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ABA-dependent bZIP transcription factor, CsbZIP18, from Camellia sinensis negatively regulates freezing tolerance in Arabidopsis

Abstract

Key message

Overexpression of the tea plant gene CsbZIP18 in Arabidopsis impaired freezing tolerance, and CsbZIP18 is a negative regulator of ABA signaling and cold stress.

Abstract

Basic region/leucine zipper (bZIP) transcription factors play important roles in the abscisic acid (ABA) signaling pathway and abiotic stress response in plants. However, few bZIP transcription factors have been functionally characterized in tea plants (Camellia sinensis). In this study, a bZIP transcription factor, CsbZIP18, was found to be strongly induced by natural cold acclimation, and the expression level of CsbZIP18 was lower in cold-resistant cultivars than in cold-susceptible cultivars. Compared with wild-type (WT) plants, Arabidopsis plants constitutively overexpressing CsbZIP18 exhibited decreased sensitivity to ABA, increased levels of relative electrolyte leakage (REL) and reduced values of maximal quantum efficiency of photosystem II (Fv/Fm) under freezing conditions. The expression of ABA homeostasis- and signal transduction-related genes and abiotic stress-inducible genes, such as RD22, RD26 and RAB18, was suppressed in overexpression lines under freezing conditions. However, there was no significant change in the expression of genes involved in the C-repeat binding factor (CBF)-mediated ABA-independent pathway between WT and CsbZIP18 overexpression plants. These results indicate that CsbZIP18 is a negative regulator of freezing tolerance via an ABA-dependent pathway.

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References

  1. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129. https://doi.org/10.1105/tpc.108.058941

  2. Bensmihen S, Giraudat J, Francois P (2005) Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation. J Exp Bot 56:597–603. https://doi.org/10.1093/jxb/eri050

  3. Cao HL, Wang L, Yue C, Hao XY, Wang XC, Yang YJ (2015) Isolation and expression analysis of 18 CsbZIP genes implicated in abiotic stress responses in the tea plant (Camellia sinensis). Plant Physiol Bioch 97:432–442. https://doi.org/10.1016/j.plaphy.2015.10.030

  4. Chang Y, Nguyen BH, Xie YJ, Xiao B, Tang N, Zhu WL, Mou TM, Xiong LZ (2017) Co-overexpression of the constitutively active form of OsbZIP46 and ABA-activated protein kinase SAPK6 improves drought and temperature stress resistance in rice. Front Plant Sci 8:1102. https://doi.org/10.3389/fpls.2017.01102

  5. Chen H, Lai ZB, Shi JW, Xiao Y, Chen ZX, Xu XP (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281. https://doi.org/10.1186/1471-2229-10-281

  6. Choi HI, Hong JH, Ha JO, Kang JY, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730. https://doi.org/10.1074/jbc.275.3.1723

  7. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108:7247–7252. https://doi.org/10.1073/pnas.1102117108

  8. Ding YL, Li H, Zhang XY, Xie Q, Gong ZZ, Yang SH (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32:278–289. https://doi.org/10.1016/j.devcel.2014.12.023

  9. Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48. https://doi.org/10.1042/bse0580029

  10. Droge-Laser W, Snoek BL, Snel B, Weiste C (2018) The Arabidopsis bZIP transcription factor family-an update. Curr Opin Plant Biol 45:36–49. https://doi.org/10.1016/j.pbi.2018.05.001

  11. Dröge-Laser W, Weiste C (2018) The C/S1 bZIP network: a regulatory hub orchestrating plant energy homeostasis. Trends Plant Ssi 23:422–433. https://doi.org/10.1016/j.tplants.2018.02.003

  12. Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, Vicente-Carbajosa J, Dröge-Laser W (2006) Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46:890–900. https://doi.org/10.1111/j.1365-313X.2006.02731.x

  13. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690. https://doi.org/10.1105/tpc.003483

  14. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664. https://doi.org/10.1038/nature08599

