SALT OVERLY SENSITIVE 1 is Inhibited by Clade D Protein Phosphatase 2C D6 and D7 in Arabidopsis Thaliana

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2022 Sep 23

PMID 36149299

Authors

Haiqi Fu

Xiang Yu

Yuanyuan Jiang

Yuhan Wang

Yongqing Yang

She Chen

Qijun Chen

Yan Guo

Affiliations

Soon will be listed here.

Abstract

The salt overly sensitive (SOS) pathway is essential for maintaining sodium ion homeostasis in plants. This conserved pathway is activated by a calcium signaling-dependent phosphorylation cascade. However, the identity of the phosphatases and their regulatory mechanisms that would deactivate the SOS pathway remain unclear. In this study, we demonstrate that PP2C.D6 and PP2C.D7, which belong to clade D of the protein phosphatase 2C (PP2C) subfamily in Arabidopsis thaliana, directly interact with SOS1 and inhibit its Na+/H+ antiporter activity under non-salt-stress conditions. Upon salt stress, SOS3-LIKE CALCIUM-BINDING PROTEIN8 (SCaBP8), a member of the SOS pathway, interacts with the PP2Cs and suppresses their phosphatase activity; simultaneously, SCaBP8 regulates the subcellular localization of PP2C.D6 by releasing it from the plasma membrane. Thus, we identified two negative regulators of the SOS pathway that repress SOS1 activity under nonstress conditions. These processes set the stage for the activation of SOS1 by the kinase SOS2 to achieve plant salt tolerance. Our results suggest that reversible phosphorylation/dephosphorylation is crucial for the regulation of the SOS pathway, and that calcium sensors play dual roles in activating/deactivating SOS2 and PP2C phosphatases under salt stress.

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References

Quintero F, Ohta M, Shi H, Zhu J, Pardo J . Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci U S A. 2002; 99(13):9061-6. PMC: 124423. DOI: 10.1073/pnas.132092099. View

Xue Y, Yang Y, Yang Z, Wang X, Guo Y . VAMP711 Is Required for Abscisic Acid-Mediated Inhibition of Plasma Membrane H-ATPase Activity. Plant Physiol. 2018; 178(3):1332-1343. PMC: 6236615. DOI: 10.1104/pp.18.00499. View

Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R . Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 2007; 146(2):368-76. PMC: 2245818. DOI: 10.1104/pp.107.111740. View

Batistic O, Kudla J . Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta. 2004; 219(6):915-24. DOI: 10.1007/s00425-004-1333-3. View

Wong J, Spartz A, Park M, Du M, Gray W . Mutation of a Conserved Motif of PP2C.D Phosphatases Confers SAUR Immunity and Constitutive Activity. Plant Physiol. 2019; 181(1):353-366. PMC: 6716246. DOI: 10.1104/pp.19.00496. View

Fuchs S, Grill E, Meskiene I, Schweighofer A . Type 2C protein phosphatases in plants. FEBS J. 2012; 280(2):681-93. DOI: 10.1111/j.1742-4658.2012.08670.x. View

Yang Y, Guo Y . Unraveling salt stress signaling in plants. J Integr Plant Biol. 2018; 60(9):796-804. DOI: 10.1111/jipb.12689. View

Gosti F, Beaudoin N, Serizet C, Webb A, Vartanian N, Giraudat J . ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell. 1999; 11(10):1897-910. PMC: 144098. DOI: 10.1105/tpc.11.10.1897. View

Palmgren M . PLANT PLASMA MEMBRANE H+-ATPases: Powerhouses for Nutrient Uptake. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52:817-845. DOI: 10.1146/annurev.arplant.52.1.817. View

10.

Callis J, Raasch J, Vierstra R . Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J Biol Chem. 1990; 265(21):12486-93. View

11.

Quintero F, Martinez-Atienza J, Villalta I, Jiang X, Kim W, Ali Z . Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci U S A. 2011; 108(6):2611-6. PMC: 3038701. DOI: 10.1073/pnas.1018921108. View

12.

Ohta M, Guo Y, Halfter U, Zhu J . A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci U S A. 2003; 100(20):11771-6. PMC: 208833. DOI: 10.1073/pnas.2034853100. View

13.

Creamer T . Calcineurin. Cell Commun Signal. 2020; 18(1):137. PMC: 7456046. DOI: 10.1186/s12964-020-00636-4. View

14.

Ma L, Ye J, Yang Y, Lin H, Yue L, Luo J . The SOS2-SCaBP8 Complex Generates and Fine-Tunes an AtANN4-Dependent Calcium Signature under Salt Stress. Dev Cell. 2019; 48(5):697-709.e5. DOI: 10.1016/j.devcel.2019.02.010. View

15.

Guo Y, Qiu Q, Quintero F, Pardo J, Ohta M, Zhang C . Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell. 2004; 16(2):435-49. PMC: 341915. DOI: 10.1105/tpc.019174. View

16.

Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z . A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell. 2012; 24(6):2546-61. PMC: 3406912. DOI: 10.1105/tpc.112.100107. View

17.

Lin Z, Li Y, Zhang Z, Liu X, Hsu C, Du Y . A RAF-SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat Commun. 2020; 11(1):613. PMC: 6992735. DOI: 10.1038/s41467-020-14477-9. View

18.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

19.

Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S . In vitro reconstitution of an abscisic acid signalling pathway. Nature. 2009; 462(7273):660-4. PMC: 2803041. DOI: 10.1038/nature08599. View

20.

Wang Z, Xing H, Dong L, Zhang H, Han C, Wang X . Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 2015; 16:144. PMC: 4507317. DOI: 10.1186/s13059-015-0715-0. View