed  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Orozco-Cárdenas ML, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    CAS  PubMed  Google Scholar 

  • Kaur N, Dhawan M, Sharma I, Pati PK (2016) Interdependency of reactive oxygen species generating and scavenging system in salt sensitive and salt tolerant cultivars of rice. BMC Plant Biol 16:131

    PubMed  PubMed Central  Google Scholar 

  • Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsua K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971

    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

    CAS  PubMed  Google Scholar 

  • Kollist H, Nuhkat M, Roelfsema MR (2014) Closing gaps: linking elements that control stomatal movement. New Phytol 203:44–62

    CAS  PubMed  Google Scholar 

  • Königshofer H, Tromballa HW, Löppert HG (2008) Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant, Cell Environ 31:1771–1780

    Google Scholar 

  • Konopka CA, Backues SK, Bednarek SY (2008) Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20:1363–1380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    CAS  PubMed  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    CAS  PubMed  Google Scholar 

  • Lara-Ortíz T, Riveros-Rosas H, Aguirre J (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50:1241–1255

    PubMed  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann S, Serrano M, Haridon F, Tjamos SE, Metraux J (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54–62

    CAS  PubMed  Google Scholar 

  • Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    CAS  PubMed  Google Scholar 

  • Leymarie J, Vitkauskaité G, Hoang HH, Gendreau E, Chazoule V, Meimoun P, Corbineau F, El-Maarouf-Bouteau H, Bailly C (2014) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol 53:96–106

    Google Scholar 

  • Li C, Wang P, Wei Z, Liang D, Liu C, Yin L, Jia D, Fu M, Ma F (2012) The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J Pineal Res 53:298–306

    CAS  PubMed  Google Scholar 

  • Lim GH, Singhal R, Kachroo A, Kachroo P (2017) Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol 55:505–536

    CAS  PubMed  Google Scholar 

  • Liu Y, He C (2016) Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Rep 35:995–1007

    CAS  PubMed  Google Scholar 

  • Liu SS, Wang WQ, Li M, Wan SB, Sui N (2017) Antioxidants and unsaturated fatty acids are involved in salt tolerance in peanut. Acta Physiol Plant 39:207

    CAS  Google Scholar 

  • Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JH (2014) Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat Commun 5:3767

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Macpherson N, Takeda S, Shang Z, Dark A, Mortimer JC, Brownlee C, Dolan L, Davies JM (2008) NADPH oxidase involvement in cellular integrity. Planta 227:1415–1418

    CAS  PubMed  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2011) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    PubMed  Google Scholar 

  • McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behaviour and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467–472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266

    CAS  PubMed  Google Scholar 

  • Meng X, Yang DY, Li XD, Zhao SY, Sui N, Meng QW (2015) Physiological changes in fruit ripening caused by overexpression of tomato SlAN2, an R2R3-MYB factor. Plant Physiol Bioch 89:24–30

    CAS  Google Scholar 

  • Miao YC, Lü D, Wang PC, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox-transducer and a scavenger in ABA and drought stress responses. Plant Cell 18:2749–2766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Van Breusegem F, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67:3831–3844

    CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and a response to abiotic stress. Plant Physiol 144:1777–1785

    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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001

    CAS  PubMed  Google Scholar 

  • Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341–2356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morales J, Kadota Y, Zipfel C, Molina A, Torres M (2016) The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J Exp Bot 67:1663–1676

    CAS  PubMed  Google Scholar 

  • Müller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G (2009) The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol 184:885–897

    PubMed  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder JI (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neill S, Desikan R, Clarke A, Hurst R, Hancock J (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1242

    CAS  PubMed  Google Scholar 

  • Noctora G, Reichheld JP, Foyer CH (2018) ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol 80:3–12

    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

    CAS  PubMed  Google Scholar 

  • Omran RG (1980) Peroxide levels and the activities of catalase, peroxidase, and indoleacetic acid oxidase during and after chilling cucumber seedlings. Plant Physiol 65:407–408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    PubMed  PubMed Central  Google Scholar 

  • Pang C, Li K, Wang B (2011) Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana. Physiol Plant 143:355–366

    CAS  PubMed  Google Scholar 

  • Parish RW, Li SF (2010) Death of a tapetum: a programme of developmental altruism. Plant Sci 178:73–89

    CAS  Google Scholar 

  • Pastori G, Foyer C (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of ‘redox’ and abscisic acid-mediated controls. Plant Physiol 129:460–468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pei Z, Murata Y, Benning G, Thomine S, Klüsener B, Allen G, Grill E, Schroeder J (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    CAS  PubMed  Google Scholar 

  • Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant Microbe in. 23:846–860

    CAS  Google Scholar 

  • Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119:849–858

    CAS  PubMed  PubMed Central  Google Scholar 

  • Potocký M, Jones MA, Bezvoda R, Smirnoff N, Žárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    PubMed  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of Arabidopsis. Russ J Plant Physiol 57:233–240

    CAS  Google Scholar 

  • Qin G, Tian S, Chan Z, Li B (2007) Crucial role of antioxidant proteins and hydrolytic enzymes in pathogenicity of Penicillium expansum: analysis based on proteomic approach. Mol Cell Proteom 6:425–438

    CAS  Google Scholar 

  • Qin G, Meng X, Wang Q, Tian S (2009) Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redox proteomics analysis. J Proteome Res 8:2449–2462

    CAS  PubMed  Google Scholar 

  • Qin G, Liu J, Cao B, Li B, Tian S (2011) Hydrogen peroxide acts on sensitive mitochondrial proteins to induce death of a fungal pathogen revealed by proteomic analysis. PLoS ONE 6:e21945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    CAS  PubMed  Google Scholar 

  • Rejeb KB, Vos DL, Disquet IL, Leprince A, Bordenave M, Maldiney R, Jdey A, Abdelly C, Savouré A (2015) Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol 208:1138–1148

    PubMed  Google Scholar 

  • Rosen E, Chen R, Masson PH (1999) Root gravitropism: a complex response to a simple stimulus? Trends Plant Sci 4:407–412

    CAS  PubMed  Google Scholar 

  • Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13:432–436

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    CAS  PubMed  Google Scholar 

  • Scott IM, Clarke SM, Wood JE, Mur LA (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 13:1040–1049

    Google Scholar 

  • Shen XY, Wang ZL, Song XF, Xu JJ, Jiang CY, Zhao YX, Ma CL, Zhang H (2014) Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Mol Biol 86:303–317

    CAS  PubMed  Google Scholar 

  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sierla M, Waszczak C, Vahisalu T, Kangasjärvi J (2016) Reactive oxygen species in the regulation of stomatal movements. Plant Physiol 171:1569–1580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sirichandra C, Gu D, Hu H, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986

    CAS  PubMed  Google Scholar 

  • Song J, Wang BS (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot-London 115:541–553

    CAS  Google Scholar 

  • Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140

    CAS  PubMed  Google Scholar 

  • Song J, Zhou JC, Zhao WW, Xu HL, Wang FX, Xu YG, Wang L, Tian CY (2016) Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Spec Biol 31:19–28

    Google Scholar 

  • Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS, Teige M, Van Breusegem F (2015) Plant innate immunity–sunny side up? Trends Plant Sci 20:3–11

    CAS  PubMed  Google Scholar 

  • Sui N, Tian SS, Wang WQ, Wang MJ, Fan H (2017) Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Front Plant Sci 8:1337

    PubMed  PubMed Central  Google Scholar 

  • Sui N, Wang Y, Liu SS, Yang Z, Wang F, Wan SB (2018) Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut. Front Plant Sci 9:7

    PubMed  PubMed Central  Google Scholar 

  • Sumimoto H (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J 275:3249–3277

    CAS  PubMed  Google Scholar 

  • Sun ZB, Qi XY, Wang ZL, Li PH, Wu CX, Zhang H, Zhao YX (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Bioch 69:82–89

    CAS  Google Scholar 

  • Sun W, Li Y, Zhao YX, Zhang H (2015) The TsnsLTP4, a nonspecific lipid transfer protein involved in wax deposition and stress tolerance. Plant Mol Biol Report 33:962–974

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Swanson S, Gilroy S (2012) ROS in plant development. Physiol Plant 138:384–392

    Google Scholar 

  • Szechynska-Hebda M, Kruk J, Gorecka M, Karpinska B, Karpinski S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22:2201–2218

    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

    CAS  PubMed  Google Scholar 

  • Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244

    CAS  PubMed  Google Scholar 

  • Tian S, Qin G, Li B (2013) Reactive oxygen species involved in regulating fruit senescence and fungal pathogenicity. Plant Mol Biol 82:593–602

    CAS  PubMed  Google Scholar 

  • Torres MA (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    CAS  PubMed  PubMed Central  Google Scholar 

  • Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J 14:365–370

    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

    CAS  PubMed  Google Scholar 

  • Townsley BT, Sinha NR (2012) A new development: evolving concepts in leaf ontogeny. Annu Rev Plant Biol 63:535–562

