Genes underlying cold acclimation in the tea plant (Camellia sinensis (L.) Kuntze)
https://doi.org/10.18699/VJ19.572
Abstract
The article reviews the latest studies showing the diversity of genetic mechanisms and gene families underlying the increased cold and frost tolerance of tea and other plant species. It has been shown that cell responses to chilling (0…+15°C) and freezing (< 0°C) are not the same and gene expression under cold stress is genotype-specific. In recent decades, progress has been made in understanding the genetic mechanisms underlying the cold response of plants – ICE1 (inducer of CBF expression 1), CBF (C-repeat-binding factor), COR (cold-regulated genes) pathways and signaling have been discovered. The ICE, CBF and DHN gene groups play a key role in the cold acclimation of the tea plant. The accumulation of CBF transcripts occurs after 15 min of chilling induction, and longer cold stress leads to accumulation of CBF transcripts. It is shown that the transcripts of the CsDHN1, CsDHN2 and CsDHN3 genes accumulate at a higher level in resistant genotypes of tea in comparison with susceptible cultivars during freezing. CBF-independent pathways include genes involved in metabolism and transcription factors such as HSFC1, ZAT12, CZF1, PLD (phospholipase D), WRKY, HD-Zip, CsLEA, LOX, NAC, HSP, which are widely distributed in plants and are involved in the basic mechanisms of tea resistance to cold and frost. The most recent studies show an important role of miRNA in the mechanisms of response to chilling and freezing in tea. The data obtained on different plant species may correlate with the mechanisms of frost tolerance of tea and are the basis for future studies of the signaling pathways of response to cold in the tea plant. The results of the research emphasize the need to further explore the ways in which various genes regulate the tolerance of tea to cold stress to find the molecular markers of frost tolerance.
Keywords
About the Authors
L. S. SamarinaRussian Federation
Sochi
L. S. Malyukova
Russian Federation
Sochi
M. V. Gvasaliya
Russian Federation
Sochi
A. M. Efremov
Russian Federation
Sochi
V. I. Malyarovskaya
Russian Federation
Sochi
S. V. Loshkareva
Russian Federation
Sochi
M. T. Tuov
Russian Federation
Sochi
References
1. Achard P., Gong F., Cheminant S., Alioua M., Hedden P., Genschik P. The coldinducible CBF1 factordependent signaling pathway modulates the accumulation of the growthrepressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell. 2008;20:21172129.
2. Ban Q., Wang X., Pan C., Wang Y., Kong L., Jiang H., Xu Y., Wang W., Pan Y., Li Y., Jiang Ch. Comparative analysis of the response and gene regulation in cold resistant and susceptible tea plants. PLoS One. 2017;12(12):e0188514. DOI 10.1371/journal.pone.0188514.
3. Cao H., Wang L., Yue C., Hao X., Wang X., Yang Y. Isolation and expression analysis of 18 CsbZIP genes implicated in abiotic stress responses in the tea plant (Camellia sinensis). Plant Physiol. Biochem. 2015;97:432442.
4. Chen J., Gao T., Wan S., Zhang Y., Yang J., Yu Y., Wang W. Genomewide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis). Int. J. Mol. Sci. 2018;19:2633. DOI 10.3390/ijms19092633.
5. Chinnusamy V., Ohta M., Kanrar S., Lee B.H., Hong X., Agarwal M., Zhu J.K. ICE1: a regulator of coldinduced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003;17:10431054.
6. Ding Z., Li C., Shi H., Wang H., Wang Y. Pattern of CsICE1 expression under cold or drought treatment and functional verification through analysis of transgenic Arabidopsis. Genet. Mol. Res. 2015;14:1125911270.
7. El Kayal W., Navarro M., Marque G., Keller G., Marque C., Teulieres C. Expression profile of CBFlike transcriptional factor genes from Eucalyptus in response to cold. J. Exp. Bot. 2006;57:24552469.
8. Eriksson M.E., Webb A.A.R. Plant cell responses to cold are all about timing. Curr. Opin. Plant Biol. 2011;14:731737.
9. Gao S.Q., Chen M., Xu Z.S. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol. Biol. 2011;75:537553.
10. Hua J. Defining roles of tandemly arrayed CBF genes in freezing tolerance with new genome editing tools. New Phytol. 2016;212: 301302.
