5.9
CiteScore
5.9
Impact Factor
Volume 49 Issue 8
Aug.  2022
Turn off MathJax
Article Contents
Article Navigation >  Journal of Genetics and Genomics  > 2022  >  49(8): 756-765

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

doi: 10.1016/j.jgg.2022.02.023
  •  

    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:

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).

  • Received Date: 2022-02-23
  • Accepted Date: 2022-02-28
  • Rev Recd Date: 2022-02-27
  • Publish Date: 2022-03-08
    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.
    • FullText(HTML)
  • loading
    • References(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
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 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
    Get Citation
    PDF

    Article Metrics

    Article views (208) PDF downloads (33) Cited by ()
    Proportional views
    Related

    Editorial Office

    Journal of Genetics and Genomics

    京ICP备09063187号-7

    No.1, West Beichen Road, Chaoyang District, Beijing 100101, P.R.China

    +86-10-64806528+86-10-64807786jgg@genetics.ac.cn

    Supported by: Beijing Renhe Information Technology Co. Ltd  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return