Tyrosylprotein sulfotransferase suppresses ABA signaling via sulfation of SnRK2.2/2.3/2.6.
ABA signaling
Arabidopsis
SnRK2.2/2.3/2.6
sulfation
tyrosylprotein sulfotransferase
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
13
12
2022
accepted:
07
04
2023
medline:
23
8
2023
pubmed:
14
4
2023
entrez:
13
4
2023
Statut:
ppublish
Résumé
Phytohormone abscisic acid (ABA) plays vital roles in stress tolerance, while long-term overactivation of ABA signaling suppresses plant growth and development. However, the braking mechanism of ABA responses is not clear. Protein tyrosine sulfation catalyzed by tyrosylprotein sulfotransferase (TPST) is a critical post-translational modification. Through genetic screening, we identified a tpst mutant in Arabidopsis that was hypersensitive to ABA. In-depth analysis revealed that TPST could interact with and sulfate SnRK2.2/2.3/2.6, which accelerated their degradation and weakened the ABA signaling. Taken together, these findings uncovered a novel mechanism of desensitizing ABA responses via protein sulfation.
Substances chimiques
protein-tyrosine sulfotransferase
EC 2.8.2.20
Plant Growth Regulators
0
Abscisic Acid
72S9A8J5GW
Sulfotransferases
EC 2.8.2.-
Arabidopsis Proteins
0
SnRK2 protein, Arabidopsis
0
Protein Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1846-1851Subventions
Organisme : National Natural Science Foundation of China
ID : 31771878 and 32071931
Informations de copyright
© 2023 Institute of Botany, Chinese Academy of Sciences.
Références
Ali, A., Kim, J.K., Jan, M., Khan, H.A., Khan, I.U., Shen, M.Z., Park, J., Lim, C.J., Hussain, S., Baek, D., et al. (2019). Rheostatic control of ABA signaling through HOS15-mediated OST1 degradation. Mol. Plant 12: 1447-1462.
Amano, Y., Tsubouchi, H., Shinohara, H., Ogawa, M., and Matsubayashi, Y. (2007). Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104: 18333-18338.
Chang, Y.N., Wang, Z., Ren, Z., Wang, C.H., Wang, P., Zhu, J.K., Li, X., and Duan, C.G. (2022). NUCLEAR PORE ANCHOR and EARLY IN SHORT DAYS 4 negatively regulate abscisic acid signaling by inhibiting Snf1-related protein kinase2 activity and stability in Arabidopsis. J. Integr. Plant Biol. 64: 2060-2074.
Chen, K., Li, G.J., Bressan, R.A., Song, C.P., Zhu, J.K., and Zhao, Y. (2020a). Abscisic acid dynamics, signaling, and functions in plants. J. Integr. Plant Biol. 62: 25-54.
Chen, S.S., Jia, H.L., Wang, X.F., Shi, C., Wang, X., Ma, P.Y., Wang, J., Ren, M.J., and Li, J.S. (2020b). Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol. Plant 13: 732-744.
Cheng, C., Wang, Z., Ren, Z., Zhi, L., Yao, B., Su, C., Liu, L., and Li, X. (2017). SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet. 13: e1006947.
Davletova, S., Schlauch, K., Coutu, J., and Mittler, R. (2005). The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139: 847-856.
Doll, N.M., Royek, S., Fujita, S., Okuda, S., Chamot, S., Stintzi, A., Widiez, T., Hothorn, M., Schaller, A., and Geldner, N. (2020). A two-way molecular dialogue between embryo and endosperm is required for seed development. Science 367: 431-435.
Goettsch, S., Goettsch, W., Morawietz, H., and Bayer, P. (2002). Shear stress mediates tyrosylprotein sulfotransferase isoform shift in human endothelial cells. Biochem. Biophys. Res. Commun. 294: 541-546.
Greelman, R.A., Mason, H.S., Bensen, R.J., Boyer, J.S., and Mullet, J.E. (1990). Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings analysis of growth, sugar accumulation, and gene expression. Plant Physiol. 92: 205-214.
