Mitochondrial Pyruvate Carrier 1 Mediates Abscisic Acid-regulated Stomatal Closure and the Drought Response by Affecting Cellular Pyruvate Content in Arabidopsis Thaliana

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2017 Nov 24

PMID 29166881

Citations 17

Authors

Jian-Lin Shen

Chun-Long Li

Mei Wang

Li-Long He

Min-Yan Lin

Dong-Hua Chen

Wei Zhang

Affiliations

Soon will be listed here.

Abstract

Background: Stomata are micropores surrounded by pairs of guard cells, and their opening is finely controlled to balance water vapor loss as transpiration and CO absorption for photosynthesis. The regulatory signaling network for stomatal movement is complicated, and increasing numbers of new genes have been shown to be involved in this process. Our previous study indicated that a member of the plant putative mitochondrial pyruvate carrier (MPC) family, NRGA1, is a negative regulator of guard cell abscisic acid (ABA) signaling. In this study, we identified novel physiological roles of pyruvate and MPC1, another member of the MPC family, in the regulation of stomatal closure in Arabidopsis.

Results: Loss-of-function mutants of MPC1 (mpc1) were hypersensitive to ABA-induced stomatal closure and ABA-activated guard cell slow-type anion currents, and showed a reduced rate of water loss upon drought treatment compared with wild-type plants. In contrast, plants overexpressing MPC1 showed a hyposensitive ABA response and increased sensitivity to drought stress. In addition, mpc1 mutants accumulated more pyruvate after drought or ABA treatment. The increased pyruvate content also induced stomatal closure and activated the slow-type anion channels of guard cells, and this process was dependent on the function of RbohD/F NADPH oxidases and reactive oxygen species concentrations in guard cells.

Conclusions: Our findings revealed the essential roles of MPC1 and pyruvate in stomatal movement and plant drought resistance.

Citing Articles

Orogeny and High Pollen Flow as Driving Forces for High Genetic Diversity of Endangered (Franch.) Pax Endemic to China.

Xia X, Yu X, Wu Y, Liao J, Pan X, Zheng Y Int J Mol Sci. 2025; 26(2).

PMID: 39859290 PMC: 11765465. DOI: 10.3390/ijms26020574.

Starch metabolism in guard cells: At the intersection of environmental stimuli and stomatal movement.

Dang T, Piro L, Pasini C, Santelia D Plant Physiol. 2024; 196(3):1758-1777.

PMID: 39115378 PMC: 11531838. DOI: 10.1093/plphys/kiae414.

Beneficial Effect of Exogenously Applied Calcium Pyruvate in Alleviating Water Deficit in Sugarcane as Assessed by Chlorophyll a Fluorescence Technique.

Dias M, da Silva F, Fernandes P, Farias C, de Lima R, da Silva M Plants (Basel). 2024; 13(3).

PMID: 38337967 PMC: 10856894. DOI: 10.3390/plants13030434.

Transcriptomic Insights into Abies koreana Drought Tolerance Conferred by Aureobasidium pullulans AK10.

Park J, Mannaa M, Han G, Jung H, Jeon H, Kim J Plant Pathol J. 2024; 40(1):30-39.

PMID: 38326956 PMC: 10850533. DOI: 10.5423/PPJ.FT.11.2023.0161.

Fifty years of the mitochondrial pyruvate carrier: New insights into its structure, function, and inhibition.

Tavoulari S, Sichrovsky M, Kunji E Acta Physiol (Oxf). 2023; 238(4):e14016.

PMID: 37366179 PMC: 10909473. DOI: 10.1111/apha.14016.

