Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Hydrogen peroxide plays an important role in PERK4-mediated abscisic acid-regulated root growth in Arabidopsis

Xiaonan Ma https://orcid.org/0000-0001-9105-0377 A , Xiaoran Zhang A , Ling Yang A , Mengmeng Tang A , Kai Wang A , Li Wang A , Ling Bai A B and Chunpeng Song A
+ Author Affiliations
- Author Affiliations

A Institute of Plant Stress Biology, State Key Laboratory of Cotton Biology, Department of Biology, Henan University, 85 Minglun Street, Kaifeng 475001, China.

B Corresponding author. Email: bailing@henu.edu.cn

Functional Plant Biology 46(2) 165-174 https://doi.org/10.1071/FP18219
Submitted: 8 August 2018  Accepted: 18 September 2018   Published: 29 October 2018

Abstract

Abscisic acid (ABA) is a crucial factor that affects primary root tip growth in plants. Previous research suggests that reactive oxygen species (ROS), especially hydrogen peroxide, are important regulators of ABA signalling in root growth of Arabidopsis. PROLINE-RICH EXTENSIN-LIKE RECEPTOR KINASE 4 (PERK4) plays an important role in ABA responses. Arabidopsis perk4 mutants display attenuated sensitivity to ABA, especially in primary root growth. To gain insights into the mechanism(s) of PERK4-associated ABA inhibition of root growth, in this study we investigated the involvement of ROS in this process. Normal ROS accumulation in the primary root in response to exogenous ABA treatment was not observed in perk4 mutants. PERK4 deficiency prohibits ABA-induced expression of RESPIRATORY BURST OXIDASE HOMOLOGUE (RBOH) genes, therefore the perk4-1 mutant showed decreased production of ROS in the root. The perk4-1/rbohc double mutant displayed the same phenotype as the perk4 and rbohc single mutants in response to exogenous ABA treatment. The results suggest that PERK4-stimulated ROS accumulation during ABA-regulated primary root growth may be mediated by RBOHC.

Additional keywords: ABA response, PERK4, RBOHC, root growth, ROS accumulation.


References

Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94.
Integration of plant responses to environmentally activated phytohormonal signals.Crossref | GoogleScholarGoogle Scholar |

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. Current Biology 18, 656–660.
Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |

Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI (2002) Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. The Plant Cell 14, 1649–1662.
Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2.Crossref | GoogleScholarGoogle Scholar |

Bai L, Zhang G, Zhou Y, Zhang Z, Wang W, Du Y, Wu Z, Song CP (2009) Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca2+ signalling, is required for abscisic acid responses in Arabidopsis thaliana. The Plant Journal 60, 314–327.
Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca2+ signalling, is required for abscisic acid responses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Bai L, Ma X, Zhang G, Song S, Zhou Y, Gao L, Miao Y, Song CP (2014a) A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis. The Plant Cell 26, 1497–1511.
A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Bai L, Zhou Y, Ma X, Gao L, Song CP (2014b) Arabidopsis CAP1-mediated ammonium sensing required reactive oxygen species in plant cell growth. Plant Signaling & Behavior 9,
Arabidopsis CAP1-mediated ammonium sensing required reactive oxygen species in plant cell growth.Crossref | GoogleScholarGoogle Scholar |

Bi C, Ma Y, Wu Z, Yu YT, Liang S, Lu K, Wang XF (2017) Arabidopsis ABI5 plays a role in regulating ROS homeostasis by CATALASE 1 transcription in seed germination. Plant Molecular Biology 94, 197–213.
Arabidopsis ABI5 plays a role in regulating ROS homeostasis by CATALASE 1 transcription in seed germination.Crossref | GoogleScholarGoogle Scholar |

Boursiac Y, Léran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends in Plant Science 18, 325–333.
ABA transport and transporters.Crossref | GoogleScholarGoogle Scholar |

Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90, 856–867.
Reactive oxygen species, abiotic stress and stress combination.Crossref | GoogleScholarGoogle Scholar |

Daszkowska-Golec A, Szarejko I (2013) Open or close the gate-stomata action under the control of phytohormones in drought stress conditions. Frontiers of Plant Science 4, 138
Open or close the gate-stomata action under the control of phytohormones in drought stress conditions.Crossref | GoogleScholarGoogle Scholar |

De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant, Cell & Environment 35, 234–244.
Redox regulation in plant programmed cell death.Crossref | GoogleScholarGoogle Scholar |

De Tullio MC, Jiang K, Feldman L (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiology and Biochemistry 48, 328–336.
Redox regulation of root apical meristem organization: connecting root development to its environment.Crossref | GoogleScholarGoogle Scholar |

Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. Journal of Cell Science 116, 81–88.
Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells.Crossref | GoogleScholarGoogle Scholar |

Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. The Plant Journal 49, 377–386.
Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels.Crossref | GoogleScholarGoogle Scholar |

