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Volume 52 Issue 3
Mar.  2025
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Article Navigation >  Journal of Genetics and Genomics  > 2025  >  52(3): 388-399

An LRR-RLK protein modulates drought- and salt-stress responses in maize

doi: 10.1016/j.jgg.2024.10.016
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    Frontiers Science Center for Molecular Design Breeding (MOE), State Key Laboratory of Plant Environmental Resilience, Center for Crop Functional Genomics and Molecular Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China

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We appreciate the great technical support provided by the staff at the Center of Crop Functional Genomics and Molecular Breeding at China Agricultural University for the generation and propagation of the transgenic maize lines. This work was supported by the National Key Research and Development Program of China (2021YFD1200703 and 2022YFF1001602), the National Science Foundation of China (32272024 and 32171940), the Pinduoduo- China Agricultural University Research Fund (PC2023B01001), the Chinese Universities Scientific Fund (2022TC142), and the 2115 Talent Development Program of China Agricultural University.

  • Received Date: 2024-07-26
  • Accepted Date: 2024-10-28
  • Rev Recd Date: 2024-10-28
    • Available Online: 2025-07-11
  • Publish Date: 2024-11-13
    Abstract
  • Maize (Zea mays), which is a vital source of food, feed, and energy feedstock globally, has significant potential for higher yields. However, environmental stress conditions, including drought and salt stress, severely restrict maize plant growth and development, leading to great yield losses. Leucine-rich repeat receptor-like kinases (LRR-RLKs) function in biotic and abiotic stress responses in the model plant Arabidopsis (Arabidopsis thaliana), but their roles in abiotic stress responses in maize are not entirely understood. In this study, we determine that the LRR-RLK ZmMIK2, a homolog of the Arabidopsis LRR-RK MALE DISCOVERER 1 (MDIS1)-INTERACTING RECEPTOR LIKE KINASE 2 (MIK2), functions in resistance to both drought and salt stress in maize. Zmmik2 plants exhibit enhanced resistance to both stresses, whereas overexpressing ZmMIK2 confers the opposite phenotypes. Furthermore, we identify C2-DOMAIN-CONTAINING PROTEIN 1 (ZmC2DP1), which interacts with the intracellular region of ZmMIK2. Notably, that region of ZmMIK2 mediates the phosphorylation of ZmC2DP1, likely by increasing its stability. Both ZmMIK2 and ZmC2DP1 are mainly expressed in roots. As with ZmMIK2, knockout of ZmC2DP1 enhances resistance to both drought and salt stress. We conclude that ZmMIK2–ZmC2DP1 acts as a negative regulatory module in maize drought- and salt-stress responses.
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  • Campos, H., Cooper, M., Habben, J.E., Edmeades, G.O., Schussler, J.R., 2004. Improving drought tolerance in maize: A view from industry. F. Crop. Res. 90, 19-34.
    Cartwright, H.N., Humphries, J.A., Smith, L.G., 2009. PAN1 : a receptor-like protein asymmetric cell division in maize 323, 649-651.
    Chen, K., Gao, J., Sun, S., Zhang, Z., Yu, B., Li, J., Xie, C., Li, G., Wang, P., Song, C.P., et al., 2020. BONZAI proteins control global osmotic stress responses in plants. Curr. Biol. 30, 4815-4825.e4.
    Cho, W., Stahelin, R. V., 2006. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta - Mol. Cell Biol. Lipids 1761, 838-849.
    Connor, K.M., Davidson, J.R.T., 2024. Differential phosphorylation of Ca2+-permeable channel CNGC20 modulates calcium-mediated freezing tolerance in Arabidopsis. Plant Cell 1-27.
    Diaz, M., Sanchez-Barrena, M.J., Gonzalez-Rubio, J.M., Rodriguez, L., Fernandez, D., Antoni, R., Yunta, C., Belda-Palazon, B., Gonzalez-Guzman, M., Peirats-Llobet, M., et al., 2016. Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proc. Natl. Acad. Sci. U. S. A. 113, E396-E405.
    Dievart, A., Gottin, C., Peacuterin, C., Ranwez, V., Chantret, N., 2020. Origin and Diversity of Plant Receptor-Like Kinases. Annu. Rev. Plant Biol. 71, 131-156.
