Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization

• Published in: The Plant journal : for cell and molecular biology Vol. 56; no. 2; pp. 207 - 218
• Main Authors: Boursiac, Yann, Boudet, Julie, Postaire, Olivier, Luu, Doan-Trung, Tournaire-Roux, Colette, Maurel, Christophe
• Format: Journal Article
• Language: English
• Published: Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01-10-2008; Blackwell Publishing Ltd; Blackwell Science
• Subjects: Animals; Aquaporin; Aquaporins - metabolism; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Biological and medical sciences; Botany; Cell physiology; Cells, Cultured; Cellular biology; Down-Regulation; Fundamental and applied biological sciences. Psychology; Gene Expression Regulation, Plant; Green Fluorescent Proteins - metabolism; Hydrogen Peroxide - pharmacology; Membranes; Microscopy, Confocal; Microscopy, Immunoelectron; Molecular and cellular biology; Oocytes - metabolism; Plant Epidermis - metabolism; Plant Epidermis - ultrastructure; Plant physiology and development; Plant Roots - genetics; Plant Roots - metabolism; Plants, Genetically Modified - metabolism; reactive oxygen species; root; roots; salicylic acid; Salicylic Acid - pharmacology; salt; Signal Transduction; Sodium Chloride - pharmacology; stress; Water; Water - metabolism; Water and solutes. Absorption, translocation and permeability; Xenopus - metabolism; Water; Salicylic acid; Reactive oxygen species; Membrane protein; salt; Root; Stress; Cell signaling; Salinity; Signal transduction; Plasma membrane; Transport; Aquaporin
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/j.1365-313X.2008.03594.x

The water uptake capacity of plant roots (i.e. their hydraulic conductivity, Lpr) is determined in large part by aquaporins of the plasma membrane intrinsic protein (PIP) subfamily. In the present work, we investigated two stimuli, salicylic acid (SA) and salt, because of their ability to induce an accumulation of reactive oxygen species (ROS) and an inhibition of Lpr concomitantly in the roots of Arabidopsis plants. The inhibition of Lpr by SA was partially counteracted by preventing the accumulation of hydrogen peroxide (H₂O₂) with exogenous catalase. In addition, exogenous H₂O₂ was able to reduce Lpr by up to 90% in <15 min. Based on the lack of effects of H₂O₂ on the activity of individual aquaporins in Xenopus oocytes, and on a pharmacological dissection of the action of H₂O₂ on Lpr, we propose that ROS do not gate Arabidopsis root aquaporins through a direct oxidative mechanism, but rather act through cell signalling mechanisms. Expression in transgenic roots of PIP-GFP fusions and immunogold labelling indicated that external H₂O₂ enhanced, in <15 min, the accumulation of PIPs in intracellular structures tentatively identified as vesicles and small vacuoles. Exposure of roots to SA or salt also induced an intracellular accumulation of the PIP-GFP fusion proteins, and these effects were fully counteracted by co-treatment with exogenous catalase. In conclusion, the present work identifies SA as a novel regulator of aquaporins, and delineates an ROS-dependent signalling pathway in the roots of Arabidopsis. Several abiotic and biotic stress-related stimuli potentially share this path, which involves an H₂O₂-induced internalization of PIPs, to downregulate root water transport.