Ding ZJ, De Smet I (2013) Localised ABA signalling mediates root growth plasticity. Trends in Plant Science 18, 533–535.
Localised ABA signalling mediates root growth plasticity.Crossref | GoogleScholarGoogle Scholar |

Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Molecular Plant 6, 559–569.
The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF.Crossref | GoogleScholarGoogle Scholar |

Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Current Opinion in Plant Biology 7, 537–546.
Guard cells: a dynamic signaling model.Crossref | GoogleScholarGoogle Scholar |

Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15–S45.
Abscisic acid signaling in seeds and seedlings.Crossref | GoogleScholarGoogle 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.
Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Crossref | GoogleScholarGoogle Scholar |

Gao W, Long L, Xu L, Lindsey K, Zhang X, Zhu L (2016) Suppression of the homeobox gene HDTF1 enhances resistance to Verticillium dahliae and Botrytis cinerea in cotton. Journal of Integrative Plant Biology 58, 503–513.
Suppression of the homeobox gene HDTF1 enhances resistance to Verticillium dahliae and Botrytis cinerea in cotton.Crossref | GoogleScholarGoogle Scholar |

Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiology 141, 341–345.
Control of plant development by reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |

Hamilton DW, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proceedings of the National Academy of Sciences of the United States of America 97, 4967–4972.
Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid.Crossref | GoogleScholarGoogle Scholar |

He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu LJ, Gong Z (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. The Plant Cell 24, 1815–1833.
DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling.Crossref | GoogleScholarGoogle Scholar |

Hernandez M, Fernandez-Garcia N, Diaz-Vivancos P, Olmos E (2010) A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots. Journal of Experimental Botany 61, 521–535.
A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots.Crossref | GoogleScholarGoogle Scholar |

Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Current Opinion in Plant Biology 6, 470–479.
Relay and control of abscisic acid signaling.Crossref | GoogleScholarGoogle Scholar |

Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports 39, 969–987.
Signal transduction during cold, salt, and drought stresses in plants.Crossref | GoogleScholarGoogle Scholar |

Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Letters 508, 463

Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proceedings of the National Academy of Sciences of the United States of America 106, 20520–20525.
MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling.Crossref | GoogleScholarGoogle Scholar |

Jannat R, Uraji M, Morofuji M, Islam MM, Bloom RE, Nakamura Y, McClung CR, Schroeder JI, Mori IC, Murata Y (2011) Roles of intracellular hydrogen peroxide accumulation in abscisic acid signaling in Arabidopsis guard cells. Journal of Plant Physiology 168, 1919–1926.
Roles of intracellular hydrogen peroxide accumulation in abscisic acid signaling in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar |

Jiao Y, Sun L, Song Y, Wang L, Liu L, Zhang L, Liu B, Li N, Miao C, Hao F (2013) AtrbohD and AtrbohF positively regulate abscisic acid- inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. Journal of Experimental Botany 64, 4183–4192.
AtrbohD and AtrbohF positively regulate abscisic acid- inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. The Plant Cell 10, 255–266.

Klüsener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiology 130, 2152–2163.
Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar |

Knight MR (2007) New ideas on root hair growth appear from the flanks. Proceedings of the National Academy of Sciences of the United States of America 104, 20649–20650.
New ideas on root hair growth appear from the flanks.Crossref | GoogleScholarGoogle 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 Journal 22, 2623–2633.
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Liu B, Sun L, Ma L, Hao FS (2017) Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis. Plant Cell Reports 36, 947–957.

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. Journal of Experimental Botany 63, 305–317.
NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+homeostasis in Arabidopsis under salt stress.Crossref | GoogleScholarGoogle Scholar |

McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytologist 172, 221–228.
Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk?Crossref | GoogleScholarGoogle Scholar |

Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. The Plant Cell 18, 2749–2766.
An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses.Crossref | GoogleScholarGoogle 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. Science Signaling 2, ra45
The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.Crossref | GoogleScholarGoogle Scholar |

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

Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends in Plant Science 16, 300–309.
ROS signaling: the new wave?Crossref | GoogleScholarGoogle Scholar |

Møller IM, Sweetlove LJ (2010) ROS signalling-specificity is required. Trends in Plant Science 15, 370–374.
ROS signalling-specificity is required.Crossref | GoogleScholarGoogle 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. Proceedings of the National Academy of Sciences of the United States of America 104, 20996–21001.
Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs.Crossref | GoogleScholarGoogle Scholar |

Munemasa S, Muroyama D, Nagahashi H, Nakamura Y, Mori IC, Murata Y (2013) Regulation of reactive oxygen species-mediated abscisic acid signaling in guard cells and drought tolerance by glutathione. Frontiers of Plant Science 4, 472
Regulation of reactive oxygen species-mediated abscisic acid signaling in guard cells and drought tolerance by glutathione.Crossref | GoogleScholarGoogle 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. The Plant Cell 14, 3089–3099.
Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production.Crossref | GoogleScholarGoogle Scholar |

Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
Hydrogen peroxide signalling.Crossref | GoogleScholarGoogle Scholar |

Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. The Plant Journal 61, 1053–1066.
Arabidopsis and the plant immune system.Crossref | GoogleScholarGoogle Scholar |

O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236, 765–779.
Reactive oxygen species and their role in plant defence and cell wall metabolism.Crossref | GoogleScholarGoogle Scholar |

Okuma E, Jahan MS, Munemasa S, Hossain MA, Muroyama D, Islam MM, Ogawa K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2011) Negative regulation of abscisic acid-induced stomatal closure by glutathione in Arabidopsis. Journal of Plant Physiology 168, 2048–2055.
Negative regulation of abscisic acid-induced stomatal closure by glutathione in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends in Plant Science 8, 335–342.
Reactive oxygen species and hormonal control of cell death.Crossref | GoogleScholarGoogle Scholar |

Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.Crossref | GoogleScholarGoogle Scholar |

Peng L, Lang S, Wang Y, Pritchard HW, Wang X (2017) Modulating role of ROS in re-establishing desiccation tolerance in germinating seeds of Caragana korshinskii Kom. Journal of Experimental Botany 68, 3585–3601.
Modulating role of ROS in re-establishing desiccation tolerance in germinating seeds of Caragana korshinskii Kom.Crossref | GoogleScholarGoogle Scholar |

Pilet PE (1975) Abscisic acid as a root growth inhibitor: physiological analyses. Planta 122, 299–302.
Abscisic acid as a root growth inhibitor: physiological analyses.Crossref | GoogleScholarGoogle Scholar |

Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends in Plant Science 12, 98–105.
Stress-induced morphogenic responses: growing out of trouble?Crossref | GoogleScholarGoogle Scholar |

Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861.
OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Rubinovich L, Weiss D (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. The Plant Journal 64, 1018–1027.
The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta.Crossref | GoogleScholarGoogle 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. The Plant Cell 16, 616–628.
Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum.Crossref | GoogleScholarGoogle Scholar |

Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. Journal of Experimental Botany 55, 2343–2351.
Root growth maintenance during water deficits: physiology to functional genomics.Crossref | GoogleScholarGoogle Scholar |

Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proceedings of the National Academy of Sciences of the United States of America 101, 8827–8832.
Hydrogen peroxide mediates plant root cell response to nutrient deprivation.Crossref | GoogleScholarGoogle Scholar |

Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 1441–1452.
Root system architecture: insights from Arabidopsis and cereal crops.Crossref | GoogleScholarGoogle Scholar |

Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. The Plant Cell 17, 2384–2396.
Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses.Crossref | GoogleScholarGoogle Scholar |

Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytologist 201, 1121–1140.
Behind the scenes: the roles of reactive oxygen species in guard cells.Crossref | GoogleScholarGoogle Scholar |

Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691–699.
Respiratory burst oxidases: the engines of ROS signaling.Crossref | GoogleScholarGoogle Scholar |

Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Crossref | GoogleScholarGoogle 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). The Plant Journal 14, 365–370.
Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox).Crossref | GoogleScholarGoogle Scholar |

Trewavas AJ, Jones HG (1991) An assessment of the role of ABA in plant development. In ‘Abscisic acid: physiology and biochemistry’. (Eds WJ Davies, HG Jones) pp. 169–188. (Bios Scientific Publishers: Oxford)

Wang PT, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytologist 178, 703–718.
Guard-cell signalling for hydrogen peroxide and abscisic acid.Crossref | GoogleScholarGoogle Scholar |

Xia P, Liu H, Tian Y (2009) Cathodic detection of H2O2 based on nanopyramidal gold surface with enhanced electron transfer of myoglobin. Biosensors & Bioelectronics 24, 2470–2474.
Cathodic detection of H2O2 based on nanopyramidal gold surface with enhanced electron transfer of myoglobin.Crossref | GoogleScholarGoogle Scholar |

Yang L, Zhang J, He JN, Qin YY, Hua DP, Duan Y, Chen ZZ, Gong ZZ (2014) ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLOS Genetics 10,
ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Zhang X, Zhang L, An GY, Gao JF, Song CP (2001) Studies on ABA-induced H2O2 in Vicia guard cells by means of confocal laser scanning microscopy. Shi Yan Sheng Wu Xue Bao 34, 1–6.

Zhao Y, Zhang Z, Gao J, Wang P, Hu T, Wang Z, Hou YJ, Wan Y, Liu W, Xie S, Lu T, Xue L, Liu Y, Macho AP, Tao WA, Bressan RA, Zhu JK (2018) Arabidopsis duodecuple mutant of PYL ABA receptors reveals PYL repression of ABA-independent SnRK2 activity. Cell Reports 23, 3340–3351.e1.
Arabidopsis duodecuple mutant of PYL ABA receptors reveals PYL repression of ABA-independent SnRK2 activity.Crossref | GoogleScholarGoogle Scholar |