5.9
CiteScore
5.9
Impact Factor
Turn off MathJax
Article Contents

Inhibition of the maize salt overly sensitive pathway by ZmSK3 and ZmSK4

doi: 10.1016/j.jgg.2023.04.010
Funds:  This work was supported by grants from the National Key R&D Program of China (2022YFF1001601 and 2022YFA1303400) and supported by grants from the National Natural Science Foundation of China (32100234 and 31921001).
  • Received Date: 2023-02-22
  • Revised Date: 2023-04-13
  • Accepted Date: 2023-04-21
  • Available Online: 2023-04-29
  • Soil salinity is a worldwide problem that adversely affects plant growth and crop productivity. The salt overly sensitive (SOS) pathway is evolutionarily conserved and essential for plant salt tolerance. In this study, we reveal how the maize shaggy/glycogen synthase kinase 3 (GSK3)-like kinases ZmSK3 and ZmSK4, orthologs of brassinosteroid insensitive 2 (BIN2) in Arabidopsis thaliana, regulate the maize SOS pathway. ZmSK3 and ZmSK4 interact with and phosphorylate ZmSOS2, a core member of the maize SOS pathway. The mutants defective in ZmSK3 or ZmSK4 are hyposensitive to salt stress, with higher salt-induced activity of ZmSOS2 than that in the wild type. Furthermore, the Ca2+ sensors ZmSOS3 and ZmSOS3-like calcium binding protein 8 (ZmSCaBP8) activate ZmSOS2 to maintain Na+/K+ homeostasis under salt stress, and may participate in the regulation of ZmSOS2 by ZmSK3 and ZmSK4. These findings discover the regulation of the maize SOS pathway and provide important gene targets for breeding salt-tolerant maize.
  • loading
  • [1]
    Anderson, A., St Aubin, B., Abraham-Juarez, M.J., Leiboff, S., Shen, Z., Briggs, S., Brunkard, J.O., Hake, S., 2019. The second site modifier, sympathy for the ligule, encodes a homolog of Arabidopsis ENHANCED DISEASE RESISTANCE4 and rescues the liguleless narrow maize mutant. Plant Cell 31, 1829-1844.
    [2]
    Anne, P., Azzopardi, M., Gissot, L., Beaubiat, S., Hematy, K., Palauqui, J.C., 2015. OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol. 25, 2584-2590.
    [3]
    Barajas-Lopez, J.D., Moreno, J.R., Gamez-Arjona, F.M., Pardo, J.M., Punkkinen, M., Zhu, J.K., Quintero, F.J., Fujii, H., 2018. Upstream kinases of plant SnRKs are involved in salt stress tolerance. Plant J. 93, 107-118.
    [4]
    Batistic, O., Waadt, R., Steinhorst, L., Held, K., Kudla, J., 2010. CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 61, 211-222.
    [5]
    Brindha, C., Vasantha, S., Raja, A.K., Tayade, A.S., 2021. Characterization of the Salt Overly Sensitive pathway genes in sugarcane under salinity stress. Physiol. Plant. 171, 677-687.
    [6]
    Cai, Z., Liu, J., Wang, H., Yang, C., Chen, Y., Li, Y., Pan, S., Dong, R., Tang, G., Barajas-Lopez Jde, D., et al., 2014. GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 111, 9651-9656.
    [7]
    Chaves-Sanjuan, A., Sanchez-Barrena, M.J., Gonzalez-Rubio, J.M., Moreno, M., Ragel, P., Jimenez, M., Pardo, J.M., Martinez-Ripoll, M., Quintero, F.J., Albert, A., 2014. Structural basis of the regulatory mechanism of the plant CIPK family of protein kinases controlling ion homeostasis and abiotic stress. Proc. Natl. Acad. Sci. U. S. A. 111, E4532-E4541.
    [8]
    Cho, H., Ryu, H., Rho, S., Hill, K., Smith, S., Audenaert, D., Park, J., Han, S., Beeckman, T., Bennett, M.J., et al., 2014. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat. Cell Biol. 16, 66-76.
    [9]
    Chung, Y., Kwon, S.I., Choe, S., 2014. Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol. Cells 37, 795-803.
    [10]
    Egea, I., Pineda, B., Ortiz-Atienza, A., Plasencia, F.A., Drevensek, S., Garcia-Sogo, B., Yuste-Lisbona, F.J., Barrero-Gil, J., Atares ,A., Flores, F.B., et al., 2018. The SlCBL10 calcineurin B-like protein ensures plant growth under salt stress by regulating Na+ and Ca2+ homeostasis. Plant Physiol. 176, 1676-1693.
    [11]
    Feki, K., Quintero, F.J., Pardo, J.M., Masmoudi, K., 2011. Regulation of durum wheat Na+/H+ exchanger TdSOS1 by phosphorylation. Plant Mol. Biol. 76, 545-556.
