Overexpression of VaWRKY12, a transcription factor from Vitis amurensis with increased nuclear localization under low temperature, enhances cold tolerance of plants

Plant Molecular Biology - Tập 100 Số 1-2 - Trang 95-110 - 2019
Langlang Zhang1, Tingting Zhao1, Xiaoming Sun1, Yi Wang2, Can Du1, Zhenfei Zhu1, Duncan Kiragu Gichuki1, Qingfeng Wang1, Shaohua Li2, H. P. Xin1
1Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, People’s Republic of China
2Beijing Key Laboratory of Grape Sciences and Enology, CAS Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot 63(7):2667–2679

Borsani O, Valpuesta V, Botella A (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126(3):1024–1030

Cai H, Yang S, Yan Y, Xiao Z, Cheng J, Wu J et al (2015) CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper. J Exp Bot 66(11):3163–3174

Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CCI-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822

Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Bot 217(1):67–75

Damian O, Vera G, Patricia B, Roy B (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198:371–377

Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ et al (2013) CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 36(4):757–774

Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ (2014) WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J 79(5):810–823

Duan M, Zhang R, Zhu F, Zhang Z, Gou L, Wen J, Dong J, Wang T (2017) A lipid-anchored NAC transcription factor is translocated into the nucleus and activates glyoxalase I expression during drought stress. Plant Cell 29(7):1748–1772

Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206

Gong X, Zhang J, Hu J, Wang W, Wu H, Zhang Q, Liu JH (2015) FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ 38(11):2248–2262

Guo C, Guo R, Xu X, Gao M, Li X, Song J, Zheng Y, Wang X (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65(6):1513–1528

Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30(5):1229–1235

Hoecker U, Vasil IK, Mccarty DR (1995) Integrated control of seed maturation and germination programs by activator and repressor functions of viviparous-1 of maize. Gene Dev 9(20):2459–2469

Ishiguro S, Nakamura K (1994) Characterization of a cdna-encoding a novel DNA-binding protein, Spf1, that recognizes Sp8 sequences in the 5′ upstream regions of genes-coding for sporamin and beta-amylase from sweet-potato. Mol Gen Genet 244(6):563–571

Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102(14):5280–5285

Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20(11):3107–3121

Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plantarum 115(4):571–576

Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18(11):3132–3144

Kim SY, Kim SG, Kim YS, Seo PJ, Bae M, Yoon HK, Park CM (2007a) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res 35(1):203–213

Kim SG, Kim SY, Park CM (2007b) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226(3):647–654

Kim SG, Lee AK, Yoon HK, Park CM (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J 55(1):77–88

Kim SG, Lee S, Seo PJ, Kim SK, Kim JK, Park CM (2010) Genome-scale screening and molecular characterization of membrane-bound transcription factors in Arabidopsis and rice. Genomics 95(1):56–65

Kim MJ, Park MJ, Seo PJ, Song JS, Kim HJ, Park CM (2012) Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2.8 in the drought-stress response. Biochem J 448(3):353–363

Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130(4):2129–2141

Li Y, Zhang Q, Wu X (2001) Construction of recombinant vector which express hepatitis b surface antigen in tobacco and its transferation. Acta Agric Boreal-Occident Sin 10(1):41–43

Li HY, Ramalingam S, Chye ML (2006) Accumulation of recombinant SARS-CoV spike protein in plant cytosol and chloroplasts indicate potential for development of plant-derived oral vaccines. Exp Biol Med 231(8):1346–1352

Li H, Xu Y, Xiao Y, Zhu Z, Xie X, Zhao H, Wang Y (2010) Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta 232(6):1325–1337

Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233(6):1237–1252

Li JT, Wang NA, Xin HP, Li SH (2013) Overexpression of VaCBF4, a transcription factor from Vitis amurensis, improves cold tolerance accompanying increased resistance to drought and salinity in Arabidopsis. Plant Mol Biol Rep 31(6):1518–1528

Li J, Wang L, Zhu W, Wang N, Xin H, Li S (2014) Characterization of two VvICE1 genes isolated from ‘Muscat Hamburg’ grapevine and their effect on the tolerance to abiotic stresses. Sci Hortic-Ams Terdam 165:266–273

Li P, Song A, Gao C, Wang L, Wang Y, Sun J, Jiang J, Chen F, Chen S (2015) Chrysanthemum WRKY gene CmWRKY17 negatively regulates salt stress tolerance in transgenic chrysanthemum and Arabidopsis plants. Plant Cell Rep 34(8):1365–1378

Li S, Wang N, Ji D, Xue Z, Yu Y, Jiang Y, Liu J, Liu Z, Xiang F (2016) Evolutionary and functional analysis of membrane-bound NAC transcription factor genes in soybean. Plant Physiol 172(3):1804–1820

Liang M, Li H, Zhou F, Li H, Liu J, Hao Y, Wang Y, Zhao H, Han S (2015) Subcellular distribution of NTL transcription factors in Arabidopsis thaliana. Traffic 16(10):1062–1074

Liu JX, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19(12):4111–4119

Liu JX, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51(5):897–909

Liu H, Yang W, Liu D, Han Y, Zhang A, Li S (2011) Ectopic expression of a grapevine transcription factor VvWRKY11 contributes to osmotic stress tolerance in Arabidopsis. Mol Biol Rep 38(1):417–427

Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63(8):2933–2946

Marchive C, Mzid R, Deluc L, Barrieu F, Pirrello J, Gauthier A et al (2007) 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 58(8):1999–2010

Mare C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L (2004) Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 55(3):399–416

