Abstract
Main conclusion
TabZIP60 is found to interact with TaCDPK30 and act as a positive regulator of ABA synthesis-mediated salt tolerance in wheat.
Abstract
Wheat basic leucine zipper (bZIP) transcription factor (TabZIP60) was previously found to act as a positive regulator of salt resistance. However, its molecular mechanism in response to salt stress in wheat is still unclear. In this study, TabZIP60 was found to interact with wheat calcium-dependent protein kinase (TaCDPK30), which belonged to group III of CDPK family, and was induced by salt, polyethylene glycol, and abscisic acid (ABA) treatments. This mutation of serine 110 in TabZIP60 resulted in no interaction with TaCDPK30. Moreover, TaCDPK30 was involved in interactions with wheat protein phosphatase 2C clade A (TaPP2CA116/TaPP2CA121). TabZIP60-overexpressing wheat plants showed increased salt tolerance, as exhibited by better growth status, higher soluble sugar, and lower malonaldehyde contents of transgenic plants than wild-type wheat cv. Kenong 199 under salt stress. Moreover, transgenic lines showed high ABA content by upregulating ABA synthesis-related gene expression levels. TabZIP60 protein could bind and interact with the promoter of the wheat nine-cis epoxycarotenoid dioxygenase (TaNCED2) gene. Furthermore, TabZIP60 upregulated several stress response gene expression levels, which could also increase the plant’s ability to resist salt stress. Thus, these results suggest that TabZIP60 could function as a regulator of ABA synthesis-mediated salt tolerance through interacting with TaCDPK30 in wheat.
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Abbreviations
- bZIP:
-
Basic leucine zipper
- CDPK:
-
Calcium-dependent protein kinase
- ABA:
-
Abscisic acid
- PP2CA:
-
Protein phosphatase 2C clade A
- ABF:
-
ABA-responsive element-binding factor
- AREB:
-
ABA-responsive element-binding protein
- NCED:
-
Nine-cis epoxycarotenoid dioxygenase
References
Bao F, Du D, An Y, Yang W, Wang J, Cheng T, Zhang Q (2017) Overexpression of Prunus mume dehydrin genes in tobacco enhances tolerance to cold and drought. Front Plant Sci 8:151
Bedi S, Sengupta S, Ray A, Nag Chaudhuri R (2016) ABI3 mediates dehydration stress recovery response in Arabidopsis thaliana by regulating expression of downstream genes. Plant Sci 250:125–140
Bhatnagar N, Min MK, Choi EH, Kim N, Moon SJ, Yoon I, Kwon T, Jung KH, Kim BG (2017) The protein phosphatase 2C clade A protein OsPP2C51 positively regulates seed germination by directly inactivating OsbZIP10. Plant Mol Biol 93(4–5):389–401
Bi C, Yu Y, Dong C, Yang Y, Zhai Y, Du F, Xia C, Ni Z, Kong X, Zhang L (2021) The bZIP transcription factor TabZIP15 improves salt stress tolerance in wheat. Plant Biotechnol J 19(2):209–211
Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109(26):10593–10598
Chang Y, Nguyen BH, Xie Y, Xiao B, Tang N, Zhu W, Mou T, Xiong L (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
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139(4):1750–1761
Collin A, Daszkowska-Golec A, Kurowska M, Szarejko I (2020) Barley ABI5 (abscisic acid insensitive 5) is involved in abscisic acid-dependent drought response. Front Plant Sci 11:1138
Dröge-Laser W, Snoek BL, Snel B, Weiste C (2018) The Arabidopsis bZIP transcription factor family-an update. Curr Opin Plant Biol 45(Pt A):36–49
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993
Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8(1):93–102
Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1910
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Kirungu JN, Magwanga RO, Pu L, Cai X, Xu Y, Hou Y, Zhou Y, Cai Y, Hao F, Zhou Z, Wang K, Liu F (2020) Knockdown of Gh_A05G1554 (GhDHN_03) and Gh_D05G1729 (GhDHN_04) dehydrin genes, reveals their potential role in enhancing osmotic and salt tolerance in cotton. Genomics 112(2):1902–1915
Li S, Lin YJ, Wang P, Zhang B, Li M, Chen S, Shi R, Tunlaya-Anukit S, Liu X, Wang Z, Dai X, Yu J, Zhou C, Liu B, Wang JP, Chiang VL, Li W (2019) The AREB1 transcription factor influences histone acetylation to regulate drought responses and tolerance in Populus trichocarpa. Plant Cell 31(3):663–686
Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229(3):605–615
