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Volume 50 Issue 7
Jul.  2023
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Nitric oxide-mediated S-nitrosylation of IAA17 protein in intrinsically disordered region represses auxin signaling

doi: 10.1016/j.jgg.2023.05.001
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This work is supported by grants from the National Natural Science Foundation of China (31830017), Chinese Academy of Sciences (XDB27030207), the Hainan Excellent Talent Team, and State Key Laboratory of Plant Genomics (SKLPG2023-22).

  • Received Date: 2023-04-30
  • Accepted Date: 2023-05-01
  • Publish Date: 2023-07-28
  • The phytohormone auxin plays crucial roles in nearly every aspect of plant growth and development. Auxin signaling is activated through the phytohormone-induced proteasomal degradation of the Auxin/INDOLE-3-ACETIC ACID (Aux/IAA) family of transcriptional repressors. Notably, many auxin-modulated physiological processes are also regulated by nitric oxide (NO) that executes its biological effects predominantly through protein S-nitrosylation at specific cysteine residues. However, little is known about the molecular mechanisms in regulating the interactive NO and auxin networks. Here, we show that NO represses auxin signaling by inhibiting IAA17 protein degradation. NO induces the S-nitrosylation of Cys-70 located in the intrinsically disordered region of IAA17, which inhibits the TIR1-IAA17 interaction and consequently the proteasomal degradation of IAA17. The accumulation of a higher level of IAA17 attenuates auxin response. Moreover, an IAA17C70W nitrosomimetic mutation renders the accumulation of a higher level of the mutated protein, thereby causing partial resistance to auxin and defective lateral root development. Taken together, these results suggest that S-nitrosylation of IAA17 at Cys-70 inhibits its interaction with TIR1, thereby negatively regulating auxin signaling. This study provides unique molecular insights into the redox-based auxin signaling in regulating plant growth and development.
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  • [1]
    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.
    [2]
    Ayyar, P.V., 2016. Uncovering the role of S-nitrosylation in jasmonic acid signalling during the plant immune response. PhD thesis Edinburgh: IMPS, The University of Edinburgh.
    [3]
    Bechtold, N.,Pelletier, G., 1998. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259-266.
    [4]
    Campos, F.V., Oliveira, J.A., Pereira, M.G., Farnese, F.S., 2019. Nitric oxide and phytohormone interactions in the response of Lactuca sativa to salinity stress. Planta 250, 1475-1489.
    [5]
    Cao, M., Chen, R., Li, P., Yu, Y., Zheng, R., Ge, D., Zheng, W., Wang, X., Gu, Y., Gelova, Z., et al., 2019. TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568, 240-243.
    [6]
    Chaisupa, P., Rahman, M. M., Hildreth, S. B., Moseley, S., Gatling, C., Helm, R. F., Wright, R.C., 2023. Genetically encoded, noise-tolerant, auxin biosensors in yeast facilitate metabolic engineering and directed evolution. bioRxiv, https://doi.org/ https://doi.org/10.1101/2023.03.21.533585
    [7]
    Chen, L., Sun, S., Song, C.P., Zhou, J.M., Li, J., Zuo, J., 2022. Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis. J. Genet. Genomics 49, 756-765.
    [8]
    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.
    [9]
    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.
    [10]
    Cubuk, J., Alston, J.J., Incicco, J.J., Holehouse, A.S., Hall, K.B., Stuchell-Brereton, M.D., Soranno, A., 2023. The disordered N-terminal tail of SARS CoV-2 Nucleocapsid protein forms a dynamic complex with RNA. bioRxiv, https://doi.org/ https://doi.org/10.1101/2023.02.10.527914.
    [11]
    Dharmasiri, N., Dharmasiri, S., Estelle, M., 2005. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
    [12]
    Ding, Z.,Friml, J., 2010. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. U. S. A. 107, 12046-12051.
    [13]
    Emenecker, R.J., Griffith, D., Holehouse, A.S., 2021. Metapredict: a fast, accurate, and easy-to-use predictor of consensus disorder and structure. Biophys. J. 120, 4312-4319.
    [14]
    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.