Mills LJ, Ferguson JC, Keller M (2006) Cold-hardiness evaluation of grapevine buds and cane tissues. Am J Enol Viticult 57:194–200

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498

Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio-Costet MF, Drira N, Hamdi S, Lauvergeat V (2007) Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 131(3):434–447

Ng S, Ivanova A, Duncan O, Law SR, Van Aken O, De Clercq I et al (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25(9):3450–3471

Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648–1655

Paul J. Rushton HM, Alison K, Huttly CM, Lazarus R Hooley (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of a-Amy2 genes. Plant Mol Biol. 29:691–702

Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63(3):417–429

Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41(11):1229–1234

Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. Embo J 15(20):5690–5700

Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258

Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290(3):998–1009

Seo PJ (2014) Recent advances in plant membrane-bound transcription factor research: emphasis on intracellular movement. J Integr Plant Biol 56(4):334–342

Seo PJ, Kim SG, Park CM (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13(10):550–556

Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010a) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61(4):661–671

Seo PJ, Kim MJ, Song JS, Kim YS, Kim HJ, Park CM (2010b) Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced changes in membrane fluidity. Biochem J 427(3):359–367

Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6(5):410–417

Sun X, Zhao T, Gan S, Ren X, Fang L, Karungo SK, Wang Y, Chen L, Li S, Xin H (2016) Ethylene positively regulates cold tolerance in grapevine by modulating the expression of ETHYLENE RESPONSE FACTOR 057. Sci Rep 6:24066

Sun X, Matus JT, Chern JWD, Wang Z, Chai F, Zhang L et al (2018) The GARP/MYB-related grape transcription factor AQUILO improves cold tolerance and promotes the accumulation of raffinose family oligosaccharides. J Exp Bot 69(7):1749–1764

Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126(1):45–51

Thomashow MF (1999) PLANT COLD ACCLIMATION freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

Tillett RL, Wheatley MD, Tattersall EA, Schlauch KA, Cramer GR, Cushman JC (2012) The Vitis vinifera C-repeat binding protein 4 (VvCBF4) transcriptional factor enhances freezing tolerance in wine grape. Plant Biotechnol J 10(1):105–124

Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7(5):491–498

Wang LN, Zhu W, Fang LC, Sun XM, Su LY, Liang ZC, Wang N, Londo JP, Li SH, Xin HP (2014) Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biol. 14:103

Wang F, Chen HW, Li QT, Wei W, Li W, Zhang WK et al (2015) GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. Plant J 83(2):224–236

Xiao H, Siddiqua M, Braybrook S, Nassuth A (2006) Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid. Plant Cell Environ 29(7):1410–1421

Xiao H, Tattersall EAR, Siddiqua MK, Cramer GR, Nassuth A (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ 31(1):1–10

Xiong L, Ishitani M, Zhu JK (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119(1):205–211

Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol 135(1):507–515

Xu W, Jiao Y, Li R, Zhang N, Xiao D, Ding X, Wang Z (2014a) Chinese wild-growing Vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis. PLoS ONE 9(7):e102303

Xu W, Zhang N, Jiao Y, Li R, Xiao D, Wang Z (2014b) The grapevine basic helix-loop-helix (bHLH) transcription factor positively modulates CBF-pathway and confers tolerance to cold-stress in Arabidopsis. Mol Biol Rep 41(8):5329–5342

Xu W, Li R, Zhang N, Ma F, Jiao Y, Wang Z (2014c) Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress. Plant Mol Bio 86(4–5):527–541

Yamaguchishinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88

Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63(7):2541–2556

Yang ZT, Wang MJ, Sun L, Lu SJ, Bi DL, Sun L, Song ZT, Zhang SS, Zhou SF, Liu JX (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10(3):e1004243

Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K et al (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64(16):5085–5097

Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572

Yoon HK, Kim SG, Kim SY, Park CM (2008) Regulation of leaf senescence by NTL9-mediated osmotic stress signaling in Arabidopsis. Mol Cell 25(3):438–445

Yu F, Huaxia Y, Lu W, Wu C, Cao X, Guo X (2012) GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biol 12:144

Yu Y, Liu Z, Wang L, Kim SG, Seo PJ, Qiao M et al (2016) WRKY71 accelerates flowering via the direct activation of FLOWERING LOCUS T and LEAFY in Arabidopsis thaliana. Plant J 85(1):96–106

Yuan Y, Fang L, Karungo SK, Zhang L, Gao Y, Li S, Xin H (2016) Overexpression of VaPAT1, a GRAS transcription factor from Vitis amurensis, confers abiotic stress tolerance in Arabidopsis. Plant Cell Rep 35(3):655–666

Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135(2):615–621

Zhang Y, Yu H, Yang X, Li Q, Ling J, Wang H, Gu X, Huang S, Jiang W (2016) CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner. Plant Physiol Bioch 108:478–487

Zhao J, Xin H, Qu L, Ning J, Peng X, Yan T, Ma L, Li S, Sun M (2011) Dynamic changes of transcript profiles after fertilization are associated with de novo transcription and maternal elimination in tobacco zygote, and mark the onset of the maternal-to-zygotic transition. Plant J 65(1):131–145

Zhao T, Wang Z, Su L, Sun X, Cheng J, Zhang L, Karungo SK, Han Y, Li S, Xin H (2017) An efficient method for transgenic callus induction from Vitis amurensis petiole. PLoS ONE 12(6):e0179730

Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48(4):592–605

Zhu Z, Shi J, Cao J, He M, Wang Y (2012) VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep 31(11):2109–2120