TaBZR1 enhances wheat salt tolerance via promoting ABA biosynthesis and ROS scavenging

Ruizhen Yang; Ziyi Yang; Meng Xing; Yexing Jing; Yunwei Zhang; Kewei Zhang; Yun Zhou; Huixian Zhao; Weihua Qiao; Jiaqiang Sun

doi:10.1016/j.jgg.2023.09.006

Volume 50 Issue 11

Nov. 2023

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Article Navigation > Journal of Genetics and Genomics > 2023 > 50(11): 861-871

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TaBZR1 enhances wheat salt tolerance via promoting ABA biosynthesis and ROS scavenging

doi: 10.1016/j.jgg.2023.09.006

a. State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China;
b. College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, China;
c. National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya, Hainan 572024, China;
d. Institute of Plant Genetics and Developmental Biology, College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, Zhejiang 321004, China;
e. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, Henan 475001, China;
f. State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi 712100, China

Funds:

This work was supported by the Hainan Yazhou Bay Seed Laboratory (B21HJ0215), an open project of the State Key Laboratory of Crop Stress Adaptation and Improvement at Henan University (2021KF03), the Central Public-interest Scientific Institution Basal Research Fund (S2022ZD02) and Agricultural Science and Technology Innovation Program of CAAS. We thank Beijing Genovo Biotechnology Co., Ltd. for their assistance with the generation of transgenic bread wheat plants.

Received Date: 2023-07-19
Accepted Date: 2023-09-12
Rev Recd Date: 2023-09-12
Publish Date: 2023-09-19

Abstract

Abstract

Brassinosteroids (BRs) are vital plant steroid hormones involved in numerous aspects of plant life including growth, development, and responses to various stresses. However, the underlying mechanisms of how BR regulates abiotic stress responses in wheat (Triticum aestivum L.) remain to be elucidated. Here, we find that BR signal core transcription factor BRASSINAZOLE-RESISTANT1 (TaBZR1) is significantly up-regulated by salt treatment. Overexpression of Tabzr1-1D (a gain-of-function TaBZR1 mutant protein) improves wheat salt tolerance. Furthermore, we show that TaBZR1 binds directly to the G-box motif in the promoter of ABA biosynthesis gene TaNCED3 to activate its expression and promotes ABA accumulation. Moreover, TaBZR1 associates with the promoters of ROS-scavenging genes TaGPX2 and TaGPX3 to activate their expression. Taken together, our results elucidate that TaBZR1 improves salt-stress tolerance by activating some genes involved in the biosynthesis of ABA and ROS scavenging in wheat, which gives us a new strategy to improve the salt tolerance of wheat.
- Wheat,
- TaBZR1,
- Salt stress,
- ABA,
- ROS

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References(58)

References

Baxter, A., Mittler, R., Suzuki, N., 2014. ROS as key players in plant stress signalling. J Exp Bot 65, 1229-1240.

Byrt, C.S., Xu, B., Krishnan, M., Lightfoot, D.J., Athman, A., Jacobs, A.K., Watson-Haigh, N.S., Plett, D., Munns, R., Tester, M., Gilliham, M., 2014. The Na(+) transporter, TaHKT1;5-D, limits shoot Na(+) accumulation in bread wheat. Plant J 80, 516-526.

Cano-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-Garcia, S., Cheng, J.C., Nam, K.H., Li, J., Chory, J., 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341-5351.

Cao, X., Ma, W., Zeng, F., Cheng, Y., Ma, Z., Mao, J., Chen, B., 2023. Grape BES1 transcription factor gene VvBES1-3 confers salt tolerance in transgenic Arabidopsis. Gene 854, 147059.

Chen, K., Li, G.J., Bressan, R.A., Song, C.P., Zhu, J.K., Zhao, Y., 2020. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62, 25-54.

Chung, Y., Kwon, S.I., Choe, S., 2014. Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol Cells 37, 795-803.

Clouse, S.D., 1998. BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development. Annu Rev Plant Physiol Plant Mol Biol. 49, 427-451.

Cui, X.Y., Gao, Y., Guo, J., Yu, T.F., Zheng, W.J., Liu, Y.W., Chen, J., Xu, Z.S., Ma, Y.Z., 2019. BES/BZR Transcription Factor TaBZR2 Positively Regulates Drought Responses by Activation of TaGST1. Plant Physiol 180, 605-620.