    [15]
    Feng, J., Chen, L., Zuo, J., 2019. Protein S-nitrosylation in plants: Current progresses and challenges. J. Integr. Plant Biol. 61, 1206-1223.
    [16]
    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.
    [17]
    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 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. U. S. A. 108, 18506-18511.
    [18]
    Fernando, V., Zheng, X., Walia, Y., Sharma, V., Letson, J.,Furuta, S., 2019. S-nitrosylation: an emerging paradigm of redox signaling. Antioxidants 8, 404.
    [19]
    Figueiredo, M.R.A., Strader, L.C., 2022. Intrinsic and extrinsic regulators of Aux/IAA protein degradation dynamics. Trends Biochem. Sci. 47, 865-874.
    [20]
    Gietz, R.D.,Woods, R.A., 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96.
    [21]
    Gray, W.M., del Pozo, J.C., Walker, L., Hobbie, L., Risseeuw, E., Banks, T., Crosby, W.L., Yang, M., Ma, H., Estelle, M., 1999. Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev. 13, 1678-1691.
    [22]
    Gray, W.M., Kepinski, S., Rouse, D., Leyser, O., Estelle, M., 2001. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271-276.
    [23]
    Gupta, K.J., Kaladhar, V.C., Fitzpatrick, T.B., Fernie, A.R., Moller, I.M., Loake, G.J., 2022. Nitric oxide regulation of plant metabolism. Mol. Plant 15, 228-242.
    [24]
    Gupta, K.J., Kolbert, Z., Durner, J., Lindermayr, C., Corpas, F.J., Brouquisse, R., Barroso, J.B., Umbreen, S., Palma, J.M., Hancock, J.T., et al., 2020. Regulating the regulator: nitric oxide control of post-translational modifications. New Phytol. 227, 1319-1325.
    [25]
    Havens, K.A., Guseman, J.M., Jang, S.S., Pierre-Jerome, E., Bolten, N., Klavins, E., Nemhauser, J.L., 2012. A synthetic approach reveals extensive tunability of auxin signaling. Plant Physiol. 160, 135-142.
    [26]
    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.
    [27]
    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.
    [28]
    Humphrey, W., Dalke, A., Schulten, K., 1996. Vmd: Visual molecular dynamics. J. Mol. Graph. 14, 33-38.
    [29]
    Iglesiasa, M.J., Terrile, M.C., Correa-Aragunde, N., Colman, S.L., Izquierdo-Alvarez, A., Fiol, D.F., Paris, R., Sanchez-Lopez, N., Marina, A., Villalobos, L.I.A.C., et al., 2018. Regulation of SCFTIR1/AFBs E3 ligase assembly by S-nitrosylation of Arabidopsis SKP1-like1 impacts on auxin signaling. Redox Biol. 18, 200-210.
    [30]
    Jing, H., Korasick, D.A., Emenecker, R.J., Morffy, N., Wilkinson, E.G., Powers, S.K., Strader, L.C., 2022. Regulation of auxin response factor condensation and nucleo-cytoplasmic partitioning. Nat. Commun. 13, 4015.
    [31]
    Jing, H., Strader, L.C., 2018. Structural biology of auxin signal transduction. In Plant Structural Biology: Hormonal Regulations J Hejatko, ed, 49-66.
    [32]
    Jing, H., Yang, X., Zhang, J., Liu, X., Zheng, H., Dong, G., Nian, J., Feng, J., Xia, B., Qian, Q., et al., 2015. Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling. Nat. Commun. 6, 7395.
    [33]
    Joseph, J.A., Reinhardt, A., Aguirre, A., Chew, P.Y., Russell, K.O., Espinosa, J.R., Garaizar, A., Collepardo-Guevara, R., 2022. Physics-driven coarse-grained model for biomolecular phase separation with near-quantitative accuracy. Nat. Comput. Sci. 1, 732-743.
    [34]
    Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Zidek, A., Potapenko, A., et al., 2021. Highly accurate protein structure prediction with AlphFold. Nature 596, 583-589.
    [35]
    Kohli, S.K., Khanna, K., Bhardwaj, R., Corpas, F.J., Ahmad, P., 2022. Nitric oxide, salicylic acid and oxidative stress: Is it a perfect equilateral triangle? Plant Physiol. Biochem. 184, 56-64.