  15. Fujita M, Mizukado S, Fujita Y, Ichikawa T, Nakazawa M, Seki M, Matsui M, Yamaguchi-Shinozaki K, Shinozaki K (2007) Identification of stress-tolerance-related transcription-factor genes via mini-scale Full-length cDNA Over-eXpressor (FOX) gene hunting system. Biochem Bioph Res Co 364:250–257. https://doi.org/10.1016/j.bbrc.2007.09.124

  16. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442. https://doi.org/10.1046/j.1365-313x.1998.00310.x

  17. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865. https://www.plantphysiol.org/content/124/4/1854

  18. Gusta LV, Wisniewski M, Nesbitt NT, Gusta ML (2004) The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and nonacclimated canola leaves. Plant Physiol 135:1642–1653. https://doi.org/10.1104/pp.103.028308

  19. Hao XY, Horvath DP, Chao WS, Yang YJ, Wang XC, Xiao B (2014) Identification and evaluation of reliable reference genes for quantitative real-time PCR analysis in tea plant (Camellia sinensis (L.) O. Kuntze). Int J Mol Sci 15:22155–22172. https://doi.org/10.3390/ijms151222155

  20. Hou Y, Wu AL, He YX, Li FD, Wei CL (2018) Genome-wide characterization of the basic leucine zipper transcription factors in Camellia sinensis. Tree Genet Genomes 14:27. https://doi.org/10.1007/s11295-018-1242-4

  21. Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499. https://doi.org/10.1146/annurev-arplant-050312-120053

  22. 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 102:5280–5285. https://doi.org/10.1073/pnas.0408941102

  23. Joo J, Lee YH, Song SI (2019) OsbZIP42 is a positive regulator of ABA signaling and confers drought tolerance to rice. Planta 249:1521–1533. https://doi.org/10.1007/s00425-019-03104-7

  24. Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177–3189. https://doi.org/10.1105/tpc.005272

  25. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357. https://doi.org/10.1105/tpc.010362

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

  27. Li YJ, Humbert S, Howell SH (2012) ZmbZIP60 mRNA is spliced in maize in response to ER stress. BMC Res Notes 5:144. https://doi.org/10.1186/1756-0500-5-144

  28. Li ZX, Srivastava R, Tang J, Zheng ZH, Howell SH (2018) Cis-effects condition the induction of a major unfolded protein response factor, ZmbZIP60, in response to heat stress in maize. Front Plant Sci 9:833. https://doi.org/10.3389/fpls.2018.00833

  29. Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240. https://doi.org/10.1007/s00425-008-0731-3

  30. Liu JX, Howell SH (2012) bZIP28 and NF-Y transcription factors are activated by ER Stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22:782–796. https://doi.org/10.1105/tpc.109.072173

  31. Liu JX, Srivastava R, Che P, Howell SH (2008) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119. https://doi.org/10.1105/tpc.106.050021

  32. Liu CT, Wu YB, Wang XP (2012) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235:1157–1169. https://doi.org/10.1007/s00425-011-1564-z

  33. Liu CT, Ou SJ, Mao BG, Tang JY, Wang W, Wang HR, Cao SY, Schläppi MR, Zhao BR, Xiao GY, Wang XP, Chu CC (2018) Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates. Nat Commun 9:3302–3312. https://doi.org/10.1038/s41467-018-05753-w

  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

  35. Lu GJ, Gao CX, Zheng XN, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229:605–615. https://doi.org/10.1007/s00425-008-0857-3

  36. Ma HZ, Liu C, Li ZX, Ran QJ, Xie GN, Wang BM, Fang S, Chu JF, Zhang JR (2018) ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol 178:753–770. https://doi.org/10.1104/pp.18.00436

  37. Nagashima Y, Mishiba KI, Suzuki E, Shimada Y, Iwata Y, Koizumi N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1:29. https://doi.org/10.1038/srep00029

  38. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95. https://doi.org/10.1104/pp.108.129791

  39. Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350. https://doi.org/10.1104/pp.107.112821

  40. Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T (2005) LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants. Plant Cell Physiol 46:1623–1634. https://doi.org/10.1093/pcp/pci178