    Ding, S., Zhang, B., Qin, F., 2015. Arabidopsis rzfp34/chyr1, a ubiquitin e3 ligase, regulates stomatal movement and drought tolerance viasnrk2.6-mediated phosphorylation. Plant Cell 27, 3228-3244.
    Dong, Q., Wallrad, L., Almutairi, B.O., Kudla, J., 2022. Ca2+ signaling in plant responses to abiotic stresses. J. Integr. Plant Biol. 64, 287-300.
    Eckhoff, S.R., Paulsen, M.R., 1996. Maize, in: Henry, R.J., Kettlewell, P.S. (Eds.), Cereal grain quality. Springer Netherlands, Dordrecht, pp. 77-112.
    Feng, L., Gao, Z., Xiao, G., Huang, R., Zhang, H., 2014. Leucine-rich repeat receptor-like kinase FON1 regulates drought stress and seed germination by activating the expression of ABA-responsive genes in rice. Plant Mol. Biol. Report. 32, 1158-1168.
    Fu, S., Fu, L., Zhang, X., Huang, J., Yang, G., Wang, Z., Liu, Y.-G., Zhang, G., Wu, D., Xia, J., 2019a. OsC2DP, a novel C2 domain-containing protein is required for salt tolerance in rice. Plant Cell Physiol. 60, 2220-2230.
    Fu, S., Huang, J., Chen, Z., Xia, J., 2019b. C2 domain plays critical roles in localization of novel C2 domain-containing protein OsC2DP. Plant Signal. Behav. 14, 3-5.
    Gao, H., Cui, J., Liu, S., Wang, S., Lian, Y., Bai, Y., Zhu, T., Wu, H., Wang, Y., Yang, S., et al., 2022. Natural variations of ZmSRO1d modulate the trade-off between drought resistance and yield by affecting ZmRBOHC-mediated stomatal ROS production in maize. Mol. Plant 15, 1558-1574.
    Gupta, A., Rico-Medina, A., Cano-Delgado, A.I., 2020. The physiology of plant responses to drought. Science 368, 266-269.
    Hou, S., Liu, D., Huang, S., Luo, D., Liu, Z., Xiang, Q., Wang, P., Mu, R., Han, Z., Chen, S., et al., 2021. The Arabidopsis MIK2 receptor elicits immunity by sensing a conserved signature from phytocytokines and microbes. Nat. Commun. 12, 1-15.
    Hsu, P.K., Takahashi, Y., Merilo, E., Costa, A., Zhang, L., Kernig, K., Lee, K.H., Schroeder, J.I., 2021. Raf-like kinases and receptor-like (pseudo)kinase GHR1 are required for stomatal vapor pressure difference response. Proc. Natl. Acad. Sci. U. S. A. 118, 1-12.
    Hua, D., Wang, C., He, J., Liao, H., Duan, Y., Zhu, Z., Guo, Y., Chen, Z., Gong, Z., 2012. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546-2561.
    Jiang, Z., Zhou, X., Tao, M., Yuan, F., Liu, L., Wu, F., Wu, X., Xiang, Y., Niu, Y., Liu, F., et al., 2019. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca(2+) influx. Nature 572, 341-346.
    Jing, T., Wu, Y., Yu, Y., Li, J., Mu, X., Xu, L., Wang, X., Qi, G., Tang, J., Wang, D., et al., 2024. Copine proteins are required for brassinosteroid signaling in maize and Arabidopsis. Nat. Commun. 15.
    Julkowska, M.M., Klei, K., Fokkens, L., Haring, M.A., Schranz, M.E., Testerink, C., 2016. Natural variation in rosette size under salt stress conditions corresponds to developmental differences between Arabidopsis accessions and allelic variation in the LRR-KISS gene. J. Exp. Bot. 67, 27-38.
    Khan, I., Gratz, R., Denezhkin, P., Schott-Verdugo, S.N., Angrand, K., Genders, L., Basgaran, R.M., Fink-Straube, C., Brumbarova, T., Gohlke, H., Bauer, P., et al., 2019. Calcium-promoted interaction between the C2-domain protein EHB1 and metal transporter IRT1 inhibits arabidopsis iron acquisition. Plant Physiol. 180, 1564-1581.