Dong, H., Li, D., Yang, R., Zhang, L., Zhang, Y., Liu, X., Kong, X., Sun, J., 2023. GSK3 phosphorylates and regulates the Green Revolution protein Rht-B1b to reduce plant height in wheat. Plant Cell 35, 1970-1983.

Dong, H., Yan, S., Jing, Y., Yang, R., Zhang, Y., Zhou, Y., Zhu, Y., Sun, J., 2021. MIR156-Targeted SPL9 Is Phosphorylated by SnRK2s and Interacts With ABI5 to Enhance ABA Responses in Arabidopsis. Front Plant Sci 12, 708573.

Faris, J.D., 2014. Wheat domestication: key to agricultural revolutions past and future. Genomics of plant genetic resources. Netherlands: Springer, 439-464.

Feng, L., Li, Y., Zhou, Y.-L., Meng, G.-H., Ji, Z.-L., Lin, W.-H., He, J.-X., 2023. Integrative transcriptomic and proteomic analyses reveal a positive role of BES1 in salt tolerance in Arabidopsis. Front Plant Sci. 14, 1034393.

Gui, J., Zheng, S., Liu, C., Shen, J., Li, J., Li, L., 2016. OsREM4.1 Interacts with OsSERK1 to Coordinate the Interlinking between Abscisic Acid and Brassinosteroid Signaling in Rice. Dev Cell 38, 201-213.

Han, C., Wang, L., Lyu, J., Shi, W., Yao, L., Fan, M., Bai, M.Y., 2023. Brassinosteroid signaling and molecular crosstalk with nutrients in plants. J Genet Genomics. 50, 541-553.

He, G., Zhang, Y., Liu, P., Jing, Y., Zhang, L., Zhu, Y., Kong, X., Zhao, H., Zhou, Y., Sun, J., 2021. The transcription factor TaLAX1 interacts with Q to antagonistically regulate grain threshability and spike morphogenesis in bread wheat. New Phytol. 230, 988-1002.

He, J.X., Gendron, J.M., Yang, Y.L., Li, J.M., Wang, Z.Y., 2002. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis Proceedings of the National Academy of Sciences of the United States of America 99, 10185-10190.

Huang, Y., Guo, Y., Liu, Y., Zhang, F., Wang, Z., Wang, H., Wang, F., Li, D., Mao, D., Luan, S., Liang, M., Chen, L., 2018. 9-cis-Epoxycarotenoid Dioxygenase 3 Regulates Plant Growth and Enhances Multi-Abiotic Stress Tolerance in Rice. Front Plant Sci 9, 162.

Huang, Y., Jiao, Y., Xie, N., Guo, Y., Zhang, F., Xiang, Z., Wang, R., Wang, F., Gao, Q., Tian, L., Li, D., Chen, L., Liang, M., 2019. OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Sci 287, 110188.

Jia, C., Zhao, S., Bao, T., Zhao, P., Peng, K., Guo, Q., Gao, X., Qin, J., 2021. Tomato BZR/BES transcription factor SlBZR1 positively regulates BR signaling and salt stress tolerance in tomato and Arabidopsis. Plant Sci 302, 110719.

Jiang, J., Zhang, C., Wang, X., 2015. A recently evolved isoform of the transcription factor BES1 promotes brassinosteroid signaling and development in Arabidopsis thaliana. Plant Cell 27, 361-374.

Kavi Kishor, P.B., Tiozon, R.N., Jr., Fernie, A.R., Sreenivasulu, N., 2022. Abscisic acid and its role in the modulation of plant growth, development, and yield stability. Trends Plant Sci. 27, 1283-1295.

Kesawat, M.S., Kherawat, B.S., Singh, A., Dey, P., Kabi, M., Debnath, D., Saha, D., Khandual, A., Rout, S., Manorama Ali, A, Palem, R.R., Gupta, R., Kadam, A.A., Kim, H.U., Chung, S.M., Kumar, M., 2021. Genome-Wide Identification and Characterization of the Brassinazole-resistant (BZR) Gene Family and Its Expression in the Various Developmental Stage and Stress Conditions in Wheat (Triticum aestivum L.). Int J Mol Sci 22, 8743.

Kim, T.W., Guan, S., Sun, Y., Deng, Z., Tang, W., Shang, J.X., Sun, Y., Burlingame, A.L., Wang, Z.Y., 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11, 1254-1260.