References

Ren S, Lyle C, Jiang G, Penumala A . Soybean Salt Tolerance 1 (GmST1) Reduces ROS Production, Enhances ABA Sensitivity, and Abiotic Stress Tolerance in Arabidopsis thaliana. Front Plant Sci. 2016; 7:445. PMC: 4826999. DOI: 10.3389/fpls.2016.00445. View

Pan Y . Mitochondria, reactive oxygen species, and chronological aging: a message from yeast. Exp Gerontol. 2011; 46(11):847-52. DOI: 10.1016/j.exger.2011.08.007. View

Bender T, Pena G, Martinou J . Regulation of mitochondrial pyruvate uptake by alternative pyruvate carrier complexes. EMBO J. 2015; 34(7):911-24. PMC: 4388599. DOI: 10.15252/embj.201490197. View

Choi D, Hwang I, Hwang B . Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper. Plant Cell. 2012; 24(4):1675-90. PMC: 3398571. DOI: 10.1105/tpc.112.095869. View

You J, Chan Z . ROS Regulation During Abiotic Stress Responses in Crop Plants. Front Plant Sci. 2015; 6:1092. PMC: 4672674. DOI: 10.3389/fpls.2015.01092. View

Daloso D, Dos Anjos L, Fernie A . Roles of sucrose in guard cell regulation. New Phytol. 2016; 211(3):809-18. DOI: 10.1111/nph.13950. View

Okamoto M, Peterson F, Defries A, Park S, Endo A, Nambara E . Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. Proc Natl Acad Sci U S A. 2013; 110(29):12132-7. PMC: 3718107. DOI: 10.1073/pnas.1305919110. View

Shang Y, Dai C, Lee M, Kwak J, Nam K . BRI1-Associated Receptor Kinase 1 Regulates Guard Cell ABA Signaling Mediated by Open Stomata 1 in Arabidopsis. Mol Plant. 2016; 9(3):447-460. DOI: 10.1016/j.molp.2015.12.014. View

Wang M, Ma X, Shen J, Li C, Zhang W . The ongoing story: the mitochondria pyruvate carrier 1 in plant stress response in Arabidopsis. Plant Signal Behav. 2014; 9(10):e973810. PMC: 4623219. DOI: 10.4161/15592324.2014.973810. View

10.

Gray L, Rauckhorst A, Taylor E . A Method for Multiplexed Measurement of Mitochondrial Pyruvate Carrier Activity. J Biol Chem. 2016; 291(14):7409-17. PMC: 4817172. DOI: 10.1074/jbc.M115.711663. View

11.

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

12.

Rauckhorst A, Taylor E . Mitochondrial pyruvate carrier function and cancer metabolism. Curr Opin Genet Dev. 2016; 38:102-109. PMC: 5017534. DOI: 10.1016/j.gde.2016.05.003. View

13.

Hu H, Xiong L . Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol. 2013; 65:715-41. DOI: 10.1146/annurev-arplant-050213-040000. View

14.

Yang D, Shi Z, Bao Y, Yan J, Yang Z, Yu H . Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity. Plant Physiol. 2017; 175(1):424-437. PMC: 5580750. DOI: 10.1104/pp.17.00495. View

15.

Perez I, Brown P . The role of ROS signaling in cross-tolerance: from model to crop. Front Plant Sci. 2015; 5:754. PMC: 4274871. DOI: 10.3389/fpls.2014.00754. View

16.

Zhang W, Nilson S, Assmann S . Isolation and whole-cell patch clamping of Arabidopsis guard cell protoplasts. CSH Protoc. 2011; 2008:pdb.prot5014. DOI: 10.1101/pdb.prot5014. View

17.

Osakabe Y, Osakabe K, Shinozaki K, Tran L . Response of plants to water stress. Front Plant Sci. 2014; 5:86. PMC: 3952189. DOI: 10.3389/fpls.2014.00086. View

18.

Lee S, Lim C, Lan W, He K, Luan S . ABA signaling in guard cells entails a dynamic protein-protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol Plant. 2012; 6(2):528-38. DOI: 10.1093/mp/sss078. View

19.

Santelia D, Lawson T . Rethinking Guard Cell Metabolism. Plant Physiol. 2016; 172(3):1371-1392. PMC: 5100799. DOI: 10.1104/pp.16.00767. View

20.

Schroeder J, Allen G, Hugouvieux V, Kwak J, Waner D . GUARD CELL SIGNAL TRANSDUCTION. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52:627-658. DOI: 10.1146/annurev.arplant.52.1.627. View