Skip to main content

Advertisement

Log in

Molecular hydrogen can take part in phytohormone signal pathways in wild rice

  • Original papers
  • Published:
Biologia Plantarum

Abstract

Molecular hydrogen (H2) could be a novel signal in phytohormone signaling pathways in response to biotic and abiotic stresses. Here, we employed two wild rice species (Oryza rufipogon Griff. and O. minuta J. Presl) to test this hypothesis using hydrogen-rich water (HW). The expression differences of phytohormone and hydrogenase genes between conventional rice (Oryza sativa L,) and wild rice were determined by real-time quantitative polymerase chain reaction, and the effects of HW on gene expression of wild rice were detected during three growth stages. Expression of hydrogenase genes, synthesis genes, and receptor genes of salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) signalling pathways was higher in six wild rice types than in conventional rice. Hydrogen-rich water up-regulated expression of two hydrogenase genes, SA, JA, and ET receptor genes and synthesis genes in the seedling stage of wild rice. But this positive regulation by HW was less significant in the vegetative and reproductive stages.

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.

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

AJ:

Anjiashan

CL:

Chaling

CK:

cytokinin

DX:

Dongxiang

ET:

ethylene

GA:

gibberellic acid

GORK:

guard cell outwardly rectifying K+ channel protein

HW:

hydrogen-rich water

JA:

jasmonic acid

LS:

Lingshui

NC:

Nanchang

qPCR:

quatitative polymerase chain reaction

ROS:

reactive oxygen species

SA:

salicylic acid

ST:

Shuitao

References

  • Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., Neill, S.J.: ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. — Plant J. 45: 113–122, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Chen, D.Z., Zhang, B.K., Xiong, W.H.: [Advance in research and application of Dongxiang wild rice germplasm resources.] - Acta agricult. Jiangxi 20: 12–16, 2008. [In Chin.]

    CAS  Google Scholar 

  • Cho, U.H., Park, J.O.: Mercury-induced oxidative stress in tomato seedlings. — Plant Sci. 156: 1–9, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Cui, W., Fang, P., Zhu, K., Mao, Y., Gao, C., Xie, Y., Wang, J., Shen, W.: Hydrogen-rich water confers plant tolerance to mercury toxicity in alfalfa seedlings. — Ecotoxicol. Environ. Safety 105: 103–111, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Cui, W., Gao, C., Fang, P., Lin, G., Shen, W.: Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. — J. Hazard. Mater. 260: 715–724, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Eroglu, E., Melis, A.: Photobiological hydrogen production: recent advances and state of the art. — Bioresour. Technol. 102: 8403–8413, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Forestier, M., King, P., Zhang, L., Posewitz, M., Schwarzer, S., Happe, T., Ghirardi, M.L., Seibert, M.: Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. — Eur. J. Biochem. 270: 2750–2758, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. — Curr. Opin. Plant Biol. 9: 436–442, 2006.

    Article  PubMed  Google Scholar 

  • Gaffron, H.: Reduction of carbon dioxide with molecular hydrogen in green algae. — Nature 143: 204–205, 1939.

    Article  CAS  Google Scholar 

  • Gaffron, H., Rubin, J.: Fermentative and photochemical production of hydrogen in algae. — J. gen. Physiol. 26: 219–240, 1942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gest, H., Kamen, M.D.: Photochemical production of molecular hydrogen by growing cultures of photosynthetic bacteria. Studies on the metabolism of photosynthetic bacteria IV. — J. Bacteriol. 58: 239–245, 1949.

    CAS  PubMed Central  Google Scholar 

  • Hao, L.-H., Wang, W.-X., Chen, C., Wang, Y.-F., Liu, T., Li, X., Shang, Z.-L.: Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein a subunit and reactive oxygen species. — Mol. Plant 5: 852–864, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Hatchikian, E.C., Forget, N., Fernandez, V.M., Williams, R., Cammack, R.: Further characterization of the [Fe]-hydrogenase from Desulfovibrio desulfuricans ATCC 7757. - Eur. J. Biochem. 209: 357–366, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Huang, C.S., Kawamura, T., Toyoda, Y., Nakao, A.: Recent advances in hydrogen research as a therapeutic medical gas. — Free Radical Res. 44: 971–982, 2010.

    Article  CAS  Google Scholar 

  • Jin, Q., Zhu, K., Cui, W., Xie, Y., Han, B.I.N., Shen, W.: Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. — Plant Cell Environ. 36: 956–969, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ju, C., Chang, C.: Mechanistic insights in ethylene perception and signal transduction. — Plant Physiol. 169: 85–95, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Kunkel, B.N., Brooks, D.M.: Cross talk between signaling pathways in pathogen defense. — Curr. Opin. Plant Biol. 5: 325–331, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Li, L.P., Ying, D.S., Zhang, R.L.: [Research and application progress of valuable genes of wild rice.] - Chin. J. tropic. Agr. 34: 34–41, 2014. [In Chin.]

