Plastidial and cytosolic thiol reductases participate in the control of stomatal functioning

• Published in: Plant, cell and environment Vol. 44; no. 5; pp. 1417 - 1435
• Main Authors: Montillet, Jean‐Luc, Rondet, Damien, Brugière, Sabine, Henri, Patricia, Rumeau, Dominique, Reichheld, Jean‐Philippe, Couté, Yohann, Leonhardt, Nathalie, Rey, Pascal
• Format: Journal Article
• Language: English
• Published: Chichester, UK John Wiley & Sons, Ltd 01.05.2021; Wiley Subscription Services, Inc; Wiley
• Subjects: Abscisic acid; Arabidopsis thaliana; Biochemistry, Molecular Biology; Botanics; Conductance; Environmental effects; Gas exchange; Gene expression; Genomics; glutaredoxin; Growth conditions; guard cell; Guard cells; Hydrogen peroxide; Infrared imaging; Leaves; Life Sciences; Mass spectrometry; Mass spectroscopy; peroxiredoxin; Plant growth; Protein structure; Proteins; proteomics; Reactive oxygen species; Reductases; Resistance; Signal transduction; Signaling; signalling; Stomata; Stomatal conductance; Switches; Thermal imaging; Thioredoxin; Vegetal Biology; Arabidopsis thaliana; peroxiredoxin; stomata; proteomics; thioredoxin; guard cell; glutaredoxin; signalling; signaling; thiol reductase
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14013

Stomatal movements via the control of gas exchanges determine plant growth in relation to environmental stimuli through a complex signalling network involving reactive oxygen species that lead to post‐translational modifications of Cys and Met residues, and alter protein activity and/or conformation. Thiol‐reductases (TRs), which include thioredoxins, glutaredoxins (GRXs) and peroxiredoxins (PRXs), participate in signalling pathways through the control of Cys redox status in client proteins. Their involvement in stomatal functioning remains poorly characterized. By performing a mass spectrometry‐based proteomic analysis, we show that numerous thiol reductases, like PRXs, are highly abundant in guard cells. When investigating various Arabidopsis mutants impaired in the expression of TR genes, no change in stomatal density and index was noticed. In optimal growth conditions, a line deficient in cytosolic NADPH‐thioredoxin reductases displayed higher stomatal conductance and lower leaf temperature evaluated by thermal infrared imaging. In contrast, lines deficient in plastidial 2‐CysPRXs or type‐II GRXs exhibited compared to WT reduced conductance and warmer leaves in optimal conditions, and enhanced stomatal closure in epidermal peels treated with abscisic acid or hydrogen peroxide. Altogether, these data strongly support the contribution of thiol redox switches within the signalling network regulating guard cell movements and stomatal functioning. The contribution of thiol reductases to the signalling network governing stomatal functioning remains poorly known. Using proteomics, we show that numerous thiol reductases are abundant in a guard cell‐enriched fraction, and we unveil a stomatal phenotype in Arabidopsis mutants for thiol reductases.