    [36]
    Kolbert, Z., 2019. Strigolactone-nitric oxide interplay in plants: The story has just begun. Physiol. Plant 165, 487-497.
    [37]
    Kolbert, Z., Barroso, J.B., Brouquisse, R., Corpas, F.J., Gupta, K.J., Lindermayr, C., Loake, G.J., Palma, J.M., Petrivalsky, M., Wendehenne, D., et al., 2019. A forty year journey: The generation and roles of NO in plants. Nitric Oxide 93, 53-70.
    [38]
    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.
    [39]
    Lalmansingh, J.M., Keeley, A.T., Ruff, K.M., Pappu, R.V., Holehouse, A.S., 2023. SOURSOP: A Python package for the analysis of simulations of intrinsically disordered proteins. bioRxiv, https://doi.org/ 10.1101/2023.02.16.528879.
    [40]
    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.
    [41]
    Li, D., Fu, Y., Sun, R., Ling, C.X., Wei, Y., Zhou, H., Zeng, R., Yang, Q., He, S., Gao, W., 2005. pFind: a novel database-searching software system for automated peptide and protein identification via tandem mass spectrometry. Bioinformatics 21, 3049-3050.
    [42]
    Li, R., Jia, Y., Yu, L., Yang, W., Chen, Z., Chen, H., Hu, X., 2018. Nitric oxide promotes light-initiated seed germination by repressing PIF1 expression and stabilizing HFR1. Plant Physiol. Biochem. 123, 204-212.
    [43]
    Li, X., Pan, Y., Chang, B., Wang, Y., Tang, Z., 2016. NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis. Front. Plant Sci. 6, 1203.
    [44]
    Lindermayr, C., Saalbach, G., Bahnweg, G., Durner, J., 2006. Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J. Biol. Chem. 281, 4285-4291.
    [45]
    Lv, B., Yu, Q., Liu, J., Wen, X., Yan, Z., Hu, K., Li, H., Kong, X., Li, C., Tian, H., et al., 2020. Non-canonical AUX/IAA protein IAA33 competes with canonical AUX/IAA repressor IAA5 to negatively regulate auxin signaling. EMBO J. 39, e101515.
    [46]
    McGibbon, R.T., Beauchamp, K.A., Harrigan, M.P., Klein, C., Swails, J.M., Hernandez, C.X., Schwantes, C.R., Wang, L.P., Lane, T.J., Pande, V.S., 2015. MDTraj: a modern open library for the analysis of molecular dynamics trajectories. Biophys. J. 109, 1528-1532.
    [47]
    Mirdita, M., Schutze, K., Moriwaki, Y., Heo, L., Ovchinnikov, S., Steinegger, M., 2022. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679-682.
    [48]
    Morffy, N., Strader, L.C., 2022. Structural aspects of auxin signaling. Cold Spring Harb Perspect Biol. 14, a039883.
    [49]
    Ni, M., Zhang, L., Shi, Y.F., Wang, C., Lu, Y., Pan, J., Liu, J.Z., 2017. Excessive cellular S-nitrosothiol impairs endocytosis of auxin efflux transporter PIN2. Front. Plant Sci. 8, 1988.
    [50]
    Niemeyer, M., Castillo, E.M., Ihling, C.H., Iacobucci, C., Wilde, V., Hellmuth, A., Hoehenwarter, W., Samodelov, S.L., Zurbriggen, M.D., Kastritis, P.L., et al., 2020. Flexibility of intrinsically disordered degrons in AUX/IAA proteins reinforces auxin co-receptor assemblies. Nat. Commun. 11, 2277.
    [51]
    Otvos, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szucs, A., Bottka, S., Dudits, D., Feher, A., 2005. Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J. 43, 849-860.
    [52]
    Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2003. Nitric oxide and cyclic gmp are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol. 132, 1241-1248.
    [53]
    Pagnussat, G.C., Simontacchi, M., Puntarulo, S., Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954-956.
    [54]
    Pande, A., Mun, B.G., Rahim, W., Khan, M., Lee, D.S., Lee, G.M., Al Azzawi, T.N.I., Hussain, A., Kim, C.K., Yun, B.W., 2022. Phytohormonal regulation through protein S-nitrosylation under stress. Front. Plant Sci. 13, 865542.
