Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization.
The water uptake capacity of plant roots (i.e. their hydraulic conductivity, Lp(r)) 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 Lp(r) concomitantly in the roots of Arabidopsis plants. The inhibition of Lp(r) by SA was partially counteracted by preventing the accumulation of hydrogen peroxide (H(2)O(2)) with exogenous catalase. In addition, exogenous H(2)O(2) was able to reduce Lp(r) by up to 90% in <15 min. Based on the lack of effects of H(2)O(2) on the activity of individual aquaporins in Xenopus oocytes, and on a pharmacological dissection of the action of H(2)O(2) on Lp(r), 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 H(2)O(2) 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 H(2)O(2)-induced internalization of PIPs, to downregulate root water transport.
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Yann
Y
Boursiac
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Julie
J
Boudet
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Olivier
O
Postaire
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Doan-Trung
DT
Luu
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Colette
C
Tournaire-Roux
Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université Montpellier 2, F-34060 Montpellier Cedex 1, France.
Christophe
C
Maurel
D000818:Animals; D020346:Aquaporins / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism; D002478:Cells, Cultured; D015536:Down-Regulation; D018506:Gene Expression Regulation, Plant; D049452:Green Fluorescent Proteins / Q000378:metabolism; D006861:Hydrogen Peroxide / Q000494:pharmacology*; D018613:Microscopy, Confocal; D016253:Microscopy, Immunoelectron; D009865:Oocytes / Q000378:metabolism; D019441:Plant Epidermis / Q000378:metabolism / Q000648:ultrastructure; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified / Q000378:metabolism; D020156:Salicylic Acid / Q000494:pharmacology; D015398:Signal Transduction; D012965:Sodium Chloride / Q000494:pharmacology; D014867:Water / Q000378:metabolism*; D014981:Xenopus / Q000378:metabolism
D020346:Aquaporins; D029681:Arabidopsis Proteins; D014867:Water; D049452:Green Fluorescent Proteins; D012965:Sodium Chloride; D006861:Hydrogen Peroxide; D020156:Salicylic Acid