Lei, Y., Cui, Y., Cui, R., Chen, X., Wang, J., Lu, X., Wang, D., Wang, S., Guo, L., Zhang, Y., Rui, C., Fan, Y., Han, M., Zhao, L., Zhang, H., Liu, X., Xu, N., Wang, J., Huang, H., Feng, X., Xi, Y., Ni, K., Zhang, M., Jiang, T., Ye, W., 2023. Characterization and gene expression patterns analysis implies BSK family genes respond to salinity stress in cotton. Front Genet 14, 1169104.

Li, Q., Xu, F., Chen, Z., Teng, Z., Sun, K., Li, X., Yu, J., Zhang, G., Liang, Y., Huang, X., Du, L., Qian, Y., Wang, Y., Chu, C., Tang, J., 2021. Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nat Plants 7, 1108-1118.

Li, H., Ye, K.Y., Shi, Y.T., Cheng, J.K., Zhang, X.Y., Yang, S.H., 2017. BZR1 Positively Regulates Freezing Tolerance via CBF-Dependent and CBF-Independent Pathways in Arabidopsis. Mol Plant 10, 545-559.

Li, J., Wen, J.Q., Walker, J.C., Lease, K.A., Doke, J.T., Tax, F.E., 2002. BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling. Cell 110, 213-222.

Li, J., Zhou, X., Wang, Y., Song, S., Ma, L., He, Q., Lu, M., Zhang, K., Yang, Y., Zhao, Q., Jin, W., Jiang, C., Guo, Y., 2023. Inhibition of the maize salt overly sensitive pathway by ZmSK3 and ZmSK4. J Genet Genomics S1673-8527(23)00097-00098.

Li, J.F., Zhou, H.P., Zhang, Y., Li, Z., Yang, Y.Q., Guo, Y., 2020. The GSK3-like Kinase BIN2 Is a Molecular Switch between the Salt Stress Response and Growth Recovery in Arabidopsis thaliana. Dev Cell 55, 367-380.

Liu, S., Liu, S., Wang, M., Wei, T., Meng, C., Wang, M., Xia, G., 2014. A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell 26, 164-180.

Liu, L., Sun, Y., Di, P., Cui, Y., Meng, Q., Wu, X., Chen, Y., Yuan, J., 2022. Overexpression of a Zea mays Brassinosteroid-Signaling Kinase Gene ZmBSK1 Confers Salt Stress Tolerance in Maize. Front Plant Sci 13, 894710.

Liu, J., Xia, C., Dong, H., Liu, P., Yang, R., Zhang, L., Liu, X., Jia, J., Kong, X., Sun, J., 2022. Wheat male-sterile 2 reduces ROS levels to inhibit anther development by deactivating ROS modulator 1. Mol Plant 15, 1428-1439.

Lv, M.H., Li, J., 2020. Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis. Int J Mol Sci 21, 2737.

Mhamdi, A., Van Breusegem, F., 2018. Reactive oxygen species in plant development. Development 145(15).

Nambara, E., Marion-Poll, A., 2005. Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56, 165-185.

Nolan, T.M., Chen, J.N., Yin, Y.H., 2017. Cross-talk of Brassinosteroid signaling in controlling growth and stress responses. Biochemical Journal 474, 2641-2661.

Peng, P., Yan, Z.Y., Zhu, Y.Y., Li, J.M., 2008. Regulation of the Arabidopsis GSK3-like Kinase BRASSINOSTEROID-INSENSITIVE 2 through Proteasome-Mediated Protein Degradation. Molecular Plant 1, 338-346.

Shewry, P.R., 2009. Wheat. J Exp Bot 60, 1537-1553.

Sun, F., Yu, H., Qu, J., Cao, Y., Ding, L., Feng, W., Khalid, M.H.B., Li, W., Fu, F., 2020. Maize ZmBES1/BZR1-5 Decreases ABA Sensitivity and Confers Tolerance to Osmotic Stress in Transgenic Arabidopsis. Int J Mol Sci 21, 996.

Sun, Z., Liu, X., Zhu, W., Lin, H., Chen, X., Li, Y., Ye, W., Yin, Z., 2022. Molecular Traits and Functional Exploration of BES1 Gene Family in Plants. Int J Mol Sci. 23, 4242.

Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., Wang, Z.Y., 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560.

