OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice

Meiru Jia; Nan Luo; Xiangbing Meng; Xiaoguang Song; Yanhui Jing; Liquan Kou; Guifu Liu; Xiahe Huang; Yingchun Wang; Jiayang Li; Bing Wang; Hong Yu

doi:10.1016/j.jgg.2022.06.009

Volume 49 Issue 8

Aug. 2022

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2022 > 49(8): 766-775

PDF( 2436 KB)

OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice

doi: 10.1016/j.jgg.2022.06.009

a. State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China;
c. State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China

Funds:

This work was supported by the National Natural Science Foundation of China (31788103, 32122064, 32122012), the Chinese Academy of Sciences (XDA24030504, 2019099), China Agricultural Research System (CARS-01-4), and the China Postdoctoral Science Foundation (2019M650885).

Received Date: 2022-04-14
Accepted Date: 2022-06-30
Rev Recd Date: 2022-06-20
Publish Date: 2022-07-05

Abstract

Abstract

Salt stress adversely affects plant growth, development, and crop yield. Rice (Oryza sativa L.) is one of the most salt-sensitive cereal crops, especially at the early seedling stage. Mitogen-activated protein kinase (MAPK/MPK) cascades have been shown to play critical roles in salt response in Arabidopsis. However, the roles of the MPK cascade signaling in rice salt response and substrates of OsMPK remain largely unknown. Here, we report that the salt-induced OsMPK4-Ideal Plant Architecture 1 (IPA1) signaling pathway regulates the salt tolerance in rice. Under salt stress, OsMPK4 could interact with IPA1 and phosphorylate IPA1 at Thr180, leading to degradation of IPA1. Genetic evidence shows that IPA1 is a negative regulator of salt tolerance in rice, whereas OsMPK4 promotes salt response in an IPA1-dependent manner. Taken together, our results uncover an OsMPK4-IPA1 signal cascade that modulates the salt stress response in rice and sheds new light on the breeding of salt-tolerant rice varieties.
- Oryza sativa,
- MPK,
- OsMPK4,
- IPA1,
- Salt tolerance

FullText(HTML)

References(50)

References

Bart, R., Chern, M., Park, C. J., Bartley, L. Ronald, P.C., 2006. A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2, 13

Chen, R., Deng, Y., Ding, Y., Guo, J., Qiu, J., Wang, B., Wang, C., Xie, Y., Zhang, Z., Chen, J., et al., 2022. Rice functional genomics:decades' efforts and roads ahead. Sci. China Life Sci. 65, 33-92

Chen, X., Ding, Y., Yang, Y., Song, C., Wang, B., Yang, S., Guo, Y., Gong, Z., 2021. Protein kinases in plant responses to drought, salt, and cold stress. J. Integr. Plant Biol. 63, 53-78

Ding, Y., Li, H., Zhang, X., Qi, X., Gong, Z., Yang, S., 2015. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev. Cell 32, 278-289

Evrard, A., Kumar, M., Lecourieux, D., Lucks, J., von Koskull-Doring, P., Hirt, H., 2013. Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. Peer J. 1, e59

Gao, F., Su, Q., Fan, Y., Wang, L., 2010. Expression pattern and core region analysis of AtMPK3 promoter in response to environmental stresses. Sci. China. Life Sci. 53, 1315-1321

Gong, Z., Xiong, L., Shi, H., Yang, S., Herrera-Estrella, L.R., Xu, G., Chao, D.Y., Li, J., Wang, P.Y., Qin, F., et al., 2020. Plant abiotic stress response and nutrient use efficiency. Sci. China. Life Sci. 63, 635-674

Hamel, L.P., Nicole, M.C., Sritubtim, S., Morency, M.J., Ellis, M., Ehlting, J., Beaudoin, N., Barbazuk, B., Klessig, D., Lee, J., et al., 2006. Ancient signals:comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 11, 192-198

Hazell, P., Wood, S., 2008. Drivers of change in global agriculture. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363, 495-515