    [55]
    Pierre-Jerome, E., Wright, R.C., Nemhauser, J.L., 2017. Characterizing auxin response circuits in Saccharomyces cerevisiae by flow cytometry. Methods Mol. Biol. 1497, 271-281.
    [56]
    Powers, S.K.,Strader, L.C., 2020. Regulation of auxin transcriptional responses. Dev. Dyn. 249, 483-495.
    [57]
    Rose, A.S., Bradley, A.R., Valasatava, Y., Duarte, J.M., Prlic, A.,Rose, P.W., 2018. NGL viewer: web-based molecular graphics for large complexes. Bioinformatics 34, 3755-3758.
    [58]
    Shang, J.X., Li, X., Li, C., Zhao, L., 2022. The role of nitric oxide in plant responses to salt stress. Int. J. Mol. Sci. 23, 6167.
    [59]
    Shi, Y.F., Wang, D.L., Wang, C., Culler, A.H., Kreiser, M.A., Suresh, J., Cohen, J.D., Pan, J., Baker, B., Liu, J.Z., 2015. Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol. Plant 8, 1350-1365.
    [60]
    Signorelli, S., Considine, M.J., 2018. Nitric oxide enables germination by a four-pronged attack on ABA-induced seed dormancy. Front. Plant Sci. 9, 296.
    [61]
    Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D., Callis, J., 2006. Keep on going, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18, 3415-3428.
    [62]
    Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zuo, J., Dong, X., 2008. Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952-956.
    [63]
    Tan, X., Calderon-Villalobos, L.I.A., Sharon, M., Zheng, C., Robinson, C.V., Estelle, M., Zheng, N., 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645.
    [64]
    Terrile, M.C., Paris, R., Calderon-Villalobos, L.I.A., 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.
    [65]
    Thompson, A.P., Aktulga, H.M., Berger, R., Bolintineanu, D.S., Brown, W.M., Crozier, P.S., Veld, P.J.I., Kohlmeyer, A., Moore, S.G., Nguyen, T.D., et al., 2022. LAMMPS-a flexible simulation tool for particle-based materials modeling at the atomic, meso, and continuum scales. Comput. Phys. Commun. 271, 108171.
    [66]
    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.
    [67]
    Wang, Y.Q., Feechan, A., Yun, B.W., Shafiei, R., Hofmann, A., Taylor, P., Xue, P., Yang, F.Q., Xie, Z.S., Pallas, J.A., et al., 2009. S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J. Biol. Chem. 284, 2131-2137.
    [68]
    Winkler, M., Niemeyer, M., Hellmuth, A., Janitza, P., Christ, G., Samodelov, S.L., Wilde, V., Majovsky, P., Trujillo, M., Zurbriggen, M.D., et al., 2017. Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction. Nat. Commun. 8, 15706.
    [69]
    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.
    [70]
    Yu, Z., Zhang, F., Friml, J., Ding, Z., 2022. Auxin signaling: Research advances over the past 30 years. J. Integr. Plant Biol. 64, 371-392.
    [71]
    Yun, B.W., Feechan, A., Yin, M., Saidi, N.B.B., Le Bihan, T., Yu, M., Moore, J.W., Kang, J.G., Kwon, E., Spoel, S.H., et al., 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264-268.
    [72]
    Zhan, N., Wang, C., Chen, L., Yang, H., Feng, J., Gong, X., Ren, B., Wu, R., Mu, J., Li, Y., et al., 2018. S-nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants. Mol. Cell 71, 142-154.
    [73]
    Zhang, H.T., Zeng, L.F., He, Q.Y., Tao, W.A., Zha, Z.G., Hu, C.D., 2016. The E3 ubiquitin ligase CHIP mediates ubiquitination and proteasomal degradation of PRMT5. Biochim. Biophys. Acta 1863, 335-346.
    [74]
    Zhang, J., Huang, D., Wang, C., Wang, B., Fang, H., Huo, J., Liao, W., 2019. Recent progress in protein S-nitrosylation in phytohormone signaling. Plant Cell Physiol. 60, 494-502.
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