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Overexpression of wheat TaNCED gene in Arabidopsis enhances tolerance to drought stress and delays seed germination

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Biologia Plantarum

Abstract

Abscisic acid (ABA) regulates various plant physiological processes, especially participates in the plant responses to harsh environments. The 9-cis-epoxycarotenoid dioxygenase (NCED) is a key enzyme in ABA biosynthesis pathway. Here, a TaNCED with an 1 887-bp open reading frame was cloned from wheat, which encodes a peptide of 628 amino acids. A chloroplast transit peptide sequence was found at the N-terminus of the TaNCED protein. Multiple sequence alignments indicate that the TaNCED protein shared high similarities with other NCEDs from different species. Real-time quantitative PCR analysis shows that expression of TaNCED was strongly up-regulated by treatments with ABA, polyethylene glycol, and drought stress, and it was down-regulated during germination of the wheat seeds. Ectopic overexpression of the TaNCED gene in Arabidopsis resulted in an increase of endogenous ABA and free proline content. A lower water loss rate and stomatal conductance of leaves were found in the transgenic plants in comparison with the wild type. Subsequently, the transgenic plants displayed an enhanced tolerance to drought stress but delayed seed germination. These data provide evidence that the TaNCED might play a primary role in regulation of ABA content during water stress and seed dormancy.

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Abbreviations

ABA:

abscisic acid

DEX:

dexamethasone

Fv/Fm :

variable to maximum chlorophyll fluorescence ratio (maximum efficiency of photosystem II)

g s :

stomatal conductance

NCED:

9-cis-epoxycarotenoid dioxygenase

ORF:

open reading frame

PCR:

polymerase chain reaction

PPFD:

photosynthetic photon flux density

vp14 :

viviparous 14

WT:

wild type

References

  • Ábrahám, E., Hourton-Cabassa, C., Erdei, L., Szabados, L.: Methods for determination of proline in plants. - In: Ramanjulu S. (ed.): Plant Stress Tolerance. Pp. 317–331. Springer, Berlin - Heidelberg 2010.

    Chapter  Google Scholar 

  • Chandler, P.M, Robertson M.: Gene expression regulated by abscisic acid and its relation to stress tolerance. - Annu. Rev. Plant Biol. 45: 113–141, 1994.

    Article  CAS  Google Scholar 

  • Chernys, J.T., Zeevaart, J.A.: Characterization of the 9-cisepoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. - Plant Physiol. 124: 343–354, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough, S.J., Bent, A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. - Plant J. 16: 735–743, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Davies, W.J., Zhang, J.: Root signals and the regulation of growth and development of plants in drying soil. - Annu. Rev. Plant Biol. 42: 55–76, 1991.

    Article  CAS  Google Scholar 

  • Destefano-Beltran, L., Knauber, D., Huckle, L., Suttle, J.C.: Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. - Plant mol. Biol. 61: 687–697, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Domínguez, F., González, M., Cejudo, F.J.: A germinationrelated gene encoding a serine carboxypeptidase is expressed during the differentiation of the vascular tissue in wheat grains and seedlings. - Planta 215: 727–734, 2002.

    Article  PubMed  Google Scholar 

  • Duckham, S., Linforth, R., Taylor, I.: Abscisic-acid-deficient mutants at the aba gene locus of Arabidopsis thaliana are impaired in the epoxidation of zeaxanthin. - Plant Cell Environ. 14: 601–606, 1991.

    Article  CAS  Google Scholar 

  • Frey, A., Effroy, D., Lefebvre, V., Seo, M., Perreau, F., Berger, A., Sechet, J., To, A., North, H.M., Marion-Poll, A.: Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. - Plant J. 70: 501–512, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Grappin, P., Bouinot, D., Sotta, B., Miginiac, E., Jullien, M.: Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance. - Planta 210: 279–285, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Gubler, F., Millar, A.A., Jacobsen, J.V.: Dormancy release, ABA and pre-harvest sprouting. - Curr. Opin. Plant Biol. 8: 183–187, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Hilhorst, H., Groot, S., Bino, R.: The tomato seed as a model system to study seed development and germination. - Acta bot. neerl. 47: 169–183, 1998.

    Google Scholar 

  • Hwang, S.G., Chen, H.C., Huang, W.Y., Chu, Y.C., Shii, C.T., Cheng, W.H.: Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. - Plant Sci. 178: 12–22, 2010.

    Article  CAS  Google Scholar 

  • Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: A stress-inducible gene for 9-cisepoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. - Plant Physiol. 123: 553–562, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. - Plant J. 27: 325–333, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Ji, X., Dong, B., Shiran, B., Talbot, M.J., Edlington, J.E., Hughes, T., White, R.G., Gubler, F., Dolferus, R.: Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. - Plant Physiol. 156: 647–662, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kende, H., Zeevaart, J.: The five “classical” plant hormones. - Plant Cell 9: 1197–1210, 1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koornneef, M., Lé on-Kloosterziel, K.M., Schwartz, S.H., Zeevaart, J.A.: The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. - Plant Physiol. Biochem. 36: 83–89, 1998.