Jagodzik, P., Tajdel-Zielinska, M., Ciesla, A., Marczak, M., Ludwikow, A., 2018. Mitogen-activated protein kinase cascades in plant hormone signaling. Front. Plant Sci. 9, 1387

Jalmi, S.K., Sinha, A.K., 2016. Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice. Sci. Rep. 6, 37974

Jerome Jeyakumar, J. M., Ali, A., Wang, W. M., Thiruvengadam, M., 2020. Characterizing the role of the miR156-SPL network in plant development and stress response. Plants 9, 1206

Jia, W., Li, B., Li, S., Liang, Y., Wu, X., Ma, M., Wang, J., Gao, J., Cai, Y., Zhang, Y., et al., 2016. Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis. PLoS Biol. 1, e1002550

Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544

Kumar, K., Sinha, A.K., 2013. Overexpression of constitutively active mitogen activated protein kinase kinase 6 enhances tolerance to salt stress in rice. Rice (N Y), 6, 25

Lan, T., Zheng, Y., Su, Z., Yu, S., Song, H., Zheng, X., Lin, G., Wu, W., 2019. OsSPL10, a SBP-Box Gene, plays a dual role in salt tolerance and trichome formation in rice (Oryza sativa L.). G3 (Bethesda). 9, 4107-4114

Li, X., Yu, B., Wu, Q., Min, Q., Zeng, R., Xie, Z., Huang, J., 2021. OsMADS23 phosphorylated by SAPK9 confers drought and salt tolerance by regulating ABA biosynthesis in rice. PLoS Genet. 17, e1009699

Liao, Z., Yu, H., Duan, J., Yuan, K., Yu, C., Meng, X., Kou, L., Chen, M., Jing, Y., Liu, G., et al., 2019. SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nat. Commun. 10, 2738

Liu, M., Shi, Z., Zhang, X., Wang, M., Zhang, K., Liu, J., Hu, X., Di, C., Qian, Q., He, Z., Yang, D., 2019. Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat. Plants 5, 389-400

Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., Zhang, S., 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639-1653

Meng, X., Xu, J., He, Y., Yang, K.Y., Mordorski, B., Liu, Y., Zhang, S., 2013. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25, 1126-1142

Meng, X., Yu, H., Zhang, Y., Zhuang, F., Song, X., Gao, S., Gao, C., Li, J., 2017. Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Mol. Plant, 10, 1238-1241

Miura, K., Ikeda, M., Matsubara, A., Song, X. J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., Ashikari, M., 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549

Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681

Na Y.J., Choi H.K., Park M.Y., Choi S.W., Xuan Vo K.T., Jeon J.S., Kim S.Y., 2019. OsMAPKKK63 is involved in salt stress response and seed dormancy control. Plant Signal. Behav. 14, e1578633

Perez-Salamo, I., Papdi, C., Rigo, G., Zsigmond, L., Vilela, B., Lumbreras, V., Nagy, I., Horvath, B., Domoki, M., Darula, Z., et al., 2014. The Heat Shock Factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol. 165, 319-334

Qadir, M., Quillerou, E., Nangia, V., Murtaza, G., Singh, M., Thomas, R.J., Drechsel, P., Noble, A.D., 2014. Economics of salt-induced land degradation and restoration. Nat. Resour. Forum. 38, 282-295

Rodriguez, M.C., Petersen, M., Mundy, J., 2010. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649

Shao, G., Lu, Z., Xiong, J., Wang, B., Jing, Y., Meng, X., Liu, G., Ma, H., Liang, Y., Chen, F., et al., 2019. Tiller bud formation regulators MOC1 and MOC3 cooperatively promote tiller bud outgrowth by activating FON1 expression in rice. Mol. Plant 12, 1090-1102

Shen, H., Liu, C., Zhang, Y., Meng, X., Zhou, X., Chu, C., Wang, X., 2012. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol. Biol. 80, 241-253

Shen, X.L., Bin, Y., Liu, H.B., Li, X.H., Xu, C.G., Wang S.P., 2010. Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J. 64, 86-99