    [12]
    Gong, Z.Z., Xiong, L.M., Shi, H.Z., Yang, S.H., Herrera-Estrella, L.R., Xu, G.H., Chao, D.Y., Li, J.R., Wang, P.Y., Qin, F., et al., 2020. Plant abiotic stress response and nutrient use efficiency. Sci. China Life. Sci. 63, 635-674.
    [13]
    Guo, Y., Qiu, Q.S., Quintero, F.J., Pardo, J.M., Ohta, M., Zhang, C., Schumaker, K.S., Zhu, J.K., 2004. Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell 16, 435-449.
    [14]
    Halfter, U., Ishitani, M., Zhu, J.K., 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. U. S. A. 97, 3735-3740.
    [15]
    He, C., Gao, H., Wang, H., Guo, Y., He, M., Peng, Y., Wang, X., 2021. GSK3-mediated stress signaling inhibits legume-rhizobium symbiosis by phosphorylating GmNSP1 in soybean. Mol. Plant 14, 488-502.
    [16]
    Ismail, A.M., Horie, T., 2017. Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu. Rev. Plant Biol. 68, 405-434.
    [17]
    Jiang, H., Tang, B., Xie, Z., Nolan, T., Ye, H., Song, G.Y., Walley, J., Yin, Y., 2019a. GSK3-like kinase BIN2 phosphorylates RD26 to potentiate drought signaling in Arabidopsis. Plant J. 100, 923-937.
    [18]
    Jiang, Z., Zhou, X., Tao, M., Yuan, F., Liu, L., Wu, F., Wu, X., Xiang, Y., Niu, Y., Liu, F., et al., 2019b. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572, 341-346.
    [19]
    Kim, B.G., Waadt, R., Cheong, Y.H., Pandey, G.K., Dominguez-Solis, J.R., Schultke, S., Lee, S.C., Kudla, J., Luan, S., 2007. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52, 473-484.
    [20]
    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.
    [21]
    Kim, T.W., Michniewicz, M., Bergmann, D.C., Wang, Z.Y., 2012. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482, 419-422.
    [22]
    Koh, S., Lee, S.C., Kim, M.K., Koh, J.H., Lee, S., An, G., Choe, S., Kim, S.R., 2007. T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol. Biol. 65, 453-466.
    [23]
    Kondo, Y., Fujita, T., Sugiyama, M., Fukuda, H., 2015. A novel system for xylem cell differentiation in Arabidopsis thaliana. Mol. Plant 8, 612-621.
    [24]
    Li, B., Tester, M., Gilliham, M., 2017. Chloride on the move. Trends Plant Sci. 22, 236-248.
    [25]
    Li, J.F., Shen, L.K., Han, X.L., He, G.F., Fan, W.X., Li, Y., Yang, S.P., Zhang, Z.D., Yang, Y.Q., Jin, W.W., et al., 2023. Phosphatidic acid-regulated SOS2 controls sodium and potassium homeostasis in Arabidopsis under salt stress. EMBO J. e112401. Online ahead of print.
    [26]
    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.
    [27]
    Liang, Y., Liu, H.J., Yan, J., Tian, F., 2021. Natural variation in crops: realized understanding, continuing promise. Annu. Rev. Plant Biol. 72, 357-385.
    [28]
    Lin, H., Yang, Y., Quan, R., Mendoza, I., Wu, Y., Du, W., Zhao, S., Schumaker, K.S., Pardo, J.M., Guo, Y., 2009. Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. Plant Cell 21, 1607-1619.
    [29]
    Ma, L., Ye, J., Yang, Y., Lin, H., Yue, L., Luo, L., Long, Y., Fu, H., Liu, X., Zhang. Y., et al., 2019. The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev. Cell 48, 697-709.
    [30]
    Martinez-Atienza, J., Jiang, X., Garciadeblas, B., Mendoza, I., Zhu, J.K., Pardo, J.M., Quintero, F.J., 2007. Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 143, 1001-1012.
    [31]
    Monihan, S.M., Magness, C.A., Ryu, C.H., McMahon, M.M., Beilstein, M.A, Schumaker, K.S., 2020. Duplication and functional divergence of a calcium sensor in the Brassicaceae. J. Exp. Bot. 71, 2782-2795.
    [32]
    Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M., Guo, Y., 2007. SCABP8/CBL10 a putative calcium sensor interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19, 1415-1431.
    [33]
    Quintero, F.J., Martinez-Atienza, J., Villalta, I., Jiang, X., Kim, W.Y., Ali, Z., Fujii ,H., Mendoza, I., Yun, D.J., Zhu, J.K., et al., 2011. Activation of the plasma membrane Na+/H+ antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc. Natl. Acad. Sci. U. S. A. 108, 2611-2616.
    [34]
    Ren, X.L., Qi, G.N., Feng, H.Q., Zhao, S., Zhao, S.S., Wang, Y., Wu, W.H., 2013. Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J. 74, 258-266.
