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Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins

Abstract

Flooding of soils results in acute oxygen deprivation (anoxia) of plant roots during winter in temperate latitudes, or after irrigation1, and is a major problem for agriculture. One early response of plants to anoxia and other environmental stresses is downregulation of water uptake due to inhibition of the water permeability (hydraulic conductivity) of roots (Lpr)2,3,4,5. Root water uptake is mediated largely by water channel proteins (aquaporins) of the plasma membrane intrinsic protein (PIP) subgroup6,7,8. These aquaporins may mediate stress-induced inhibition of Lpr2,4,9 but the mechanisms involved are unknown. Here we delineate the whole-root and cell bases for inhibition of water uptake by anoxia and link them to cytosol acidosis. We also uncover a molecular mechanism for aquaporin gating by cytosolic pH. Because it is conserved in all PIPs, this mechanism provides a basis for explaining the inhibition of Lpr by anoxia and possibly other stresses. More generally, our work opens new routes to explore pH-dependent cell signalling processes leading to regulation of water transport in plant tissues or in animal epithelia10.

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Acknowledgements

We thank H. Höfte, H. Sentenac and C. Vander Willigen for critical reading of the manuscript; N. Declerk for discussions; Y. Boursiac for help with cell pressure probe measurements; and J. B. Thibaud and C. Plassard for assistance in micro-electrode pH measurements. This work was supported in part by the Centre National de la Recherche Scientifique (Action Thématique Incitative sur Programme et Equipe ‘Function and regulation of plant aquaporins’). M.S. is on leave from the Laboratorio de Biomembranas, Departamento de Fisiología, Facultad de Medicina, Universidad de Buenos Aires, Argentina.

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Correspondence to Christophe Maurel.

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The authors declare that they have no competing financial interests.

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Further reading

Figure 1: Effects of anoxia and respiratory inhibitors on Arabidopsis root water transport and cytosolic pH.
Figure 2: Effects of an acid load on cytosolic pH and water transport in whole roots and cortex cells.
Figure 3: Effects of a stepwise acid load treatment on cytosolic pH and aquaporin water transport activity in Xenopus oocytes.
Figure 4: Sensitivity of wild-type (WT) and mutant PIP2;2 to cytosolic acidification.

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