Lynch T, Erickson BJ, Finkelstein RR (2012) Direct interactions of ABA-insensitive (ABI)-clade protein phosphatase (PP)2Cs with calcium-dependent protein kinases and ABA response element-binding bZIPs may contribute to turning off ABA response. Plant Mol Biol 80(6):647–658
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
Ma H, Liu C, Li Z, Ran Q, Xie G, Wang B, Fang S, Chu J, Zhang J (2018) ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol 178(2):753–770
Martínez-Andújar C, Martínez-Pérez A, Albacete A, Martínez-Melgarejo PA, Dodd IC, Thompson AJ, Mohareb F, Estelles-Lopez L, Kevei Z, Ferrández-Ayela A, Pérez-Pérez JM, Gifford ML, Pérez-Alfocea F (2021) Overproduction of ABA in rootstocks alleviates salinity stress in tomato shoots. Plant Cell Environ 44(9):2966–2986
Muñiz García MN, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235(4):761–778
Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236–243
Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci U S A 106(41):17588–17593
Wang L, Hu W, Sun J, Liang X, Yang X, Wei S, Wang X, Zhou Y, Xiao Q, Yang G, He G (2015) Genome-wide analysis of SnRK gene family in Brachypodium distachyon and functional characterization of BdSnRK2.9. Plant Sci 237:33–45
Wen F, Ye F, Xiao Z, Liao L, Li T, Jia M, Liu X, Wu X (2020) Genome-wide survey and expression analysis of calcium-dependent protein kinase (CDPK) in grass Brachypodium distachyon. BMC Genomics 21(1):53
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60:796–804
Yang S, Xu K, Chen S, Li T, Xia H, Chen L, Liu H, Luo L (2019) A stress-responsive bZIP transcription factor OsbZIP62 improves drought and oxidative tolerance in rice. BMC Plant Biol 19(1):260
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(4):672–685
Zhang L, Zhang L, Xia C, Zhao G, Liu J, Jia J, Kong X (2015) A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol Plant 153(4):538–554
Zhang C, Li C, Liu J, Lv Y, Yu C, Li H, Zhao T, Liu B (2017a) The OsABF1 transcription factor improves drought tolerance by activating the transcription of COR413-TM1 in rice. J Exp Bot 68(16):4695–4707
Zhang L, Zhang L, Xia C, Gao L, Hao C, Zhao G, Jia J, Kong X (2017b) A novel wheat C-bZIP gene, TabZIP14-B, participates in salt and freezing tolerance in transgenic plants. Front Plant Sci 8:710
Zhang L, Xie J, Wang L, Si L, Zheng S, Yang Y, Yang H, Tian S (2020) Wheat TabZIP8, 9, 13 participate in ABA biosynthesis in NaCl-stressed roots regulated by TaCDPK9-1. Plant Physiol Biochem 151:650–658
Zhang L, Wang L, Chen X, Zhao L, Liu X, Wang Y, Wu G, Xia C, Zhang L, Kong X (2022a) The protein phosphatase 2C clade A TaPP2CA interact with calcium-dependent protein kinases, TaCDPK5/TaCDPK9–1, that phosphorylate TabZIP60 transcription factor from wheat (Triticum aestivum L.). Plant Sci 321:111304
Zhang H, Zhu J, Gong Z, Zhu JK (2022b) Abiotic stress responses in plants. Nat Rev Genet 23(2):104–119
Zhao P, Liu Y, Kong W, Ji J, Cai T, Guo Z (2021) Genome-wide identification and characterization of calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in Medicago truncatula. Int J Mol Sci 22(3):1044
Zhou X, Hao H, Zhang Y, Bai Y, Zhu W, Qin Y, Yuan F, Zhao F, Wang M, Hu J, Xu H, Guo A, Zhao H, Zhao Y, Cao C, Yang Y, Schumaker KS, Guo Y, Xie CG (2015) SOS2-Like Protein Kinase5, an SNF1-Related Protein Kinase3-type protein kinase, is important for abscisic acid responses in arabidopsis through phosphorylation of abscisic acid-insensitive5. Plant Physiol 168(2):659–676
Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273
Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19(10):3019–3036
Zong W, Tang N, Yang J, Peng L, Ma S, Xu Y (2016) Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes. Plant Physiol 171(4):2810–2825
Acknowledgements
This study was supported by the National Natural Science Foundation of China [31660392, 32260471], the Academic Backbone Project from the Northwest Normal University [2019GG-3], and the Young Teachers Improving Program from the Northwest Normal University [NWNU-LKQN-14-11].
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Zhang, L., Zhao, L., Wang, L. et al. TabZIP60 is involved in the regulation of ABA synthesis-mediated salt tolerance through interacting with TaCDPK30 in wheat (Triticum aestivum L.). Planta 257, 107 (2023). https://doi.org/10.1007/s00425-023-04141-z
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DOI: https://doi.org/10.1007/s00425-023-04141-z