    [35]
    Tang, R.J., Yang, Y., Yang, L., Liu, H., Wang, C.T., Yu, M.M., Gao, X.S., Zhang, H.X., 2014. Poplar calcineurin B-like proteins PtCBL10A and PtCBL10B regulate shoot salt tolerance through interaction with PtSOS2 in the vacuolar membrane. Plant Cell Environ. 37, 573-588.
    [36]
    Vert, G., Walcher, C.L., Chory, J., Nemhauser, J.L., 2008. Integration of auxin and brassinosteroid pathways by auxin response factor 2. Proc. Natl. Acad. Sci. U. S. A. 105, 9829-9834.
    [37]
    Wang, Y., Xu, J., Yu, J., Zhu, D., Zhao, Q., 2022. Maize GSK3-like kinase ZmSK2 is involved in embryonic development. Plant Sci. 318, 111221.
    [38]
    Wang, Z., Hong, Y., Zhu, G., Li, Y., Niu, Q., Yao, J., Hua, K., Bai, J., Zhu, Y., Shi, H., Huang, S., Zhu, J.K., 2020. Loss of salt tolerance during tomato domestication conferred by variation in a Na+/K+ transporter. EMBO J. 39, e103256.
    [39]
    Xiao, Y., Zhang, G., Liu, D., Niu, M., Tong, H., Chu, C., 2020. GSK2 stabilizes OFP3 to suppress brassinosteroid responses in rice. Plant J. 102, 1187-1201.
    [40]
    Xie, Z., Nolan, T., Jiang, H., Tang, B., Zhang, M., Li, Z., Yin, Y., 2019. The AP2/ERF transcription factor TINY modulates brassinosteroid-regulated plant growth and drought responses in Arabidopsis. Plant Cell 31, 1788-1806.
    [41]
    Xing, H.L., Dong, L., Wang, Z.P., Zhang, H.Y., Han, C.Y., Liu, B., Wang, X.C., Chen, Q.J., 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.
    [42]
    Yan, Z., Zhao, J., Peng, P., Chihara, R.K, Li, J., 2009. BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol. 150, 710-721.
    [43]
    Yang, Y., Zhang, C, Tang, R.J., Xu, H.X., Lan, W.Z., Zhao, F., Luan, S., 2019a. Calcineurin B-like proteins CBL4 and CBL10 mediate two independent salt tolerance pathways in Arabidopsis. Int. J. Mol. Sci. 20, 2421.
    [44]
    Yang, Y.Q., Guo, Y., 2018. Unraveling salt stress signaling in plants. J. Integr. Plant. Biol. 60, 796-804.
    [45]
    Yang, Z.J., Wang, C.W., Xue, Y., Liu, X., Chen, S., Song, C.P., Yang, Y.Q., Guo, Y., 2019b. Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat. Commun. 10, 1199.
    [46]
    Ye, K., Li, H., Ding, Y., Shi, Y., Song, C., Gong, Z., Yang, S., 2019. BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 31, 2682-2696.
    [47]
    Yin, X., Xia, Y., Xi, Q., Cao, Y., Wang, Z., Hao, G., Song, .J, Zhou, Y., Jiang, X., 2020. The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance. J. Exp. Bot. 71, 1801-1814.
    [48]
    Yoo, S.D., Cho, Y.H., Sheen, J., 2017. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565−1572.
    [49]
    Youn, J.H., Kim, T.W., 2015. Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways. Mol. Plant 8, 552-565.
    [50]
    Zhang, F., Li, L., Jiao, Z., Chen, Y., Liu, H., Chen, X., Fu, J., Wang, G., Zheng, J., 2016. Characterization of the calcineurin B-Like (CBL) gene family in maize and functional analysis of ZmCBL9 under abscisic acid and abiotic stress treatments. Plant Sci. 253, 118-129.
    [51]
    Zhang, M., Cao, Y., Wang, Z., Wang, Z.Q., Shi, J., Liang, X., Song, W., Chen, Q., Lai, J., Jiang, C., 2018. A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. New Phytol. 217, 1161-1176.
    [52]
    Zhang, M., Liang, X., Wang, L., Cao, Y., Song, W., Shi, J., Lai, J., Jiang, C., 2019. A HAK family Na+ transporter confers natural variation of salt tolerance in maize. Nat. Plants 5, 1297-1308.
    [53]
    Zhao, C., William, D., Sandhu, D., 2021. Isolation and characterization of Salt Overly Sensitive family genes in spinach. Physiol Plant. 171, 520-532.
    [54]
    Zhou, X., Li, J., Wang, Y., Liang, X., Zhang, M., Lu, M., Guo, Y., Qin, F., Jiang, C., 2022. The classical SOS pathway confers natural variation of salt tolerance in maize. New Phytol. 236, 479-494.
    [55]
    Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (177) PDF downloads (52) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return