FRET Kinase Sensor Development Reveals SnRK2/OST1 Activation by ABA but Not by MeJA and High CO During Stomatal Closure

Overview

Journal Elife

Specialty Biology

Date 2020 May 29

PMID 32463362

Citations 35

Authors

Li Zhang

Yohei Takahashi

Po-Kai Hsu

Hannes Kollist

Ebe Merilo

Patrick J Krysan

Julian I Schroeder

Affiliations

Soon will be listed here.

Abstract

Sucrose-non-fermenting-1-related protein kinase-2s (SnRK2s) are critical for plant abiotic stress responses, including abscisic acid (ABA) signaling. Here, we develop a genetically encoded reporter for SnRK2 kinase activity. This sensor, named SNACS, shows an increase in the ratio of yellow to cyan fluorescence emission by OST1/SnRK2.6-mediated phosphorylation of a defined serine residue in SNACS. ABA rapidly increases FRET efficiency in leaf cells and guard cells. Interestingly, protein kinase inhibition decreases FRET efficiency in guard cells, providing direct experimental evidence that basal SnRK2 activity prevails in guard cells. Moreover, in contrast to ABA, the stomatal closing stimuli, elevated CO and MeJA, did not increase SNACS FRET ratios. These findings and gas exchange analyses of quintuple/sextuple ABA receptor mutants show that stomatal CO signaling requires basal ABA and SnRK2 signaling, but not SnRK2 activation. A recent model that CO signaling is mediated by PYL4/PYL5 ABA-receptors could not be supported here in two independent labs. We report a potent approach for real-time live-cell investigations of stress signaling.

Citing Articles

Revisiting the Role of Sensors for Shaping Plant Research: Applications and Future Perspectives.

Tyagi A, Mir Z, Ali S Sensors (Basel). 2024; 24(11).

PMID: 38894052 PMC: 11174810. DOI: 10.3390/s24113261.

A network-based modeling framework reveals the core signal transduction network underlying high carbon dioxide-induced stomatal closure in guard cells.

Gan X, Sengottaiyan P, Park K, Assmann S, Albert R PLoS Biol. 2024; 22(5):e3002592.

PMID: 38691548 PMC: 11090369. DOI: 10.1371/journal.pbio.3002592.

GABA does not regulate stomatal CO2 signalling in Arabidopsis.

Piechatzek A, Feng X, Sai N, Yi C, Hurgobin B, Lewsey M J Exp Bot. 2024; 75(21):6856-6871.

PMID: 38628155 PMC: 11565201. DOI: 10.1093/jxb/erae168.

Distinct guard cell-specific remodeling of chromatin accessibility during abscisic acid- and CO-dependent stomatal regulation.

Seller C, Schroeder J Proc Natl Acad Sci U S A. 2023; 120(52):e2310670120.

PMID: 38113262 PMC: 10756262. DOI: 10.1073/pnas.2310670120.

gene enhances drought tolerance via modulating flavonoid biosynthesis in .

Wang A, Liu Y, Li Q, Li X, Zhang X, Kong J Front Plant Sci. 2023; 14:1279468.

PMID: 37885669 PMC: 10598875. DOI: 10.3389/fpls.2023.1279468.

References

Dittrich M, Mueller H, Bauer H, Peirats-Llobet M, Rodriguez P, Geilfus C . The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nat Plants. 2019; 5(9):1002-1011. DOI: 10.1038/s41477-019-0490-0. View

Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N . Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 2009; 50(12):2123-32. DOI: 10.1093/pcp/pcp147. View

Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang P . Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. Elife. 2015; 4. PMC: 4507714. DOI: 10.7554/eLife.03599. View

Sluchanko N, Beelen S, Kulikova A, Weeks S, Antson A, Gusev N . Structural Basis for the Interaction of a Human Small Heat Shock Protein with the 14-3-3 Universal Signaling Regulator. Structure. 2017; 25(2):305-316. PMC: 5321513. DOI: 10.1016/j.str.2016.12.005. View

