Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

Lichao Chen; Shuhao Sun; Chun-Peng Song; Jian-Min Zhou; Jiayang Li; Jianru Zuo

doi:10.1016/j.jgg.2022.02.023

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

doi: 10.1016/j.jgg.2022.02.023

Lichao Chen^a,b,c, ,,
Shuhao Sun^a,b,c,
Chun-Peng Song^d,
Jian-Min Zhou^a,b,e,
Jiayang Li^a,b,e,
Jianru Zuo^a,b,c,e, ,

a. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
b. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
c. CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing 100101, China;
d. State Key Laboratory of Crop Stress Adaptation and Improvement, Collaborative Innovation Center of Crop Stress Biology, Henan University, Kaifeng, Henan 475001, China;
e. Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China

基金项目:

We thank the Arabidopsis Biological Resource Center (ABRC) and Xiangdong Fu for seeds. This work was supported by grants from the National Natural Science Foundation of China (31830017 and 31521001), Chinese Academy of Sciences (XDB27030207), and State Key Laboratory of Plant Genomics (SKLPG2020-22).

详细信息

通讯作者:
Lichao Chen,E-mail:lcchen@genetics.ac.cn

Jianru Zuo,E-mail:jrzuo@genetics.ac.cn

计量
- 文章访问数: 43
- HTML全文浏览量: 28
- PDF下载量: 0
- 被引次数: 0
出版历程
- 收稿日期: 2022-02-23
- 修回日期: 2022-02-27
- 录用日期: 2022-02-28
- 网络出版日期: 2023-03-17

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

Lichao Chen^{a,b,c
, ,},
Shuhao Sun^a,b,c,
Chun-Peng Song^d,
Jian-Min Zhou^a,b,e,
Jiayang Li^a,b,e,
Jianru Zuo^{a,b,c,e
, ,}

a. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
b. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
c. CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Beijing 100101, China;
d. State Key Laboratory of Crop Stress Adaptation and Improvement, Collaborative Innovation Center of Crop Stress Biology, Henan University, Kaifeng, Henan 475001, China;
e. Hainan Yazhou Bay Seed Laboratory, Sanya, Hainan 572025, China

Funds:

摘要

摘要: In response to dynamically altered environments, plants must finely coordinate the balance between growth and stress responses for their survival. However, the underpinning regulatory mechanisms remain largely elusive. The phytohormone gibberellin promotes growth via a derepression mechanism by proteasomal degradation of the DELLA transcription repressors. Conversely, the stress-induced burst of nitric oxide (NO) enhances stress tolerance, largely relying on NO-mediated S-nitrosylation, a redox-based posttranslational modification. Here, we show that S-nitrosylation of Cys-374 in the Arabidopsis RGA protein, a key member of DELLAs, inhibits its interaction with the F-box protein SLY1, thereby preventing its proteasomal degradation under salinity condition. The accumulation of RGA consequently retards growth but enhances salt tolerance. We propose that NO negatively regulates gibberellin signaling via S-nitrosylation of RGA to coordinate the balance of growth and stress responses when challenged by adverse environments.
- Gibberellin /
- Nitric oxide /
- S-nitrosylation /
- DELLA repressors /
- Stress responses
Abstract: In response to dynamically altered environments, plants must finely coordinate the balance between growth and stress responses for their survival. However, the underpinning regulatory mechanisms remain largely elusive. The phytohormone gibberellin promotes growth via a derepression mechanism by proteasomal degradation of the DELLA transcription repressors. Conversely, the stress-induced burst of nitric oxide (NO) enhances stress tolerance, largely relying on NO-mediated S-nitrosylation, a redox-based posttranslational modification. Here, we show that S-nitrosylation of Cys-374 in the Arabidopsis RGA protein, a key member of DELLAs, inhibits its interaction with the F-box protein SLY1, thereby preventing its proteasomal degradation under salinity condition. The accumulation of RGA consequently retards growth but enhances salt tolerance. We propose that NO negatively regulates gibberellin signaling via S-nitrosylation of RGA to coordinate the balance of growth and stress responses when challenged by adverse environments.
- Gibberellin /
- Nitric oxide /
- S-nitrosylation /
- DELLA repressors /
- Stress responses

HTML全文

参考文献(65)

Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J.,Harberd, N.P., 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91-94

