VvWRKY13 enhances ABA biosynthesis in Vitis vinifera

JIe Hao, Qian Ma, Lixia Hou, Fanggui Zhao, Liu Xin


Abscisic acid (ABA) plays critical roles in plant growth and development as well as in plants’ responses to abiotic stresses. We previously isolated VvWRKY13, a novel transcription factor, from Vitis vinifera (grapevine), and here we present evidence that VvWRKY13 may regulate ABA biosynthesis in plants. When VvWRKY13 was ectopically expressed in Arabidopsis, the transgenic lines showed delayed seed germination, smaller stomatal aperture size, and several other phenotypic changes, indicating elevated ABA levels in these plants. Sequence analysis of several genes that are involved in grapevine ABA synthetic pathway identified WRKY-specific binding elements (W-box or W-like box) in the promoter regions. Indeed, transient overexpression of VvWRKY13 in grapevine leaves significantly increased the transcript levels of ABA synthetic pathway genes. Taken together, we conclude that VvWRKY13 may promote ABA production by activating genes in the ABA synthetic pathway.


VvWRKY13; transcription factor; senescence; ABA; Vitis vinifera

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Taiz L, Zeiger E. Abscisic Acid: a seed maturation and antistress signal. In: Taiz L, Zeiger E, editors. Plant physiology. 4th ed. Sunderland: Sinauer Associates; 2006. p. 593–616.

Zeevaart JAD, Creelman RA. Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol. 1988;39(4):439–473. https://doi.org/10.1146/annurev.pp.39.060188.002255

Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, et al. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 1996;15(10):2331–2342.

Audran C, Liotenberg S, Gonneau M, North H, Frey A, Tap-Waksman K, et al. Localization and expression of zeaxanthin epoxidase mRNA in Arabidopsis in response to drought stress and during seed development. Aust J Plant Physiol. 2001;28(12):1161–1173.

Qin X. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA. 1999;96(26):15354–15361. https://doi.org/10.1073/pnas.96.26.15354

Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol. 2000;123(2):553–562. https://doi.org/10.1104/pp.123.2.553

Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, et al. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 2001;27(4):325–333. https://doi.org/10.1046/j.1365-313x.2001.01096.x

Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, et al. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell. 2002;14(11):2723–2743. https://doi.org/10.1105/tpc.006494

Gonzalez-Guzman M, Apostolova N, Belles JM, Barrero JM, Piqueras P, Ponce MR, et al. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell. 2002;14(8):1833–1846. https://doi.org/10.1105/tpc.002477

Seo M, Koiwai H, Akaba S, Komano T, Oritani T, Kamiya Y, et al. Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. Plant J. 2000;23(4):481–488. https://doi.org/10.1046/j.1365-313x.2000.00812.x

Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, et al. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. Embo J. 2004;23(7):1647–1656. https://doi.org/10.1038/sj.emboj.7600121

Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, et al. Arabidopsis CYP707As encode (+)-abscisic acid 8’-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol. 2004;134(4):1439–1449. https://doi.org/10.1104/pp.103.037614

Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B. PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res. 2010;38:822–827. https://doi.org/10.1093/nar/gkp805

Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. Embo J. 1999;18(17):4689–4699. https://doi.org/10.1093/emboj/18.17.4689

Yu D, Chen C, Chen Z. Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell. 2001;13(7):1527–1540. https://doi.org/10.1105/tpc.13.7.1527

Xiao J, Cheng T, Li X, Xiao J, Xu C, Wang S. Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selective binding to different cis-elements. Plant Physiol. 2013;163(4):1868–1882. https://doi.org/10.1104/pp.113.226019

Rushton PJ, Somssich IE, Ringler P, Shen QJ. WRKY transcription factors. Trends Plant Sci. 2010;15(5):247–258. https://doi.org/10.1016/j.tplants.2010.02.006

Yan H, Jia H, Chen X, Hao L, An H, Guo X. The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol. 2014;55(12):2060. https://doi.org/10.1093/pcp/pcu133

Liu S, Kracher B, Ziegler J, Birkenbihl RP, Somssich IE. Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100. eLife. 2015;4(e07295). https://doi.org/10.7554/eLife.07295

Marchive C, Mzid R, Deluc L, Barrieu F, Pirrello J, Gauthier A, et al. Isolation and characterization of a Vitis vinifera transcription factor, VvWRKY1, and its effect on responses to fungal pathogens in transgenic tobacco plants. J Exp Bot. 2007;58(8):1999–2010. https://doi.org/10.1093/jxb/erm062

Marchive C, Leon C, Kappel C, Coutos Thevenot P, Corio Costet MF, Delrot S, et al. Over-expression of VvWRKY1 in grapevines induces expression of jasmonic acid pathway-related genes and confers higher tolerance to the downy mildew. PLoS One. 2013;8(1):e54185. https://doi.org/10.1371/journal.pone.0054185