Unterholzner, S.J., Rozhon, W., Papacek, M., Ciomas, J., Lange, T., Kugler, K.G., Mayer, K.F., Sieberer, T., Poppenberger, B., 2015. Brassinosteroids Are Master Regulators of Gibberellin Biosynthesis in Arabidopsis. Plant Cell 27, 2261-2272.

Vert, G., Chory, J., 2006. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96-100.

Wang, H., Tang, J., Liu, J., Hu, J., Liu, J., Chen, Y., Cai, Z., Wang, X., 2018. Abscisic Acid Signaling Inhibits Brassinosteroid Signaling through Dampening the Dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant 11, 315-325.

Wang, H.J., Wei, Z.Y., Li, j., Wang, X.L., 2017. Brassinosteroids: Hormone Metabolism and Signaling in Plants, The current model of BR signaling pp. 299-308.

Wang, M., Xia, G.M., 2018. The landscape of molecular mechanisms for salt tolerance in wheat. The Crop Journal 6, 42-47.

Wang, X., Chen, X., Wang, Q., Chen, M., Liu, X., Gao, D., Li, D., Li, L., 2019. MdBZR1 and MdBZR1-2like Transcription Factors Improves Salt Tolerance by Regulating Gibberellin Biosynthesis in Apple. Front Plant Sci 10, 1473.

Wang, Z.Y., Nakano, T., Gendron, J., He, J.X., Chen, M., Vafeados, D., Yang, Y.L., Fujioka, S., Yoshida, S., Asami, T., Chory, J., 2002. Nuclear-Localized BZR1 Mediates Brassinosteroid-Induced Growth and Feedback Suppression of Brassinosteroid Biosynthesis. Developmental Cell 2, 505-513.

Wang, Z.Y., Seto, H., Fujioka, S., Yoshida, S., Chory, J., 2001. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380-383.

Wang, D., Zuo, J., Liu, S., Wang, W., Lu, Q., Hao, X., Fang, Z., Liang, T., Sun, Y., Guo, C., Zhao, C., Tang, Y., 2023. BRI1 EMS SUPPRESSOR1 genes regulate abiotic stress and anther development in wheat (Triticum aestivum L.). Frontiers in Plant Science 14.

Waszczak, C., Carmody, M., Kangasjarvi, J., 2018. Reactive Oxygen Species in Plant Signaling. Annu Rev Plant Biol 69, 209-236.

Yang, C., Zhao, L., Zhang, H., Yang, Z., Wang, H., Wen, S., Zhang, C., Rustgi, S., von Wettstein, D., Liu, B., 2014. Evolution of physiological responses to salt stress in hexaploid wheat. Proc Natl Acad Sci U S A 111, 11882-11887.

Yang, Y., Guo, Y., 2018. Unraveling salt stress signaling in plants. J Integr Plant Biol 60, 796-804.

Zhang, L., He, G., Li, Y., Yang, Z., Liu, T., Xie, X., Kong, X., Sun, J., 2022. PIL transcription factors directly interact with SPLs and repress tillering/branching in plants. New Phytol 233, 1414-1425.

Zhao, J., Ju, M., Qian, J., Zhang, M., Liu, T., Zhang, K., 2021. A Tobacco Syringe Agroinfiltration-Based Method for a Phytohormone Transporter Activity Assay Using Endogenous Substrates. Front Plant Sci 12, 660966.

Zheng, M., Lin, J., Liu, X., Chu, W., Li, J., Gao, Y., An, K., Song, W., Xin, M., Yao, Y., Peng, H., Ni, Z., Sun, Q., Hu, Z., 2021. Histone acetyltransferase TaHAG1 acts as a crucial regulator to strengthen salt tolerance of hexaploid wheat. Plant Physiol. 186, 1951-1969.

Zhou, H., Shi, H., Yang, Y., Feng, X., Chen, X., Xiao, F., Lin, H., Guo, Y., 2023. Insights into plant salt stress signaling and tolerance. J Genet Genomics. S1673-8527(23)00179-0.

Zhu, J.Y., Li, Y., Cao, D.M., Yang, H., Oh, E., Bi, Y., Zhu, S., Wang, Z.Y., 2017. The F-box Protein KIB1 Mediates Brassinosteroid-Induced Inactivation and Degradation of GSK3-like Kinases in Arabidopsis. Mol Cell 66, 648-657.

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