GENERAL CONTROL NONREPRESSIBLE4 Degrades 14-3-3 and the RIN4 Complex to Regulate Stomatal Aperture with Implications on Nonhost Disease Resistance and Drought Tolerance

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2017 Sep 1

PMID 28855332

Citations 32

Authors

Amita Kaundal

Vemanna S Ramu

Sunhee Oh

Seonghee Lee

Bikram Pant

Hee-Kyung Lee

Clemencia M Rojas

Muthappa Senthil-Kumar

Kirankumar S Mysore

Affiliations

Soon will be listed here.

Abstract

Plants have complex and adaptive innate immune responses against pathogen infections. Stomata are key entry points for many plant pathogens. Both pathogens and plants regulate stomatal aperture for pathogen entry and defense, respectively. Not all plant proteins involved in stomatal aperture regulation have been identified. Here, we report GENERAL CONTROL NONREPRESSIBLE4 (GCN4), an AAA-ATPase family protein, as one of the key proteins regulating stomatal aperture during biotic and abiotic stress. Silencing of in and compromises host and nonhost disease resistance due to open stomata during pathogen infection. overexpression plants have reduced H-ATPase activity, stomata that are less responsive to pathogen virulence factors such as coronatine (phytotoxin produced by the bacterium ) or fusicoccin (a fungal toxin produced by the fungus ), reduced pathogen entry, and enhanced drought tolerance. This study also demonstrates that AtGCN4 interacts with RIN4 and 14-3-3 proteins and suggests that GCN4 degrades RIN4 and 14-3-3 proteins via a proteasome-mediated pathway and thereby reduces the activity of the plasma membrane H-ATPase complex, thus reducing proton pump activity to close stomata.

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References

Mackey D, Holt 3rd B, Wiig A, Dangl J . RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell. 2002; 108(6):743-54. DOI: 10.1016/s0092-8674(02)00661-x. View

Ustun S, Bartetzko V, Bornke F . The Xanthomonas effector XopJ triggers a conditional hypersensitive response upon treatment of N. benthamiana leaves with salicylic acid. Front Plant Sci. 2015; 6:599. PMC: 4522559. DOI: 10.3389/fpls.2015.00599. View

Lee S, Yang D, Uppalapati S, Sumner L, Mysore K . Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol. 2013; 13:65. PMC: 3648423. DOI: 10.1186/1471-2229-13-65. View

Sousa R . Structural mechanisms of chaperone mediated protein disaggregation. Front Mol Biosci. 2015; 1:12. PMC: 4428496. DOI: 10.3389/fmolb.2014.00012. View

Bar-Nun S, Glickman M . Proteasomal AAA-ATPases: structure and function. Biochim Biophys Acta. 2011; 1823(1):67-82. DOI: 10.1016/j.bbamcr.2011.07.009. View

Chitrakar R, Melotto M . Assessing stomatal response to live bacterial cells using whole leaf imaging. J Vis Exp. 2010; (44). PMC: 3185621. DOI: 10.3791/2185. View

Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J . Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe. 2010; 7(2):164-75. PMC: 3328509. DOI: 10.1016/j.chom.2010.01.009. View

Melotto M, Underwood W, Koczan J, Nomura K, He S . Plant stomata function in innate immunity against bacterial invasion. Cell. 2006; 126(5):969-80. DOI: 10.1016/j.cell.2006.06.054. View

Sirichandra C, Gu D, Hu H, Davanture M, Lee S, Djaoui M . Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 2009; 583(18):2982-6. DOI: 10.1016/j.febslet.2009.08.033. View

10.

Serebriiskii I, Khazak V, Golemis E . A two-hybrid dual bait system to discriminate specificity of protein interactions. J Biol Chem. 1999; 274(24):17080-7. DOI: 10.1074/jbc.274.24.17080. View

11.

Misra B, de Armas E, Tong Z, Chen S . Metabolomic Responses of Guard Cells and Mesophyll Cells to Bicarbonate. PLoS One. 2015; 10(12):e0144206. PMC: 4671721. DOI: 10.1371/journal.pone.0144206. View

12.

Mara C, Grigorova B, Liu Z . Floral-dip transformation of Arabidopsis thaliana to examine pTSO2::beta-glucuronidase reporter gene expression. J Vis Exp. 2010; (40). PMC: 3153893. DOI: 10.3791/1952. View

13.

Lim C, Baek W, Jung J, Kim J, Lee S . Function of ABA in Stomatal Defense against Biotic and Drought Stresses. Int J Mol Sci. 2015; 16(7):15251-70. PMC: 4519898. DOI: 10.3390/ijms160715251. View

14.

Jahn T, Fuglsang A, Olsson A, Bruntrup I, Collinge D, Volkmann D . The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. Plant Cell. 1997; 9(10):1805-14. PMC: 157023. DOI: 10.1105/tpc.9.10.1805. View

15.

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

16.

Arnaud D, Hwang I . A sophisticated network of signaling pathways regulates stomatal defenses to bacterial pathogens. Mol Plant. 2015; 8(4):566-81. DOI: 10.1016/j.molp.2014.10.012. View

17.

Hanson P, Whiteheart S . AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol. 2005; 6(7):519-29. DOI: 10.1038/nrm1684. View

18.

Lozano-Duran R, Bourdais G, He S, Robatzek S . The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol. 2013; 202(1):259-269. DOI: 10.1111/nph.12651. View

19.

Meng X, Zhang S . MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol. 2013; 51:245-66. DOI: 10.1146/annurev-phyto-082712-102314. View

20.

Lee D, Bourdais G, Yu G, Robatzek S, Coaker G . Phosphorylation of the Plant Immune Regulator RPM1-INTERACTING PROTEIN4 Enhances Plant Plasma Membrane H⁺-ATPase Activity and Inhibits Flagellin-Triggered Immune Responses in Arabidopsis. Plant Cell. 2015; 27(7):2042-56. PMC: 4531345. DOI: 10.1105/tpc.114.132308. View