Discovery of cold-resistance genes in Vitis amurensis using bud-based quantitative trait locus mapping and RNA-seq

Fennell A. Freezing tolerance and injury in grapevines. J Crop Improv. 2004;10(1–2):201–35. Wang Z, Wong DCJ, Wang Y, Xu G, Ren C, Liu Y, Kuang Y, Fan P, Li S, Xin H, et al. GRAS-domain transcription factor PAT1 regulates jasmonic acid biosynthesis in grape cold stress response. Plant Physiol. 2021;186(3):1660–78. Wang Y, Xin H, Fan P, Zhang J, Liu Y, Dong Y, Wang Z, Yang Y, Zhang Q, Ming R, et al. The genome of Shanputao (Vitis amurensis) provides a new insight into cold tolerance of grapevine. Plant J. 2021;105(6):1495–506. Su K, Xing H, Guo Y, Zhao F, Liu Z, Li K, Li Y, Guo X. High-density genetic linkage map construction and cane cold hardiness QTL mapping for Vitis based on restriction site-associated DNA sequencing. BMC Genomics. 2020;21(1):419. Sun X, Zhang L, Wong DCJ, Wang Y, Zhu Z, Xu G, Wang Q, Li S, Liang Z, Xin H. The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance. Plant J. 2019;99(5):988–1002. Wang Z, Wang Y, Tong Q, Xu G, Xu M, Li H, Fan P, Li S, Liang Z. Transcriptomic analysis of grapevine Dof transcription factor gene family in response to cold stress and functional analyses of the VaDof17d gene. Planta. 2021;253(2):55. Sun X, Matus JT, Wong DCJ, Wang Z, Chai F, Zhang L, Fang T, Zhao L, Wang Y, Han Y, et al. The GARP/MYB-related grape transcription factor AQUILO improves cold tolerance and promotes the accumulation of raffinose family oligosaccharides. J Exp Bot. 2018;69(7):1749–64. Yu D, Zhang L, Zhao K, Niu R, Zhai H, Zhang J. VaERD15, a transcription factor gene associated with cold-tolerance in Chinese Wild Vitis amurensis. Front Plant Sci. 2017;8:297. Zhang L, Zhao T, Sun X, Wang Y, Du C, Zhu Z, Gichuki DK, Wang Q, Li S, Xin H. Overexpression of VaWRKY12, a transcription factor from Vitis amurensis with increased nuclear localization under low temperature, enhances cold tolerance of plants. Plant Mol Biol. 2019;100(1–2):95–110. Ju YL, Yue XF, Min Z, Wang XH, Fang YL, Zhang JX. VvNAC17, a novel stress-responsive grapevine (Vitis vinifera L.) NAC transcription factor, increases sensitivity to abscisic acid and enhances salinity, freezing, and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem. 2020;146:98–111. Gao Z, Li J, Luo M, Li H, Chen Q, Wang L, Song S, Zhao L, Xu W, Zhang C, et al. Characterization and cloning of grape circular RNAs identified the cold resistance-related Vv-circATS1. Plant Physiol. 2019;180(2):966–85. Hou L, Zhang G, Zhao F, Zhu D, Fan X, Zhang Z, Liu X. VvBAP1 is involved in cold tolerance in Vitis vinifera L. Front Plant Sci. 2018;9:726. Liu J, Shi Y, Yang S. Insights into the regulation of C-repeat binding factors in plant cold signaling. J Integr Plant Biol. 2018;60(9):780–95. Ding Y, Shi Y, Yang S. Molecular regulation of plant responses to environmental temperatures. Mol Plant. 2020;13(4):544–64. Guo Y, Shi G, Liu Z, Zhao Y, Yang X, Zhu J, Li K, Guo X. Using specific length amplified fragment sequencing to construct the high-density genetic map for Vitis (Vitis vinifera L. x Vitis amurensis Rupr.). Front Plant Sci. 2015;6:393. Jones DF. Gene action in heterosis. Genetics. 1957;42:93–103. Gowda M, Longin CFH, Lein V, Reif JC. Relevance of specific versus general combining ability in winter wheat. Crop Sci. 2012;52(6):2494–500. Tao Z, Xian LN, Kai FJ, Hua FD, Qing H, Qian-h-Hua Y, Li Y, XianQi W, Ying-Jiang C, Jia-Kui Z. Relationship between heterosis and parental genetic distance based on molecular markers for functional genes related to yield traits in rice. Rice Sci. 2010;17(4):288–95. Hajela RK, Horvath DP, Gilmour SJ, Thomashow MF. Molecular cloning and expression of cor (Cold-Regulated) genes in Arabidopsis thaliana. Plant Physiol. 1990;93(3):1246–52. Zhang L, Guo X, Zhang Z, Wang A, Zhu J. Cold-regulated gene LeCOR413PM2 confers cold stress tolerance in tomato plants. Gene. 2021;764:145097. Hwarari D, Guan Y, Ahmad B, Movahedi A, Min T, Hao Z, Lu Y, Chen J, Yang L. ICE-CBF-COR signaling cascade and its regulation in plants responding to cold stress. Int J Mol Sci. 2022;23(3):1549. Guo W, Ward RW, Thomashow MF. Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol. 1992;100(2):915–22. Horvath DP, McLarney BK, Thomashow MF. Regulation of Arabidopsis thaliana L. (Heyn) cor78 in response to low temperature. Plant Physiol. 1993;103(4):1047–53. Uemura M, Gilmour SJ, Thomashow MF, Steponkus PL. Effects of COR6.6 and COR15am polypeptides encoded by COR (cold-regulated) genes of Arabidopsis thaliana on the freeze-induced fusion and leakage of liposomes. Plant Physiol. 1996;111(1):313–27. Zhou M, Wu L, Liang J, Shen C, Lin J. Expression analysis and functional characterization of a novel cold-responsive gene CbCOR15a from Capsella bursa-pastoris. Mol Biol Rep. 2012;39(5):5169–79. Thalhammer A, Bryant G, Sulpice R, Hincha DK. Disordered cold regulated15 proteins protect chloroplast membranes during freezing through binding and folding, but do not stabilize chloroplast enzymes in vivo. Plant Physiol. 2014;166(1):190–201. Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol. 2016;212(2):345–53. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol. 2016;171(4):2744–59. Breton G, Danyluk J, Charron JB, Sarhan F. Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol. 2003;132(1):64–74. Okawa K, Nakayama K, Kakizaki T, Yamashita T, Inaba T. Identification and characterization of Cor413im proteins as novel components of the chloroplast inner envelope. Plant Cell Environ. 2008;31(10):1470–83. Ma X, Wang G, Zhao W, Yang M, Ma N, Kong F, Dong X, Meng Q. SlCOR413IM1: a novel cold-regulation gene from tomato, enhances drought stress tolerance in tobacco. J Plant Physiol. 2017;216:88–99. Wang J, Zuo K-J, Qin J, Zhang L, Su L, Liu J, Ling H, Zhao J-Y, Cao Y-F, Tang K-X. Isolation and bioinformatics analyses of a COR413-like gene from Gossypium barbadense. Acta Physiol Plant. 2006;29(1):1–9. Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F. Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep. 2014;41(2):815–22. Ma X, Chen C, Yang M, Dong X, Lv W, Meng Q. Cold-regulated protein (SlCOR413IM1) confers chilling stress tolerance in tomato plants. Plant Physiol Biochem. 2018;124:29–39. Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 2018;23(7):623–37. Dong C, Zhang Z, Ren J, Qin Y, Huang J, Wang Y, Cai B, Wang B, Tao J. Stress-responsive gene ICE1 from Vitis amurensis increases cold tolerance in tobacco. Plant Physiol Biochem. 2013;71:212–7. Xu W, Jiao Y, Li R, Zhang N, Xiao D, Ding X, Wang Z. Chinese wild-growing Vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis. PLoS One. 2014;9(7):e102303. Considine MJ, Foyer CH. Redox regulation of plant development. Antioxid Redox Signal. 2014;21(9):1305–26. Cui XY, Gao Y, Guo J, Yu TF, Zheng WJ, Liu YW, Chen J, Xu ZS, Ma YZ. BES/BZR transcription factor TaBZR2 positively regulates drought responses by activation of TaGST1. Plant Physiol. 2019;180(1):605–20. Abdul Kayum M, Nath UK, Park JI, Biswas MK, Choi EK, Song JY, Kim HT, Nou IS. Genome-wide identification, characterization, and expression profiling of Glutathione S-Transferase (GST) Family in pumpkin reveals likely role in cold-stress tolerance. Genes (Basel). 2018;9(2):84. Zhang Y, Ming R, Khan M, Wang Y, Dahro B, Xiao W, Li C, Liu JH. ERF9 of Poncirus trifoliata (L.) Raf. undergoes feedback regulation by ethylene and modulates cold tolerance via regulating a glutathione S-transferase U17 gene. Plant Biotechnol J. 2022;20(1):183–200. Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JH, et al. Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell. 2013;25(6):2115–31. Lin T, Yang W, Lu W, Wang Y, Qi X. Transcription factors PvERF15 and PvMTF-1 form a cadmium stress transcriptional pathway. Plant Physiol. 2017;173(3):1565–73. Zhuo C, Liang L, Zhao Y, Guo Z, Lu S. A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation. Plant Cell Environ. 2018;41(9):2021–32. Bouzroud S, Gasparini K, Hu G, Barbosa MAM, Rosa BL, Fahr M, Bendaou N, Bouzayen M, Zsogon A, Smouni A, et al. Down regulation and loss of auxin response factor 4 function using CRISPR/Cas9 alters plant growth, stomatal function and improves tomato tolerance to salinity and osmotic stress. Genes (Basel). 