    CAS  PubMed  Google Scholar 

  • Tsuda K, Katagiri F (2015) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465

    Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    CAS  PubMed  Google Scholar 

  • Turrens JF, Freeman BA, Crapo JD (1982) Hyperoxia increases H2O2 release by lung mitochondria and microsomes. Arch Biochem Biophys 217:411–421

    CAS  PubMed  Google Scholar 

  • Vera-Estrella R, Blumwald E, Higgins VJ (1992) Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells: evidence for the involvement of active oxygen species. Plant Physiol 99:1208–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stress induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746

    CAS  PubMed  Google Scholar 

  • Wang P, Song C (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718

    CAS  PubMed  Google Scholar 

  • Wang YS, Tian SP, Xu Y (2005) Effects of high oxygen concentration on pro- and anti-oxidant enzymes in peach fruits during postharvest stages. Food Chem 91:99–104

    CAS  Google Scholar 

  • Wang C, Huang L, Buchenauer H, Han Q, Zhang H, Kang Z (2007) Histochemical studies on the accumulation of reactive oxygen species (O·−2 and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f sp. tritici. Physiol Mol Plant P 71:230–239

    CAS  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236

    CAS  PubMed  Google Scholar 

  • Wu H, Liu X, You L, Zhang L, Zhou D, Feng J, Zhao J, Yu J (2012) Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in halophyte Suaeda salsa. J Plant Growth Regul 31:332–341

    CAS  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Y, Xu S, Han B, Wu M, Yuan X, Han Y, Gu Q, Xu D, Yang Q, Shen W (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

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yalpani N, Silverman P, Wilson TM, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809–818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S, Yu Q, Zhang Y, Jia Y, Wan S, Kong X, Ding Z (2018) ROS: the fine-tuner of plant stem cell fate. Trends Plant Sci. TRPLSC 1713:3

    Google Scholar 

  • Yao L, Zhou Q, Pei B, Li Y (2011) Hydrogen peroxide modulates the dynamic microtubule cytoskeleton during the defence responses to Verticillium dahliae toxins in Arabidopsis. Plant, Cell Environ 34:1586–1598

    CAS  Google Scholar 

  • Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12:e1006175

    PubMed  PubMed Central  Google Scholar 

  • Yuan F, Lyu MJ, Leng BY, Zheng GY, Feng ZT, Li PH, Zhu XG, Wang BS (2015) Comparative transcriptome analysis of developmental stages of the limonium bicolor leaf generates insights into salt gland differentiation. Plant, Cell Environ 38:1637–1657

    CAS  Google Scholar 

  • Zeng J, Dong Z, Wu H, Tian Z (2017) Redox regulation of plant stem cell fate. EMBO J 36:2844–2855

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SR, Song J, Wang H, Feng G (2010) Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia. J Plant Ecol 3:259–267

    Google Scholar 

  • Zhang Q, Zhao CZ, Li M, Sun W, Liu Y, Xia H, Sun MN, Li AQ, Li CS, Zhao SZ, Hou L, Picimbon JF, Wang XJ, Zhao YX (2013) Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response. BMC Plant Biol 13:180

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Zhao SS, Mao TL, Qu XL, Cao WH, Zhang L, Guo Y (2011) The plant-specific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis. Plant Cell 23:2314–2330

    PubMed  PubMed Central  Google Scholar 

  • Zhao SS, Jiang YX, Zhao Y, Huang SJ, Yuan M, Zhao YX, Guo Y (2016) CASEIN KINASE1-LIKE PROTEIN2 regulates actin filament stability and stomatal closure via phosphorylation of actin depolymerizing factor. Plant Cell 28:1422–1439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Liao CC, Zhao SS, Wang CW, Guo Y (2017) The glycosyltransferase QUA1 regulates chloroplast-associated calcium signaling during salt and drought stress in Arabidopsis. Plant Cell Physiol 58:329–341

    CAS  PubMed  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Stephen S, Kazan K, Jin G, Fan L, Taylor J, Dennis ES, Helliwell CA, Wang M (2013) Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq. Gene 512:259–266

    CAS  PubMed  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant no. 31602186).

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Chen, Q., Yang, G. Signal Function Studies of ROS, Especially RBOH-Dependent ROS, in Plant Growth, Development and Environmental Stress. J Plant Growth Regul 39, 157–171 (2020). https://doi.org/10.1007/s00344-019-09971-4

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