Kansas, G.S. (1996). Selectins and their ligands: Current concepts and controversies. Blood 88: 3259-3287.
Kaufmann, C., Stuhrwohldt, N., and Sauter, M. (2021). Tyrosylprotein sulfotransferase-dependent and -independent regulation of root development and signaling by PSK LRR receptor kinases in Arabidopsis. J. Exp. Bot. 72: 5508-5521.
Komori, R., Amano, Y., Ogawaohnishi, M., and Matsubayashi, Y. (2009). Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106:15067-15072.
Kulik, A., Wawer, I., Krzywinska, E., Bucholc, M., and Dobrowolska, G. (2011). SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS 15: 859-872.
Ma, T., Yoo, M.J., Zhang, T., Liu, L., Koh, J., Song, W.Y., Harmon, A.C., Sha, W., and Chen, S. (2018). Characterization of thiol-based redox modifications of Brassica napus SNF1-related protein kinase 2.6-2C. FEBS Open Biol. 8: 628-645.
Matsuzaki, Y., Ogawaohnishi, M., Mori, A., and Matsubayashi, Y. (2010). Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329: 1065-1067.
Moore, K.L. (2003). The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278: 24243-24246.
Ogawa-Ohnishi, M., Yamashita, T., Kakita, M., Nakayama, T., Ohkubo, Y., Hayashi, Y., Yamashita, Y., Nomura, T., Noda, S., Shinohara, H., et al. (2022). Peptide ligand-mediated trade-off between plant growth and stress response. Science 378: 175-180.
Peng, Z., and Weyers, J.D.B. (1994). Stomatal sensitivity to abscisic acid following water deficit stress. J. Exp. Bot. 45: 835-845.
Pizzio, G.A., and Rodriguez, P.L. (2022). Dual regulation of SnRK2 signaling by Raf-like MAPKKKs. Mol. Plant 15: 1260-1262.
Takahashi, Y., Zhang, J.B., Hsu, P.-K., Ceciliato, P.H.O., Zhang, L., Dubeaux, G., Munemasa, S., Ge, C.N., Zhao, Y.D., Hauser, F., et al. (2020). MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat. Commun. 11: 12.
Tanaka, S., Nishiyori, T., Kojo, H., Otsubo, R., Tsuruta, M., Kurogi, K., Liu, M.C., Suiko, M., Sakakibara, Y., and Kakuta, Y. (2017). Structural basis for the broad substrate specificity of the human tyrosylprotein sulfotransferase-1. Sci. Rep. 7: 8776.
Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., Ishihama, Y., Hirayama, T., and Shinozaki, K. (2009). Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106: 17588-17593.
Vilela, B., Najar, E., Lumbreras, V., Leung, J., and Pages, M. (2015). Casein Kinase 2 negatively regulates abscisic acid-activated SnRK2s in the core abscisic acid-signaling module. Mol. Plant 8: 709-721.
Wang, C.C., Chen, B.H., Lu, L.Y., Hung, K.S., and Yang, Y.S. (2018). Preparation of tyrosylprotein sulfotransferases for in vitro one-pot enzymatic synthesis of sulfated proteins/peptides. ACS Omega 3: 11633-11642.
Wang, P., Du, Y., Hou, Y.J., Zhao, Y., Hsu, C.C., Yuan, F., Zhu, X., Tao, W.A., Song, C.P., and 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, X., Guo, C., Peng, J., Li, C., Wan, F., Zhang, S., Zhou, Y., Yan, Y., Qi, L., and Sun, K. (2019). ABRE-BINDING FACTORS play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol. 221: 341-355.
Yang, G.D., Yu, Z.P., Gao, L., and Zheng, C.C. (2019). SnRK2s at the crossroads of growth and stress responses. Trends Plant Sci. 24: 672-676.
Yang, Y.S., Wang, C.C., Chen, B.H., Hou, Y.H., Hung, K.S., and Mao, Y.C. (2015). Tyrosine sulfation as a protein post-translational modification. Molecules 20: 2138-2164.