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Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis

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Both AtrbohD and AtrbohF promote the increases in activities of ADH, PDC, LDH, and Ca2+ levels, and induce the expression of multiple hypoxia response genes, thus improving Arabidopsis adaptation to oxygen deficiency.

Abstract

NADPH oxidase AtrbohD and AtrbohF cooperatively play key roles in regulation of growth and stress signaling in Arabidopsis. However, reports on AtrbohD and AtrbohF functioning together in hypoxia signaling are scarce, and the underlying mechanisms remain elusive. Here, we show that the double null mutant atrbohD/F is more sensitive to oxygen deprivation compared with wild type (WT) and the single mutant atrbohD and atrbohF. Under oxygen deficiency, enhancements of the transcripts of alcohol dehydrogenase 1 (ADH1) and pyruvate decarboxylase 1 (PDC1) and the activities of ADH, PDC and lactate dehydrogenase in WT are clearly reduced in the single mutants, and more strongly reduced in the double mutant. Moreover, increases in the production of ATP, H2O2 and Ca2+ in WT are significantly arrested in atrbohD, atrbohF, and especially in atrbohD/F. Hypoxia-promoted rise in the expression of some hypoxic responsive genes is also inhibited in atrbohD/F relative to WT, atrbohD and atrbohF. These genes include ethylene response factor 73, lactate dehydrogenase, MYB transcription factor 2, sucrose synthase 1 (SUS1), SUS4, heat stress transcription factor A2 and heat-shock protein 18.2. These results suggest that both AtrbohD and AtrbohF are essential for mediating hypoxia signaling. H2O2 derived from AtrbohD and AtrbohF triggers the Ca2+ increase and induces the expression of multiple hypoxia response genes, thus improving Arabidopsis tolerance to low-oxygen stress. These findings provide new insights into the mechanisms of AtrbohF in regulating the responses to oxygen deprivation in Arabidopsis.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (30970235 and 31070239), Science and Technology Development Program of He’nan in China (162102110005), and Foundation of He’nan Educational Committee of China (15A210018, 17A180018 and 14B180029).

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Author notes

  1. Bo Liu

    Present address: Department of Ecology, College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China

  2. Liya Ma

    Present address: Anci District Agricultural Bureau of Langfang, Langfang, 065000, China

Authors and Affiliations

  1. State Key Laboratory of Cotton Biology, Henan Key Laboratory of Plant Stress Biology, College of Life Sciences, Henan University Jinming Campus, Kaifeng, 475004, China

    Bo Liu, Lirong Sun, Liya Ma & Fu-Shun Hao

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  1. Bo Liu
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Correspondence to Fu-Shun Hao.

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Communicated by Chun-Hai Dong.

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Liu, B., Sun, L., Ma, L. et al. Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis . Plant Cell Rep 36, 947–957 (2017). https://doi.org/10.1007/s00299-017-2128-x

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  • DOI: https://doi.org/10.1007/s00299-017-2128-x

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