2020;11(3):272. Xu L, Wang D, Liu S, Fang Z, Su S, Guo C, Zhao C, Tang Y. Comprehensive atlas of wheat (Triticum aestivum L.) auxin response factor expression during male reproductive development and abiotic stress. Front Plant Sci. 2020;11:586144. Su L, Xu M, Zhang J, Wang Y, Lei Y, Li Q. Genome-wide identification of auxin response factor (ARF) family in kiwifruit (Actinidia chinensis) and analysis of their inducible involvements in abiotic stresses. Physiol Mol Biol Plants. 2021;27(6):1261–76. Wang Y, Jiang H, Mao Z, Liu W, Jiang S, Xu H, Su M, Zhang J, Wang N, Zhang Z, et al. Ethylene increases the cold tolerance of apple via the MdERF1B-MdCIbHLH1 regulatory module. Plant J. 2021;106(2):379–93. Tang Y, Du G, Xiang J, Hu C, Li X, Wang W, Zhu H, Qiao L, Zhao C, Wang J, et al. Genome-wide identification of auxin response factor (ARF) gene family and the miR160-ARF18-mediated response to salt stress in peanut (Arachis hypogaea L.). Genomics. 2022;114(1):171–84. Aslam M, Sugita K, Qin Y, Rahman A. Aux/IAA14 regulates microRNA-mediated cold stress response in Arabidopsis roots. Int J Mol Sci. 2020;21(22):8441. Chen D, Wang W, Wu Y, Xie H, Zhao L, Zeng Q, Zhan Y. Expression and distribution of the auxin response factors in Sorghum bicolor during development and temperature stress. Int J Mol Sci. 2019;20(19):4816. Wang M, Dai W, Du J, Ming R, Dahro B, Liu JH. ERF109 of trifoliate orange (Poncirus trifoliata (L.) Raf.) contributes to cold tolerance by directly regulating expression of Prx1 involved in antioxidative process. Plant Biotechnol J. 2019;17(7):1316–32. Khan M, Hu J, Dahro B, Ming R, Zhang Y, Wang Y, Alhag A, Li C, Liu JH. ERF108 from Poncirus trifoliata (L.) Raf. functions in cold tolerance by modulating raffinose synthesis through transcriptional regulation of PtrRafS. Plant J. 2021;108(3):705–24. Sun X, Zhao T, Gan S, Ren X, Fang L, Karungo SK, Wang Y, Chen L, Li S, Xin H. Ethylene positively regulates cold tolerance in grapevine by modulating the expression of ethylene response factor 057. Sci Rep. 2016;6:24066. Xie Y, Chen P, Yan Y, Bao C, Li X, Wang L, Shen X, Li H, Liu X, Niu C, et al. An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol. 2018;218(1):201–18. An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ. R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple. Plant J. 2018;96(3):562–77. An JP, Wang XF, Zhang XW, Xu HF, Bi SQ, You CX, Hao YJ. An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation. Plant Biotechnol J. 2020;18(2):337–53. Xing C, Liu Y, Zhao L, Zhang S, Huang X. A novel MYB transcription factor regulates ascorbic acid synthesis and affects cold tolerance. Plant Cell Environ. 2019;42(3):832–45. Yang X, Luo Y, Bai H, Li X, Tang S, Liao X, Zhang L, Liu Q. DgMYB2 improves cold resistance in chrysanthemum by directly targeting DgGPX1. Hortic Res.2022;9:uhab028. Xie XB, Li S, Zhang RF, Zhao J, Chen YC, Zhao Q, Yao YX, You CX, Zhang XS, Hao YJ. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ. 2012;35(11):1884–97. Xu W, Zhang N, Jiao Y, Li R, Xiao D, Wang Z. The grapevine basic helix-loop-helix (bHLH) transcription factor positively modulates CBF-pathway and confers tolerance to cold-stress in Arabidopsis. Mol Biol Rep. 2014;41(8):5329–42. Zhang Y, Yu H, Yang X, Li Q, Ling J, Wang H, Gu X, Huang S, Jiang W. 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 Biochem. 2016;108:478–87. Yang Y, Liu J, Zhou X, Liu S, Zhuang Y. Identification of WRKY gene family and characterization of cold stress-responsive WRKY genes in eggplant. PeerJ. 2020;8:e8777. Mills LJ, Ferguson JC, Keller M. Cold-hardiness evaluation of grapevine buds and cane tissues. Am J Enol Vitcult. 2006;57(2):194-200. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30. Kanehisa M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 2019;28(11):1947–51. Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res. 2021;49(D1):D545–51. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics (Oxford, England). 2003;19(7):889–90. Fujimori N, Enoki S, Suzuki A, Naznin HA, Shimizu M, Suzuki S. Grape apoplasmic β-1,3-glucanase confers fungal disease resistance in Arabidopsis. Sci Hortic. 2016;200:105–10.