Song, X., Lu, Z., Yu, H., Shao G., Xiong J., Meng, X., Jing, Y., Liu, G., Xiong, G., Duan, J., et al., 2017. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res. 27, 1128-1141

Unte, U. S., Sorensen A. M., Pesaresi, P., Gandikota, M., Leister, D., Saedler, H., Huijser, P., 2003. SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15, 1009-1019

Wang, B., Smith, S.M., Li, J., 2018a. Genetic regulation of shoot architecture. Annu. Rev. Plant Biol. 69, 437-468

Wang, B., Wang, H., 2017. IPA1:A New "Green Revolution" Gene? Mol. Plant. 10, 779-781

Wang, F., Jing, W., Zhang, W., 2014. The mitogen-activated protein kinase cascade MKK1-MPK4 mediates salt signaling in rice. Plant Sci. 227, 181-189

Wang, J., Long, X., Chern, M., Chen, X., 2021. Understanding the molecular mechanisms of trade-offs between plant growth and immunity. Sci. China. Life Sci. 64, 234-241

Wang, J., Yu, H., Xiong, G., Lu, Z., Jiao, Y., Meng, X., Liu, G., Chen, X., Wang, Y., Li, J., et al., 2017. Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN1 modulates IPA1 protein levels to regulate plant architecture in rice. Plant Cell 29, 697-707

Wang, J., Zhou, L., Shi, H., Chern, M., Yu H., Yi, H., He, M., Yin, J., Zhu, X., Li, Y., 2018b. A single transcription factor promotes both yield and immunity in rice. Science 361, 1026-1028

Xie, G., Kato, H., Imai, R., 2012. Biochemical identification of the OsMKK6-OsMPK3 signalling pathway for chilling stress tolerance in rice. Biochem. J. 443, 95-102

Xie, K.B., Wu C.Q., Xiong, L.Z., 2006. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol. 142, 280-293

Xiong L.Z., Yang Y.N., 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15, 745-759

Yang, C., Ma, B., He, S., Xiong, Q., Duan, K., Yin, C., Chen, H., Lu, X., Chen, S., Zhang, J., 2015. MAOHUZI6/ETHYLENE INSENSITIVE3-LIKE1 and ETHYLENE INSENSITIVE3-LIKE2 regulate ethylene response of roots and coleoptiles and negatively affect salt tolerance in rice. Plant Physiol. 169, 148-165

Yu, L.J., Nie, J.N., Cao, C.Y., Jin, Y.K., Yan, M., Wang, F.Z., Liu, J., Xiao, Y., Liang, Y.H., Zhang, W.H., 2010. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188, 762-773

Zelm, E., Zhang, Y.X., Testerink, C., 2020. Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71, 403-433

Zhang, L., Yu, H., M, B., Liu, G., Wang, J., Wang J., Gao, R., Li, J., Liu, J., Xu, J., et al., 2017. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat. Commun. 8, 14789

Zhang, Y., Wang, P., Shao, W., Zhu, J.K., Dong, J., 2015. The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev. Cell 33, 136-149

Zhang, Z., Liu, H., Sun, C., Ma, Q., Bu, H., Chong, K., Xu, Y., 2018. A C2H2 zinc-finger protein OsZFP213 interacts with OsMAPK3 to enhance salt tolerance in rice. J. Plant Physiol. 229, 100-110

Zhao, S., Zhang, Q., Liu, M., Zhou, H., Ma, C., Wang, P., 2021. Regulation of plant responses to salt stress. Int. J. Mol. Sci. 22, 4609

Zhu, M., He, Y., Zhu, M., Ahmad, A., Xu, S., He, Z., Jiang, S., Huang, J., Li, Z., Liu, S., et al., 2022. ipa1 improves rice drought tolerance at seedling stage mainly through activating abscisic acid pathway. Plant Cell Rep. 41, 221-232

Relative Articles

Supplements(0)

Cited By

Proportional views