  41. Tang N, Zhang H, Li XH, Xiao JH, Xiong LZ (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768. https://doi.org/10.1104/pp.111.190389

  42. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571

  43. Wang B, Zheng J, Liu YJ, Wang JH, Wang GY (2012a) Cloning and characterization of the stress-induced bZIP gene ZmbZIP60 from maize. Mol Biol Rep 39:6319–6327. https://doi.org/10.1007/s11033-012-1453-y

  44. Wang Y, Jiang CJ, Li YY, Wei CL, Deng WW (2012b) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant Cell Rep 31:27–34. https://doi.org/10.1007/s00299-011-1136-5

  45. Wang L, Ying YH, Narsai R, Ye LX, Zheng LQ, Tian JL, Whelan J, Shou HX (2013a) Identification of OsbHLH133 as a regulator of iron distribution between roots and shoots in Oryza sativa. Plant Cell Environ 36:224–236. https://doi.org/10.1111/j.1365-3040.2012.02569.x

  46. Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ, Jin JQ, Li X, Yang YJ (2013b) Global transcriptome profiles of Camellia sinensis during cold acclimation. Bmc Genom 14:415. https://doi.org/10.1186/1471-2164-14-415

  47. Wang L, Cao HL, Qian WJ, Yao LN, Hao XY, Li NN, Yang YJ, Wang XC (2017) Identification of a novel bZIP transcription factor in Camellia sinensis as a negative regulator of freezing tolerance in transgenic Arabidopsis. Ann Boy-Lond 119:1195–1209. https://doi.org/10.1093/aob/mcx011

  48. Wang L, Yao LN, Hao XY, Li NN, Wang YC, Ding CQ, Lei L, Qian WJ, Zeng JM, Yang YJ, Wang XC (2019) Transcriptional and physiological analyses reveal the association of ROS metabolism with cold tolerance in tea plant. Environ Exp Bot 160:45–58. https://doi.org/10.1016/j.envexpbot.2018.11.011

  49. Wei KF, Chen J, Wang YM, Chen YH, Chen SX, Lin Y, Pan S, Zhong XJ, Xie DX (2012) Genome-wide analysis of bZIP-encoding genes in maize. Dna Res 19:463–476. https://doi.org/10.1093/dnares/dss026

  50. Xiang Y, Tang N, Du H, Ye HY, Xiong LZ (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952. https://doi.org/10.1104/pp.108.128199

  51. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685. https://doi.org/10.1111/j.1365-313X.2009.04092.x

  52. Yue C, Cao HL, Wang L, Zhou YH, Huang YT, Hao XY, Wang YC, Wang B, Yang YJ, Wang XC (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88:591–608. https://doi.org/10.1007/s11103-015-0345-7

  53. Zong W, Tang N, Yang J, Peng L, Ma SQ, Xu Y, Li GL, Xiong ZL (2016) Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought resistance related genes. Plant Physiol. https://doi.org/10.1104/pp.16.00469

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Acknowledgements

This work was supported by the Central Public Interest Scientific Institution Basal Research Fund (1610212018007), the Young Elite Scientist Sponsorship Program by CAST (2016QNRC001), the National Natural Science Foundation of China (31870685) and the Earmarked Fund for China Agriculture Research System (CARS-19). We thank Professor Dr. Huixia Shou of Zhejiang University for providing vector PBI101.3.

Author information

YY, LW and XW conceived and designed the research; LY, XH, HC and CD performed the experiments; LY, LW and XW analyzed and discussed the data; LY and LW wrote the manuscript. All authors read and approved the manuscript.

Correspondence to Yajun Yang or Lu Wang.

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Yao, L., Hao, X., Cao, H. et al. ABA-dependent bZIP transcription factor, CsbZIP18, from Camellia sinensis negatively regulates freezing tolerance in Arabidopsis. Plant Cell Rep (2020). https://doi.org/10.1007/s00299-020-02512-4

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Keywords

  • ABA sensitivity
  • Cold stress
  • CsbZIP18
  • Tea plant (Camellia sinensis)
  • Transgenic Arabidopsis