    Article  CAS  Google Scholar 

  • Lefebvre, V., North, H., Frey, A., Sotta, B., Seo, M., Okamoto, M., Nambara, E., Marion-Poll, A.: Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. - Plant J. 45: 309–319, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Li, X.L., Yang, X., Hu, Y.X., Yu, X.D., Li, Q.L.: A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. - Plant Cell Rep. 33: 767–778, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Xu, S.S., Gao, J., Pan, S., Wang, G.X.: Chlorella induces stomatal closure via NADPH oxidase-dependent ROS production and its effects on instantaneous water use efficiency in Vicia faba. - PloS ONE 9: e93290, 2014.

    Article  Google Scholar 

  • Nambara, E., Marion-Poll, A.: Abscisic acid biosynthesis and catabolism. - Annu. Rev. Plant Biol. 56: 165–185, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Neves, D., Coelho-Filho, M., Bellete, B., Silva, M., Souza, D., Soares-Filho, W., Costa, M., Gesteira, A.: Comparative study of putative 9-cis-epoxycarotenoid dioxygenase and abscisic acid accumulation in the responses of Sunki mandarin and Rangpur lime to water deficit. - Mol. Biol. Rep. 40: 5339–5349, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Qin, X., Zeevaart, J.A.: The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. - Proc. nat. Acad. Sci. USA 96: 15354–15361, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin, X., Zeevaart, J.A.: Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. - Plant Physiol. 128: 544–551, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rampino, P., Pataleo, S., Gerardi, C., Mita, G., Perrotta, C.: Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. - Plant Cell Environ. 29: 2143–2152, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo, M.J., Alquezar, B., Zacarí as, L.: Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). - J. exp. Bot. 57: 633–643, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A., McCarty, D.R.: Specific oxidative cleavage of carotenoids by VP14 of maize. - Science 276: 1872–1874, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Tan, B.C., Joseph, L.M., Deng, W.T., Liu, L., Li, Q.B., Cline, K., McCarty, D.R.: Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family. - Plant J. 35: 44–56, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, A.J., Jackson, A.C., Parker, R.A., Morpeth, D.R., Burbidge, A., Taylor, I.B.: Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. - Plant mol. Biol. 42: 833–845, 2000a.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, A.J., Jackson, A.C., Symonds, R.C., Mulholland, B.J., Dadswell, A.R., Blake, P.S., Burbidge, A., Taylor, I.B.: Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. - Plant J. 23: 363–374, 2000b.

    Article  CAS  PubMed  Google Scholar 

  • Toh, S., Imamura, A., Watanabe, A., Nakabayashi, K., Okamoto, M., Jikumaru, Y., Hanada, A., Aso, Y., Ishiyama, K., Tamura, N.: High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. - Plant Physiol. 146: 1368–1385, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong, S., Ni, Z., Peng, H., Dong, G., Sun, Q.: Ectopic overexpression of wheat TaSrg6 gene confers water stress tolerance in Arabidopsis. - Plant Sci. 172: 1079–1086, 2007.

    Article  CAS  Google Scholar 

  • Wan, X.R., Li, L.: Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. - Biochem. biophys. Res. Commun. 347: 1030–1038, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Wang, Z., Dong, J., Wang, M., Gao, H.: Cloning of a 9-cis-epoxycarotenoid dioxygenase gene and the responses of Caragana korshinskii to a variety of abiotic stresses. - Genes Genet. Syst. 84: 397–405, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Woo, N.S., Badger, M.R., Pogson, B.J.: A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. - Plant Methods 4: 27, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xian, L., Sun, P., Hu, S., Wu, J., Liu, J.H.: Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses. - Planta 239: 61–77, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Xiong, L., Ishitani, M., Lee, H., Zhu, J.K.: The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stressresponsive gene expression. - Plant Cell 13: 2063–2083, 2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, J., Guo, Z.: Cloning of a 9-cis-epoxycarotenoid dioxygenase gene (SgNCED1) from Stylosanthes guianensis and its expression in response to abiotic stresses. - Plant Cell Rep. 26: 1383–1390, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S.J., Song, G.Q., Li, Y.L., Gao, J., Liu, J.J., Fan, Q.Q., Huang, C.Y., Sui, X.X., Chu, X.S., Guo, D., Li, G.Y.: Cloning of 9-cis-epoxycarotenoid dioxygenase gene (TaNCED1) from wheat and its heterologous expression in tobacco. - Biol. Plant. 58: 89–98, 2014.

    Article  Google Scholar 

  • Zhu, C., Kauder, F., Rö mer, S., Sandmann, G.: Cloning of two individual cDNAS encoding 9-cis-epoxycarotenoid dioxygenase from Gentiana lutea, their tissue-specific expression and physiological effect in transgenic tobacco. - J. Plant physiol. 164: 195–204, 2007.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to H.-S Hou.

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Acknowledgements: The first two authors contributed equally to this research.

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Tong, SM., Xi, HX., Ai, KJ. et al. Overexpression of wheat TaNCED gene in Arabidopsis enhances tolerance to drought stress and delays seed germination. Biol Plant 61, 64–72 (2017). https://doi.org/10.1007/s10535-016-0692-5

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  • DOI: https://doi.org/10.1007/s10535-016-0692-5

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