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ERF73/HRE1 is involved in H2O2 production via hypoxia-inducible Rboh gene expression in hypoxia signaling

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Abstract

Hypoxia deprives cells of energy and induces severe physical damage in embryophytes. Under hypoxia, the equilibrium between ethylene and H2O2 affects the response of the transcription factor AtERF73/HRE1. To evaluate the role of AtERF73/HRE1 during hypoxia signaling, we used three independent AtERF73/HRE1 knockout lines to detect H2O2 accumulation. The results revealed that under hypoxia, H2O2 accumulation in the AtERF73/HRE1 knockout lines decreased, indicating that AtERF73/HRE1 uses a negative feedback regulation mechanism to influence the production of H2O2 induced through hypoxia signal transduction. Quantitative RT-PCR analyses showed that oxygen deficiency had different effects on the expression of the hypoxia-induced genes Rboh B, D, G, and I in the AtERF73/HRE1 knockout lines. In particular, Rboh B and D expression were increased, whereas Rboh G expression was decreased. The expression of Rboh I was increased at 1 h but decreased at 3 h during hypoxia treatment in the AtERF73/HRE1 knockout lines. Similarly, the transcript levels of antioxidant and hypoxia-induced/ethylene response genes in the AtERF73/HRE1 knockout lines were affected by hypoxic stress, indicating that AtERF73/HRE1 is essential to hypoxia signal transduction in embryophytes. Additionally, in histochemical analysis, AtERF73/HRE1 promoter-induced GUS expression was detected in various plant parts throughout the plant growth process (e.g., leaves, inflorescences, siliques), particularly in the edges of mature leaves and guard cells. Taken together, our results confirm that AtERF73/HRE1 plays a role in H2O2 production by affecting the hypoxia-induced expression of Rboh genes in hypoxia signal transduction.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

ERF73/HRE1:

Ethylene-responsive factors73/ hypoxia responsive1

GR:

Glutathione reductase

GUS:

β-glucuronidase

H2O2 :

Hydrogen peroxide

RBOH:

Respiratory burst oxidase homolog

ROS:

Reactive oxygen species

RT-PCR:

Reverse transcriptase-polymerase chain reaction

References

  • Bai T, Ma P, Li C, Yin R, Ma F (2013) Role of ascorbic acid in enhancing hypoxia tolerance in roots of sensitive and tolerant apple rootstocks. Sci Hortic 164:372–379

    Article  CAS  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65(5):1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296(5575):2026–2028

    Article  CAS  PubMed  Google Scholar 

  • Chang R, Jang CJ, Branco-Price C, Nghiem P, Bailey-Serres J (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol Biol 78(1–2):109–122

    Article  CAS  PubMed  Google Scholar 

  • Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42(4):273–282

    Article  CAS  PubMed  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18(8):2021–2034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7(4):465–471

    Article  CAS  PubMed  Google Scholar 

  • Hess N, Klode M, Anders M, Sauter M (2011) The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiol Plant 143(1):41–49

    Article  CAS  PubMed  Google Scholar 

  • Huang YW, Zhou ZQ, Yang HX, Wei CX, Wan YY, Wang XJ (2015). Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity. Biol Plant 59:131–138

  • 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. Proc Natl Acad Sci U S A 106(48):20520–20525

    Article  CAS  PubMed  PubMed Central  Google 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. J Plant Physiol 168:1919–1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson RA (1989) The GUS reporter gene system. Nature 342(6251):837–838

    Article  CAS  PubMed  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(11):2623–2633

  • Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62(2):302–315

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137(3):1115–1129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Rennenberg H, Kreuzwieser J (2015) Hypoxia induces stem and leaf nitric oxide (NO) emission from poplar seedlings. Planta 241(3):579–589

    Article  CAS  PubMed  Google 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 Phytol 172(2):221–228

    Article  CAS  PubMed  Google Scholar 

  • Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y (2007) The coronatine-insentitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 143:1398–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pucciariello C, Parlanti S, Banti V, Novi G, Perata P (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol 159(1):184–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rejeb KB, Vos DLD, Disquet IL, Leprince AS, 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(4): 1138–1148

  • Seok HY, Tarte VN, Lee SY, Park HY, Moon YH (2014) Arabidopsis HRE1alpha, a splicing variant of AtERF73/HRE1, functions as a nuclear transcription activator in hypoxia response and root development. Plant Cell Rep 33(8):1255–1262

    Article  CAS  PubMed  Google Scholar 

  • Singh N, Dang TT, Vergara GV, Pandey DM, Sanchez D, Neeraja CN, Septiningsih EM, Mendioro M, Tecson-Mendoza EM, Ismail AM, Mackill DJ, Heuer S (2010) Molecular marker survey and expression analyses of the rice submergence-tolerance gene SUB1A. Theor Appl Genet 121(8):1441–1453

    Article  CAS  PubMed  Google Scholar 

  • Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91 Spec No:119–127

  • 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(6):691–699

    Article  CAS  PubMed  Google Scholar 

  • Wu YS, Yang CY (2016) Physiological responses and expression profile of NADPH oxidase in rice (Oryza sativa) seedlings under different levels of submergence. Rice 9(1):2

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708

    Article  CAS  PubMed  Google Scholar 

  • Yang CY (2014) Hydrogen peroxide controls transcriptional responses of ERF73/HRE1 and ADH1 via modulation of ethylene signaling during hypoxic stress. Planta 239(4):877–885

    Article  CAS  PubMed  Google Scholar 

  • Yang CY, Hong CP (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  Google Scholar 

  • Yang CY, Hsu FC, Li JP, Wang NN, Shih MC (2011) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol 156(1):202–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Science Council (NSC 101-2311-B-005-001 to Chin-Ying Yang).

Author contribution statement

C-Y Yang designed the experiments, conducted the experiments, prepared the figures, and wrote the manuscript. Y-C Huang carried out part of the qRT-PCR experiments. S-L Ou carried out the statistical analysis.

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Authors and Affiliations

  1. Department of Agronomy, National Chung Hsing University, Taichung, 40227, Taiwan

    Chin-Ying Yang, Yi-Chun Huang & Shang-Ling Ou

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  1. Chin-Ying Yang
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  2. Yi-Chun Huang
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  3. Shang-Ling Ou
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Correspondence to Chin-Ying Yang.

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Yang, CY., Huang, YC. & Ou, SL. ERF73/HRE1 is involved in H2O2 production via hypoxia-inducible Rboh gene expression in hypoxia signaling. Protoplasma 254, 1705–1714 (2017). https://doi.org/10.1007/s00709-016-1064-x

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