Lee S, Lan W, Buchanan B, Luan S . A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci U S A. 2009; 106(50):21419-24. PMC: 2795491. DOI: 10.1073/pnas.0910601106. View

Yoshida T, Christmann A, Yamaguchi-Shinozaki K, Grill E, Fernie A . Revisiting the Basal Role of ABA - Roles Outside of Stress. Trends Plant Sci. 2019; 24(7):625-635. DOI: 10.1016/j.tplants.2019.04.008. View

Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K . Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci U S A. 2009; 106(41):17588-93. PMC: 2754379. DOI: 10.1073/pnas.0907095106. View

Kajimoto T, Caliman A, Tobias I, Okada T, Pilo C, Van A . Activation of atypical protein kinase C by sphingosine 1-phosphate revealed by an aPKC-specific activity reporter. Sci Signal. 2019; 12(562). PMC: 6657501. DOI: 10.1126/scisignal.aat6662. View

Chater C, Peng K, Movahedi M, Dunn J, Walker H, Liang Y . Elevated CO2-Induced Responses in Stomata Require ABA and ABA Signaling. Curr Biol. 2015; 25(20):2709-16. PMC: 4612465. DOI: 10.1016/j.cub.2015.09.013. View

10.

Manning G, Whyte D, Martinez R, Hunter T, Sudarsanam S . The protein kinase complement of the human genome. Science. 2002; 298(5600):1912-34. DOI: 10.1126/science.1075762. View

11.

Li J, Assmann S . An Abscisic Acid-Activated and Calcium-Independent Protein Kinase from Guard Cells of Fava Bean. Plant Cell. 1996; 8(12):2359-2368. PMC: 161358. DOI: 10.1105/tpc.8.12.2359. View

12.

Hossain M, Munemasa S, Uraji M, Nakamura Y, Mori I, Murata Y . Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiol. 2011; 156(1):430-8. PMC: 3091061. DOI: 10.1104/pp.111.172254. View

13.

Cherel I, Michard E, Platet N, Mouline K, Alcon C, Sentenac H . Physical and functional interaction of the Arabidopsis K(+) channel AKT2 and phosphatase AtPP2CA. Plant Cell. 2002; 14(5):1133-46. PMC: 150612. DOI: 10.1105/tpc.000943. View

14.

Li J, Wang X, Watson M, Assmann S . Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science. 2000; 287(5451):300-3. DOI: 10.1126/science.287.5451.300. View

15.

Akter N, Sobahan M, Uraji M, Ye W, Hossain M, Mori I . Effects of depletion of glutathione on abscisic acid- and methyl jasmonate-induced stomatal closure in Arabidopsis thaliana. Biosci Biotechnol Biochem. 2012; 76(11):2032-7. DOI: 10.1271/bbb.120384. View

16.

Cutler S, Rodriguez P, Finkelstein R, Abrams S . Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol. 2010; 61:651-79. DOI: 10.1146/annurev-arplant-042809-112122. View

17.

Wang Y, Botvinick E, Zhao Y, Berns M, Usami S, Tsien R . Visualizing the mechanical activation of Src. Nature. 2005; 434(7036):1040-5. DOI: 10.1038/nature03469. View

18.

Zhu J . Abiotic Stress Signaling and Responses in Plants. Cell. 2016; 167(2):313-324. PMC: 5104190. DOI: 10.1016/j.cell.2016.08.029. View

19.

Rudd J, Franklin F, Lord J, Franklin-Tong V . Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas. Plant Cell. 1996; 8(4):713-724. PMC: 161131. DOI: 10.1105/tpc.8.4.713. View

20.

Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia M, Nicolas C, Lorenzo O . Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 2004; 37(3):354-69. DOI: 10.1046/j.1365-313x.2003.01966.x. View