11. 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;212:345353.
12. Kargiotidou A., Deli D., Galanopoulou D., Tsaftaris A., Farmaki T. Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). J. Exp. Bot. 2008;59:20432056. DOI 10.1093/jxb/ern065.
13. Kim J., Kang J.Y., Kim S.Y. Overexpression of a transcription factor regulating ABAresponsive gene expression confers multiple stress tolerance. Plant Biotechnol. J. 2004;2:459466.
14. Kitashiba H., Ishizaka T., Isuzugawa K., Nishimura K., Suzuki T. Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J. Plant Physiol. 2004;161: 11711176.
15. Li L., Lu X., Ma H., Lyu D. Jasmonic acid regulates the ascorbate–glutathione cycle in Malus baccata Borkh. roots under low rootzone temperature. Acta Physiol. Plant. 2017;39:174.
16. Li Q., Lei S., Du K., Li L., Pang X., Wang Zh., Wei M., Fu S., Hu L., Xu L. RNAseq based transcriptomic analysis uncovers αlinolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci. Rep. 2016;7(6):36463. DOI 10.1038/srep36463.
17. Li W.Q., Li M.Y., Zhang W.H., Welti R., Wang X.M. The plasma membranebound phospholipase D delta enhances freezing tolerance in Аrabidopsis thaliana. Nat. Biotechnol. 2004;22:427433. DOI 10.1038/nbt949.
18. Li W.Q., Wang R.P., Li M.Y., Li L.X., Wang C.M., Welti R., Wang X. Differential degradation of extraplastidic and plastidic lipids during freezing and postfreezing recovery in Arabidopsis thaliana. J. Biol. Chem. 2008;283:461468. DOI 10.1074/jbc.M706692200.
19. Li Y.Y., Zhou Y.Q., Xie X.F., Shu X.T., Deng W.W., Jiang C.J. Cloning and transcription analysis of dehydrin gene (CsDHN) in tea plant (Camellia sinensis). J. Agric. Biotechnol. 2016;24:332341.
20. Megha S., Basu U., Kav N.N.V. Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ. 2018;41:115.
21. Park S., Lee C.M., Doherty C.J., Gilmour S.J., Kim Y., Thomashow M.F. Regulation of the Arabidopsis CBF regulon by a complex lowtemperature regulatory network. Plant J. 2015;82:193207.
22. Paul A., Kumar S. Dehydrin2 is a stressinducible, whereas Dehyd rin1 is constitutively expressed but upregulated gene under varied cues in tea [Camellia sinensis (L.) O. Kuntze]. Mol. Biol. Rep. 2013;40: 38593863. DOI 10.1007/s1103301224662.
23. Pennycooke J.C., Cheng H., Stockinger E.J. Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes. Plant Physiol. 2008;146:12421254. DOI 10.1104/pp.107.108779.
24. SharabiSchwager M., Samach A., Porat R. Overexpression of the CBF2 transcriptional activator in Arabidopsis counteracts hormone activation of leaf senescence. Plant Signal Behav. 2010;5(3):296309.
25. Shen W., Li H., Teng R., Wang Y., Wang W., Zhuang J. Genomic and transcriptomic analyses of HD-Zip family transcription factors and their responses to abiotic stress in tea plant (Camellia sinensis). Genomics. 2018. DOI 10.1016/j.ygeno.2018.07.009.
26. Thomashow M.F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999;50:571599.
27. Vogel J.T., Zarka D.G., Van Buskirk H.A., Fowler S.G., Thomashow M.F. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005;41:195211.
28. Vyas D., Kumar S. Tea (Camellia sinensis (L.) O. Kuntze) clone with lower period of winter dormancy exhibits lesser cellular damage in response to low temperature. Plant Physiol. Biochem. 2005;43: 383388.
29. Wang L., Cao H., Qian W., Yao L., Hao X., Li N., Yang Y., Wang X. Identification of a novel bZIP transcription factor in Camellia sinensis as a negative regulator of freezing tolerance in transgenic Arabidopsis. Ann. Bot. 2017;119:11951209.