    Google Scholar 

  • Liu, G., Lu, G., Zeng, L., Wang, G.L.: Two broad-spectrum blast resistance genes, Pi9 ( t ) and Pi2 ( t ), are physically linked on rice chromosome 6. — Mol. Genet. Genomics 267: 472–480, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Liu, T.Y., Chen, M.S.: [Genome evolution of Oryza.] - Biodiversity Science 22: 51–65, 2014. [In Chin.]

    Article  CAS  Google Scholar 

  • Lorenzo, O., Solano, R.: Molecular players regulating the jasmonate signalling network.- Curr. Opin. Plant Biol. 8: 532–540, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Meguro, A., Sato, Y.: Salicylic acid antagonizes abscisic acid inhibition of shoot growth and cell cycle progression in rice. — Sci. Rep. 4: 4555, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Melis, A., Melnicki, M.: Integrated biological hydrogen production. — Int. J. Hydrogen Energ. 31: 1563–1573, 2006.

    Article  CAS  Google Scholar 

  • Nakao, A., Toyoda, Y., Sharma, P., Evans, M., Guthrie, N.: Effectiveness of hydrogen rich water on antioxidant status of subjects with potential metabolic syndrome-an open label pilot study. — J. clin. Biochem. Nutr. 46: 140–149, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  • Norman-Setterblad, C., Vidal, S., Palva, E.T.: Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. — Mol. Plant-Microbe Interact. 13: 430–438, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Pieterse, C.M., Van Loon, L.C.: Salicylic acid-independent plant defence pathways. — Trends Plant Sci. 4: 52–58, 1999.

    Article  PubMed  Google Scholar 

  • Renwick, G.M., Giumarro, C., Siegel, S.M.: Hydrogen metabolism in higher plants. — Plant Physiol. 39: 303–306, 1964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reymond, P., Weber, H., Damond, M., Farmer, E.E.: Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. — Plant Cell 12: 707–719, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H., Hunt, M.D.: Systemic acquired resistance. — Plant Cell 8: 1809–1819, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryan, C.A.: The systemin signaling pathway differential activation of plant. — Biochim. biophys. Acta 1477: 112–121, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, S.S., Dietz, K.-J.: The relationship between metal toxicity and cellular redox imbalance. — Trends Plant Sci. 14: 43–50, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Shimada, A., Ueguchi-Tanaka, M., Nakatsu, T., Nakajima, M., Naoe, Y., Ohmiya, H., Kato, H., Matsuoka, M.: Structural basis for gibberellin recognition by its receptor GID1. — Nature 456: 520–523, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen, T.D., Livak, K.J.: Analyzing real-time PCR data by the comparative C(T) method. — Nat. Protocols 3: 1101–1108, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Thomma, B.P., Eggermont, K., Tierens, K.F., Broekaert, W.F.: Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. — Plant Physiol. 121: 1093–1101, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner, J.G., Christine E., A., D.: The jasmonate signal pathway.- Plant Cell 14 (Suppl.): S153–S164, 2002.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weng, H.B., Weng, H.B., Yuan, M.X., Xu, W.H.: [[FeFe]-hydrogenases of green glgae.] - Biotechnology 17: 89–91, 2007. [In Chin.]

    CAS  Google Scholar 

  • Xie, Y., Mao, Y., Lai, D., Zhang, W., Shen, W.: H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. — PLoS ONE 7: e49800, 2012.

    Article  Google Scholar 

  • Xie, Y., Mao, Y., Zhang, W., Lai, D., Wang, Q., Shen, W.: Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. — Plant Physiol. 165: 759–773, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, J., Tsuichihara, N., Etoh, T., Iwai, S.: Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening.- Plant Cell Environ. 30: 1320–1325, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Ye, M., Luo, S.M., Xie, J.F., Li, Y.F., Xu, T., Liu, Y., Song, Y.Y., Zhu-Salzman, K., Zeng, R.S.: Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. — PLoS ONE 8: e36214, 2012.

    Article  Google Scholar 

  • Zeng, J., Zhang, M., Sun, X.: molecular hydrogen is involved in phytohormone signaling and stress responses in plants. — PLoS ONE 8: e71038, 2013.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Y. Liu.

Additional information

Acknowledgements: This work was financially supported by the National Environmental Protection Public Welfare Science and Technology Research Program of China (grant No. 201309038) and the Special Program for New Transgenic Variety Breeding of the Ministry of Science and Technology, China (grant No. 2012ZX08011002).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, F., Li, J. & Liu, Y. Molecular hydrogen can take part in phytohormone signal pathways in wild rice. Biol Plant 60, 311–319 (2016). https://doi.org/10.1007/s10535-016-0591-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0591-9

Additional key words

Navigation