    Li, J., Zhou, X., Wang, Y., Song, S., Ma, L., He, Q., Lu, M., Zhang, K., Yang, Y., Zhao, Q., et al., 2023. Inhibition of the maize salt overly sensitive pathway by ZmSK3 and ZmSK4. J. Genet. Genomics 50, 960-970.
    Liu, L., Ashraf, M.A., Morrow, T., Facette, M., 2024. Stomatal closure in maize is mediated by subsidiary cells and the PAN2 receptor. New Phytol. 241, 1130-1143.
    Liu, S., Liu, X., Zhang, X., Chang, S., Ma, C., Qin, F., 2023. Co-expression of ZmVPP1 with ZmNAC111 confers robust drought resistance in maize. Genes (Basel). 14.
    Ma, L., Ye, J., Yang, Y., Lin, H., Yue, L., Luo, J., 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.e5.
    Masle, J., Gilmore, S.R., Farquhar, G.D., 2005. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866-870.
    Meijer, H.J.G., Munnik, T., 2003. Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54, 265-306.
    Montanarella Luca, Badraoui, M., Chude, Vi., Costa, I., Baptista, saurinda D.S., Mamo, T., Yemefack, M., Aulang, M.S., Yagi, K., Hong, S.Y., Vijarnsorn, P., Zhang, G.L., Arrouays, D., Black, H., Krasilnikov, P., et al., 2015. Status of the world’s soil resources, intergovernmental technical panel on soils.
    Moon, S., Jung, K.H., Lee, D.E., Lee, D.Y., Lee, J., An, K., Kang, H.G., An, G., 2006. The rice FON1 gene controls vegetative and reproductive development by regulating shoot apical meristem size. Mol. Cells 21, 147-152.
    Munns, R., Gilliham, M., 2015. Salinity tolerance of crops - what is the cost? New Phytol 208, 668-673.
    Nalefski, E.A., Falke, J.J., 1996. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5, 2375-2390.
    Poretsky, E., Dressano, K., Weckwerth, P., Ruiz, M., Char, S.N., Shi, D., Abagyan, R., Yang, B., Huffaker, A., 2020. Differential activities of maize plant elicitor peptides as mediators of immune signaling and herbivore resistance. Plant J. 104, 1582-1602.
    Qin, T., Tian, Q., Wang, G., Xiong, L., 2019. LOWER TEMPERATURE 1 enhances ABA responses and plant drought tolerance by modulating the stability and localization of C2-domain ABA-related proteins in Arabidopsis. Mol. Plant 12, 1243-1258.
    Rhodes, J., Yang, H., Moussu, S., Boutrot, F., Santiago, J., Zipfel, C., 2021. Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2. Nat. Commun. 12.
    Sierla, M., Horak, H., Overmyer, K., Waszczak, C., Yarmolinsky, D., Maierhofer, T., Vainonen, J.P., Salojarvi, J., Denessiouk, K., Laanemets, K., Toldsepp, K., et al., 2018. The receptor-like pseudokinase GHR1 is required for stomatal closure. Plant Cell 30, 2813-2837.
    Soltabayeva, A., Dauletova, N., Serik, S., Sandybek, M., Omondi, J.O., Kurmanbayeva, A., Srivastava, S., 2022. Receptor-like Kinases (LRR-RLKs) in response of plants to biotic and abiotic stresses. Plants 11, 1-20.
    Song, W., Liu, L., Wang, J., Wu, Z., Zhang, H., Tang, J., Lin, G., Wang, Y., Wen, X., Li, W., et al., 2016. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res. 26, 674-685.
    Suzaki, T., Sato, M., Ashikari, M., Miyoshi, M., Nagato, Y., Hirano, H.Y., 2004. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131, 5649-5657.
    Tang, J., Han, Z., Sun, Y., Zhang, H., Gong, X., Chai, J., 2015. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res. 25, 110-120.
    Tian, J., Wang, C., Xia, J., Wu, L., Xu, G., Wu, W., Li, D., Qin, W., Han, X., Chen, Q., et al., 2019. Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science 365, 658-664.