Achard, P., Gusti, A., Cheminant, S., Alioua, M., Dhondt, S., Coppens, F., Beemster, G.T.,Genschik, P., 2009. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol. 19, 1188-1193

Achard, P., Liao, L., Jiang, C., Desnos, T., Bartlett, J., Fu, X.,Harberd, N.P., 2007. Dellas contribute to plant photomorphogenesis. Plant Physiol. 143, 1163-1172

Albertos, P., Romero-Puertas, M.C., Tatematsu, K., Mateos, I., Sanchez-Vicente, I., Nambara, E.,Lorenzo, O., 2015. S-nitrosylation triggers abi5 degradation to promote seed germination and seedling growth. Nat. Commun. 6, 8669

An, F., Zhang, X., Zhu, Z., Ji, Y., He, W., Jiang, Z., Li, M.,Guo, H., 2012. Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seedlings. Cell Res. 22, 915-927

Astier, J., Rasul, S., Koen, E., Manzoor, H., Besson-Bard, A., Lamotte, O., Jeandroz, S., Durner, J., Lindermayr, C.,Wendehenne, D., 2011. S-nitrosylation:An emerging post-translational protein modification in plants. Plant Sci. 181, 527-533

Bai, M.Y., Shang, J.X., Oh, E., Fan, M., Bai, Y., Zentella, R., Sun, T.P.,Wang, Z.Y., 2012. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat. Cell Biol. 14, 810-817

Bechtold, N.,Pelletier, G., 1998. In planta agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259-266

Belda-Palazon, B., Adamo, M., Valerio, C., Ferreira, L.J., Confraria, A., Reis-Barata, D., Rodrigues, A., Meyer, C., Rodriguez, P.L.,Baena-Gonzalez, E., 2020. A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat. Plants 6, 1345-1353

Benhar, M., Forrester, M.T.,Stamler, J.S., 2009. Protein denitrosylation:Enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10, 721-732

Chen, L., Wu, R., Feng, J., Feng, T., Wang, C., Hu, J., Zhan, N., Li, Y., Ma, X., Ren, B., et al., 2020. Transnitrosylation mediated by the non-canonical catalase ROG1 regulates nitric oxide signaling in plants. Dev. Cell 53, 444-457 e445

Chen, R.Q., Sun, S.L., Wang, C., Li, Y.S., Liang, Y., An, F.Y., Li, C., Dong, H.L., Yang, X.H., Zhang, J., et al., 2009. The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res. 19, 1377-1387

Cheng, H., Qin, L., Lee, S., Fu, X., Richards, D.E., Cao, D., Luo, D., Harberd, N.P.,Peng, J., 2004. Gibberellin regulates Arabidopsis floral development via suppression of della protein function. Development 131, 1055-1064

Conti, L., Nelis, S., Zhang, C., Woodcock, A., Swarup, R., Galbiati, M., Tonelli, C., Napier, R., Hedden, P., Bennett, M., et al., 2014. Small ubiquitin-like modifier protein sumo enables plants to control growth independently of the phytohormone gibberellin. Dev. Cell 28, 102-110

Dai, C.,Xue, H.W., 2010. Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J. 29, 1916-1927

Daviere, J.M.,Achard, P., 2013. Gibberellin signaling in plants. Development 140, 1147-1151

de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E.,Prat, S., 2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480-484

Debeaujon, I.,Koornneef, M., 2000. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol. 122, 415-424

Dill, A., Thomas, S.G., Hu, J., Steber, C.M.,Sun, T.P., 2004. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16, 1392-1405

Duan, Q., Liu, M.J., Kita, D., Jordan, S.S., Yeh, F.J., Yvon, R., Carpenter, H., Federico, A.N., Garcia-Valencia, L.E., Eyles, S.J., et al., 2020. Feronia controls pectin- and nitric oxide-mediated male-female interaction. Nature 579, 561-566

Feechan, A., Kwon, E., Yun, B.W., Wang, Y., Pallas, J.A.,Loake, G.J., 2005. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U S A 102, 8054-8059

Feng, J., Chen, L.,Zuo, J., 2019. Protein S-nitrosylation in plants:Current progresses and challenges. J. Integr. Plant Biol. 61, 1206-1223

Feng, J., Wang, C., Chen, Q., Chen, H., Ren, B., Li, X.,Zuo, J., 2013. S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat. Commun. 4, 1529

Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., Chen, L., Yu, L., Iglesias-Pedraz, J.M., Kircher, S., et al., 2008. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475-479

Fernandez-Marcos, M., Sanz, L., Lewis, D.R., Muday, G.K.,Lorenzo, O., 2011. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. U S A 108, 18506-18511

He, Y., Tang, R.H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., Jing, L., Yang, Z., Chen, L., Guo, F., et al., 2004. Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968-1971

Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E.,Stamler, J.S., 2005. Protein S-nitrosylation:purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150-166

Hou, X., Lee, L.Y., Xia, K., Yan, Y.,Yu, H., 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev. Cell 19, 884-894

Hu, J., Huang, X., Chen, L., Sun, X., Lu, C., Zhang, L., Wang, Y.,Zuo, J., 2015. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol. 167, 1731-1746

Hu, J., Yang, H., Mu, J., Lu, T., Peng, J., Deng, X., Kong, Z., Bao, S., Cao, X.,Zuo, J., 2017. Nitric oxide regulates protein methylation during stress responses in plants. Mol. Cell 67, 702-710 e704

Huang, J., Tang, D., Shen, Y., Qin, B., Hong, L., You, A., Li, M., Wang, X., Yu, H., Gu, M., et al., 2010. Activation of gibberellin 2-oxidase 6 decreases active gibberellin levels and creates a dominant semi-dwarf phenotype in rice (oryza sativa L.). J Genet. Genomics 37, 23-36

King, K.E., Moritz, T.,Harberd, N.P., 2001. Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767-776

Kneeshaw, S., Gelineau, S., Tada, Y., Loake, G.J.,Spoel, S.H., 2014. Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol. Cell 56, 153-162

Kwon, E., Feechan, A., Yun, B.W., Hwang, B.H., Pallas, J.A., Kang, J.G.,Loake, G.J., 2012. AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236, 887-900

Lee, U., Wie, C., Fernandez, B.O., Feelisch, M.,Vierling, E., 2008. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20, 786-802

Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J.,Stamler, J.S., 2001. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494

Liu, W.Z., Kong, D.D., Gu, X.X., Gao, H.B., Wang, J.Z., Xia, M., Gao, Q., Tian, L.L., Xu, Z.H., Bao, F., et al., 2013. Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc. Natl. Acad. Sci. U S A 110, 1548-1553

Lozano-Juste, J.,Leon, J., 2011. Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol. 156, 1410-1423

Ren, B., Chen, Q., Hong, S., Zhao, W., Feng, J., Feng, H.,Zuo, J., 2013. The Arabidopsis eukaryotic translation initiation factor eIF5A-2 regulates root protoxylem development by modulating cytokinin signaling. Plant Cell 25, 3841-3857

Schwechheimer, C.,Willige, B.C., 2009. Shedding light on gibberellic acid signalling. Curr. Opin. Plant Biol. 12, 57-62

Shu, K., Wu, Y., Yang, W.,Xie, Q., 2014. Concurrent deficiency of gibberellins and abscisic acid causes plant male sterility. J Genet. Genomics 41, 601-604

Silverstone, A.L., Jung, H.S., Dill, A., Kawaide, H., Kamiya, Y.,Sun, T.P., 2001. Repressing a repressor:Gibberellin-induced rapid reduction of the rga protein in Arabidopsis. Plant Cell 13, 1555-1566

Smakowska, E., Kong, J., Busch, W.,Belkhadir, Y., 2016. Organ-specific regulation of growth-defense tradeoffs by plants. Curr. Opin. Plant Biol. 29, 129-137

Stamler, J.S., Simon, D.I., Osborne, J.A., Mullins, M.E., Jaraki, O., Michel, T., Singel, D.J.,Loscalzo, J., 1992. S-nitrosylation of proteins with nitric oxide:Synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. U S A 89, 444-448

Sun, T.P., 2011. The molecular mechanism and evolution of the ga-gid1-della signaling module in plants. Curr. Biol. 21, R338-345

Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zuo, J.,Dong, X., 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952-956

Terrile, M.C., Paris, R., Calderon-Villalobos, L.I., Iglesias, M.J., Lamattina, L., Estelle, M.,Casalongue, C.A., 2012. Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J. 70, 492-500

Ubeda-Tomas, S., Federici, F., Casimiro, I., Beemster, G.T., Bhalerao, R., Swarup, R., Doerner, P., Haseloff, J.,Bennett, M.J., 2009. Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr. Biol. 19, 1194-1199