30. Wang L., Li X., Zhao Q., Jing Sh., Chen Sh., Yuan H. Identification of genes induced in response to lowtemperature treatment in tea leaves. Plant Mol. Biol. Rep. 2009;27:257265. DOI 10.1007/s1110500800797.
31. Wang W., Gao T., Chen J., Yang J., Huang H., Yu Y. The late embryogenesis abundant gene family in tea plant (Camellia sinensis): Genomewide characterization and expression analysis in response to cold and dehydration stress. Plant Physiol. Biochem. 2018;135:277286. DOI 10.1016/j.plaphy.2018.12.009.
32. Wang Y., Jiang C.J., Li Y.Y., Wei C.L., Deng W.W. CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant Cell Rep. 2012;31:2734. DOI 10.1007/s0029901111365.
33. Wang Y.X., Liu Z.W., Wu Z.J., Li H., Zhuang J. Transcriptomewide identification and expression analysis of the NAC gene family in tea plant [Camellia sinensis (L.) O. Kuntze] PLoS One. 2016a; 11(11):e0166727. DOI 10.1371/journal.pone.0166727.
34. Wang Y., Shu Z., Wang W., Jiang X., Li D., Pan J., Li X. CsWRKY2, a novel WRKY gene from Camellia sinensis, is involved in cold and drought stress responses. Biol. Plant. 2016b;60:443451. DOI 10.1007/s1053501606182.
35. Welling A., Palva E.T. Molecular control of cold acclimation in trees. Physiol. Plant. 2006;127:167181.
36. Wu Zh., Li X., Liu Zh., Li H., Wang Y., Zhuang J. Transcriptomebased discovery of AP2/ERF transcription factors related to temperature stress in tea plant (Camellia sinensis) Funct. Integr. Genomics. 2015; 15(6):741752. DOI 10.1007/s1014201504579.
37. Yin Y., Ma Q., Zhu Z., Cui Q., Chen Ch., Chen X., Fang W., Li X. Functional analysis of CsCBF3 transcription factor in tea plant (Camellia sinensis) under cold stress. Plant Growth Regul. 2016;80:335. DOI 10.1007/s1072501601720.
38. Yuan H.Y., Zhu X.P., Zeng W., Yang H.M., Sun N., Xie S.X., Cheng L. Isolation and transcription activation analysis of the CsCBF1 gene from Camellia sinensis. Acta Botanica BorealiOccidentalia Sinica. 2013;110:147151.
39. Yue C., Cao H.L., Wang L., Zhou Y.H., Huang Y.T., Hao X.Y., Wang Y.C., Wang B., Yang Y.J., Wang X.C. Effects of CA on sugar metabolism and sugarrelated gene expression in tea plant during the winter season. Plant Mol. Biol. 2015;88:591608. DOI 10.1007/s1110301503457.
40. Zhang L.L., Zhao M.G., Tian Q.Y., Zhang W.H. Comparative studies on tolerance of Medicago truncatula and Medicago falcata to freezing. Planta. 2011;234:445457. DOI 10.1007/s004250111416x.
41. Zhao Ch., Zhang Zh., Xie Sh., Si T., Li Y., Zhu J. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol. 2016;171:27442759.
42. Zhao Ch., Zhu J. The broad roles of CBF genes: From development to abiotic stress. Plant Signal. Behav. 2016;11:8. DOI 10.1080/15592324.2016.1215794.
43. Zheng C., Zhao L., Wang Y., Shen J., Zhang Y., Jia S., Li Y., Ding Z. Integrated RNASeq and sRNASeq analysis identifies chilling and freezing responsive key molecular players and pathways in tea plant (Camellia sinensis). PLoS One. 2015;10(4):e0125031. DOI 10.1371/journal.pone.0125031.
44. Zhu J., Wang X., Guo L., Xu Q., Zhao S., Li F., Yan X., Liu Sh., Wei Ch. Characterization and alternative splicing profiles of the lipoxygenase gene family in tea plant (Camellia sinensis). Plant Cell Physiol. 2018;59(9):17651781. DOI 10.1093/pcp/pcy091.