    Van der Does, D., Boutrot, F., Engelsdorf, T., Rhodes, J., McKenna, J.F., Vernhettes, S., Koevoets, I., Tintor, N., Veerabagu, M., Miedes, E., Segonzac, C., Roux, M., et al., 2017. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet. 13, 1-27.
    van Zelm, E., Zhang, Y., Testerink, C., 2020. Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71, 403-433.
    Verslues, P.E., Bailey-Serres, J., Brodersen, C., Buckley, T.N., Conti, L., Christmann, A., Dinneny, J.R., Grill, E., Hayes, S., Heckman, R.W., Hsu, P.-K., Juenger, T.E., Mas, P., Munnik, T., et al., 2022. Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 1-42.
    Wang, T., Liang, L., Xue, Y., Jia, P.F., Chen, W., Zhang, M.X., Wang, Y.C., Li, H.J., Yang, W.C., 2016. A receptor heteromer mediates the male perception of female attractants in plants. Nature 531, 241-244.
    Xu, T., Niu, J., Jiang, Z., 2022. Sensing mechanisms: calcium signaling mediated abiotic stress in plants. Front. Plant Sci. 13.
    Yang, D.L., Shi, Z., Bao, Y., Yan, J., Yang, Z., Yu, H., Li, Y., Gou, M., Wang, S., Zou, B., et al., 2017. Calcium pumps and interacting BON1 protein modulate calcium signature, stomatal closure, and plant immunity. Plant Physiol. 175, 424-437.
    Yang, H., Kim, X., Sklenar, J., Aubourg, S., Sancho-Andres, G., Stahl, E., Guillou, M.C., Gigli-Bisceglia, N., Tran Van Canh, L., Bender, K.W., et al., 2023a. Subtilase-mediated biogenesis of the expanded family of SERINE RICH ENDOGENOUS PEPTIDES. Nat. Plants 9, 2085-2094.
    Yang, W.Q., Lai, Y., Li, M.N., Xu, W.Y., Xue, Y.B., 2008. A novel C2-domain phospholipid-binding protein, OsPBP1, is required for pollen fertility in rice. Mol. Plant 1, 770-785.
    Yang, Y., Guo, Y., 2018. Unraveling salt stress signaling in plants. J Integr Plant Biol 60, 796-804.
    Yang, Z., Cao, Y., Shi, Y., Qin, F., Jiang, C., Yang, S., 2023b. Genetic and molecular exploration of maize environmental stress resilience: Toward sustainable agriculture. Mol. Plant 16, 1496-1517.
    Yang, Z., Huang, Y., Yang, J., Yao, S., Zhao, K., Wang, D., Qin, Q., Bian, Z., Li, Yan, Lan, Y., et al., 2020. Jasmonate signaling enhances RNA silencing and antiviral defense in rice. Cell Host Microbe 28, 89-103.
    Ye, Y., Ding, Y., Jiang, Q., Wang, F., Sun, J., Zhu, C., 2017. The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants. Plant Cell Rep. 36, 235-242.
    Yoo, S.-D., Cho, Y.-H., Sheen, J., 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
    Yuan, F., Yang, H., Xue, Y., Kong, D., Ye, R., Li, C., Zhang, J., Theprungsirikul, L., Shrift, T., Krichilsky, B., et al., 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367-371.
    Zhang, H., Sun, X., Dai, M., 2022. Improving crop drought resistance with plant growth regulators and rhizobacteria : Mechanisms, applications, and perspectives. Plant Commun. 3, 100228.
    Zhao, C., Zhang, H., Song, C., Zhu, J.K., Shabala, S., 2020. Mechanisms of plant responses and adaptation to soil salinity. Innov. 1, 100017.
    Zhou, H., Shi, H., Yang, Y., Feng, X., Chen, X., Xiao, F., Lin, H., Guo, Y., 2024. Insights into plant salt stress signaling and tolerance. J. Genet. Genomics 51, 16-34.
    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.
    Zhou, Z., Bi, G., Zhou, J.M., 2018. Luciferase complementation assay for protein-protein interactions in plants. Curr. Protoc. Plant Biol. 3, 42-50.
    Zhu, J.-K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.
    Zhu, J.-K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324.
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