Merz RP, Moser T, Holl J, Kortekamp A, Buchholz G, Zyprian E, et al. The transcription factor VvWRKY33 is involved in the regulation of grapevine (Vitis vinifera) defense against the oomycete pathogen Plasmopara viticola. Physiol Plant. 2014;153(3):365–380. https://doi.org/10.1111/ppl.12251

Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio Costet MF, et al. Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant. 2007;131(3):434–447. https://doi.org/10.1111/j.1399-3054.2007.00975.x

Liu H, Yang W, Liu D, Han Y, Zhang A, Li S. Ectopic expression of a grapevine transcription factor VvWRKY11 contributes to osmotic stress tolerance in Arabidopsis. Mol Biol Rep. 2011;38(1):417–427. https://doi.org/10.1007/s11033-010-0124-0

Li H, Xu Y, Xiao Y, Zhu Z, Xie X, Zhao H, et al. Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta. 2010;232(6):1325–1337. https://doi.org/10.1007/s00425-010-1258-y

Zhu Z, Shi J, Cao J, He M, Wang Y. VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep. 2012;31(11):2109–2120. https://doi.org/10.1007/s00299-012-1321-1

Ma Q, Zhang G, Hou L, Wang W, Hao J, Liu X. Vitis vinifera VvWRKY13 is an ethylene biosynthesis-related transcription factor. Plant Cell Rep. 2015;34(9):1593–1603. https://doi.org/10.1007/s00299-015-1811-z

Santos-Rosa M, Poutaraud A, Merdinoglu D, Mestre P. Development of a transient expression system in grapevine via agro-infiltration. Plant Cell Rep. 2008;27(6):1053–1063. https://doi.org/10.1007/s00299-008-0531-z

Jefferson RA, Kavanagh TA, Bevan MW. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1988;6(13):3901–3907.

Ross ARS, Ambrose SJ, Cutler AJ, Feurtado JA, Kermode AR, Nelson K, et al. Determination of endogenous and supplied deuterated abscisic acid in plant tissues by high-performance liquid chromatography-electrospray ionization tandem mass spectrometry with multiple reaction monitoring. Anal Biochem. 2004;329(2):324–333. https://doi.org/10.1016/j.ab.2004.02.026

Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L. Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot. 2006;57(3):581–588. https://doi.org/10.1093/jxb/erj045

Burssens S, de Almeida Engler J, Beeckman T, Richard C, Shaul O, Ferreira P, et al. Developmental expression of the Arabidopsis thaliana CycA2;1 gene. Planta. 2000;211(5):623–631. https://doi.org/10.1007/s004250000333

Trevisan S, Pizzeghello D, Ruperti B, Francioso O, Sassi A, Palme K, et al. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element in Arabidopsis. Plant Biol (Stuttg). 2010;12(4):604–614. https://doi.org/10.1111/j.1438-8677.2009.00248.x

Lavenus J, Goh T, Guyomarch S, Hill K, Lucas M, Voß U, et al. Inference of the Arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones. Plant Cell. 2015;27(5):1368–1388. https://doi.org/10.1105/tpc.114.132993

Weaver LM, Gan S, Quirino B, Amasino RM. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol. 1998;37(3):455–469. https://doi.org/10.1023/A:1005934428906

Zhang K, Gan SS. An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 2012;158(2):961–969. https://doi.org/10.1104/pp.111.190876

de Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang H. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 2003;33(3):543–555. https://doi.org/10.1046/j.1365-313X.2003.01652.x

Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PM, et al. A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell. 2013;25(6):2132–2154. https://doi.org/10.1105/tpc.113.112896

Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, et al. Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot. 2004;55(407):2343–2351. https://doi.org/10.1093/jxb/erh276

Kim S, Kang JY, Cho DI, Park JH, Kim SY. ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 2004;40(1):75–87. https://doi.org/10.1111/j.1365-313X.2004.02192.x

Deak KI, Malamy J. Osmotic regulation of root system architecture. Plant J. 2005;43(1):17–28. https://doi.org/10.1111/j.1365-313X.2005.02425.x

Lukowitz W, Gillmor CS, Scheible WR. Positional cloning in Arabidopsis: why it feels good to have a genome initiative working for you. Plant Physiol. 2000;123(3):795–805. https://doi.org/10.1104/pp.123.3.795

Xiao L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, et al. Modulation of abscisic acid signal transduction and biosynthesis by Sm-like protein in Arabidopsis. Dev Cell. 2001;1(6):771–781. https://doi.org/10.1016/S1534-5807(01)00087-9

Signora L, de Smet I, Foyer CH, Zhang H. ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. 2001;28(6):655–662. https://doi.org/10.1046/j.1365-313x.2001.01185.x

Leon P, Sheen J. Sugar and hormone connections. Trends Plant Sci. 2003;8(3):110–116. https://doi.org/10.1016/S1360-1385(03)00011-6

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