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JXB Advance Access originally published online on January 5, 2006
Journal of Experimental Botany 2006 57(3):609-621; doi:10.1093/jxb/erj046
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© The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. The online version of this article has been published under an Open Access model. Users are entitled to use, reproduce, disseminate, or display the Open Access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and the Society for Experimental Biology are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact: journals.permissions@oxfordjournals.org

RESEARCH PAPER

Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations

Karina Alleva1 *, Christa M. Niemietz2 *, Moira Sutka1, Christophe Maurel3, Mario Parisi1, Stephen D. Tyerman2 * and Gabriela Amodeo1 *,{dagger}

1Laboratorio de Biomembranas, epartamento de Fisiología, Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155 Piso 7, (C1121ABG) Buenos Aires, Argentina
2University of Adelaide, Agriculture and Wine, Waite Campus, PMB #1, Glen Osmond, SA 5064, Australia
3Biochimie et Physiologie Moléculaire des Plantes, Agro-M/INRA/CNRS/UM2, 2 Place Viala, F-34060 Montpellier cedex, France

{dagger} To whom correspondence should be addressed. E-mail: amodeo{at}dna.uba.ar

Plasma membrane vesicles isolated by two-phase partitioning from the storage root of Beta vulgaris show atypically high water permeability that is equivalent only to those reported for active aquaporins in tonoplast or animal red cells (Pf=542 µm s–1). The values were determined from the shrinking kinetics measured by stopped-flow light scattering. This high Pf was only partially inhibited by mercury (HgCl2) but showed low activation energy (Ea) consistent with water permeation through water channels. To study short-term regulation of water transport that could be the result of channel gating, the effects of pH, divalent cations, and protection against dephosphorylation were tested. The high Pf observed at pH 8.3 was dramatically reduced by medium acidification. Moreover, intra-vesicular acidification (corresponding to the cytoplasmic face of the membrane) shut down the aquaporins. De-phosphorylation was discounted as a regulatory mechanism in this preparation. On the other hand, among divalent cations, only calcium showed a clear effect on aquaporin activity, with two distinct ranges of sensitivity to free Ca2+ concentration (pCa 8 and pCa 4). Since the normal cytoplasmic free Ca2+ sits between these ranges it allows for the possibility of changes in Ca2+ to finely up- or down-regulate water channel activity. The calcium effect is predominantly on the cytoplasmic face, and inhibition corresponds to an increase in the activation energy for water transport. In conclusion, these findings establish both cytoplasmic pH and Ca2+ as important regulatory factors involved in aquaporin gating.

Key words: Aquaporin regulation, Beta vulgaris, calcium, cytoplasmic acidification, plasma membrane, water channels


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