Ubeda-Tomas, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G.T.S., Hedden, P., Bhalerao, R.,Bennett, M.J., 2008. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat. Cell Biol. 10, 625-628

Verma, V., Ravindran, P.,Kumar, P.P., 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16, 86

Wang, P., Du, Y., Hou, Y.J., Zhao, Y., Hsu, C.C., Yuan, F., Zhu, X., Tao, W.A., Song, C.P.,Zhu, J.K., 2015. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc. Natl. Acad. Sci. U S A 112, 613-618

Wang, P., Du, Y., Li, Y., Ren, D.,Song, C.P., 2010. Hydrogen peroxide-mediated activation of MAP Kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22, 2981-2998

Wang, F., Chen, X., Dong, S., Jiang, X., Wang, L., Yu, J.,Zhou, Y., 2020a. Crosstalk of PIF4 and DELLA modulates cbf transcript and hormone homeostasis in cold response in tomato. Plant Biotechnol. J. 18, 1041-1055

Wang, Z., Liu, L., Cheng, C., Ren, Z., Xu, S.,Li, X., 2020. GAI functions in the plant response to dehydration stress in Arabidopsis thaliana. Int. J. Mol. Sci. 21

Wilson, R.N., Heckman, J.W.,Somerville, C.R., 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol. 100, 403-408

Xu, H., Liu, Q., Yao, T.,Fu, X., 2014. Shedding light on integrative GA signaling. Curr. Opin. Plant Biol. 21, 89-95

Yang, D.L., Yao, J., Mei, C.S., Tong, X.H., Zeng, L.J., Li, Q., Xiao, L.T., Sun, T.P., Li, J., Deng, X.W., et al., 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc. Natl. Acad. Sci. U S A 109, E1192-1200

Yang, H., Mu, J., Chen, L., Feng, J., Hu, J., Li, L., Zhou, J.M.,Zuo, J., 2015. S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 167, 1604-1615

Yu, M., Lamattina, L., Spoel, S.H.,Loake, G.J., 2014. Nitric oxide function in plant biology:A redox cue in deconvolution. New Phytol. 202, 1142-1156

Zentella, R., Hu, J., Hsieh, W.P., Matsumoto, P.A., Dawdy, A., Barnhill, B., Oldenhof, H., Hartweck, L.M., Maitra, S., Thomas, S.G., et al., 2016. O-glcnacylation of master growth repressor della by secret agent modulates multiple signaling pathways in Arabidopsis. Genes Dev. 30, 164-176

Zhao, M.G., Liu, R.J., Chen, L., Tian, Q.Y.,Zhang, W.H., 2009. Glucose-induced inhibition of seed germination in Lotus japonicus is alleviated by nitric oxide and spermine. J. Plant Physiol. 166, 213-218

Zhou, J.M.,Zhang, Y., 2020. Plant immunity:Danger perception and signaling. Cell 181, 978-989

Zhou, S., Jia, L., Chu, H., Wu, D., Peng, X., Liu, X., Zhang, J., Zhao, J., Chen, K.,Zhao, L., 2016. Arabidopsis CAM1 and CAM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding. PLoS Genet. 12, e1006255

Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324

Zuo, J., Niu, Q.W.,Chua, N.H., 2000. An estrogen receptor-based transactivator xve mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265-273

施引文献

资源附件(0)

访问统计

点击查看大图

计量

文章访问数: 43
HTML全文浏览量: 28
PDF下载量: 0
被引次数: 0

姓名
邮箱
手机号码
标题
留言内容
验证码

留言板

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

doi: 10.1016/j.jgg.2022.02.023

通讯作者:
Lichao Chen,E-mail:lcchen@genetics.ac.cn

Jianru Zuo,E-mail:jrzuo@genetics.ac.cn

计量

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

计量

目录

留言板

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

doi: 10.1016/j.jgg.2022.02.023

通讯作者: Lichao Chen,E-mail:lcchen@genetics.ac.cn Jianru Zuo,E-mail:jrzuo@genetics.ac.cn

计量

出版历程

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

计量

出版历程

目录

通讯作者:
Lichao Chen,E-mail:lcchen@genetics.ac.cn

Jianru Zuo,E-mail:jrzuo@genetics.ac.cn