High V‐PPase activity is beneficial under high salt loads, but detrimental without salinity

Author:

Graus Dorothea1,Konrad Kai R.1,Bemm Felix2,Patir Nebioglu Meliha Görkem3,Lorey Christian1,Duscha Kerstin4,Güthoff Tilman1,Herrmann Johannes1,Ferjani Ali5,Cuin Tracey Ann6,Roelfsema M. Rob G.1,Schumacher Karin3,Neuhaus H. Ekkehard4,Marten Irene1,Hedrich Rainer1

Affiliation:

1. Institute for Molecular Plant Physiology and Biophysics University of Würzburg Julius von‐Sachs Platz 2 Würzburg D‐97082 Germany

2. Institute of Bioinformatics Center for Computational and Theoretical, Biology University of Würzburg Am Hubland Würzburg D‐97218 Germany

3. Centre for Organismal Studies Developmental Biology of Plants Ruprecht‐Karls‐University of Heidelberg Im Neuenheimer Feld 230 Heidelberg 69120 Germany

4. Plant Physiology University Kaiserslautern Postfach 3049 Kaiserslautern D‐67653 Germany

5. Department of Biology Tokyo Gakugei University Nukui Kitamachi 4‐1‐1 Koganei‐shi Tokyo 184‐8501 Japan

6. Tasmanian Institute of Agriculture University of Tasmania Hobart TAS 7001 Australia

Abstract

Summary The membrane‐bound proton‐pumping pyrophosphatase (V‐PPase), together with the V‐type H+‐ATPase, generates the proton motive force that drives vacuolar membrane solute transport. Transgenic plants constitutively overexpressing V‐PPases were shown to have improved salinity tolerance, but the relative impact of increasing PPi hydrolysis and proton‐pumping functions has yet to be dissected. For a better understanding of the molecular processes underlying V‐PPase‐dependent salt tolerance, we transiently overexpressed the pyrophosphate‐driven proton pump (NbVHP) in Nicotiana benthamiana leaves and studied its functional properties in relation to salt treatment by primarily using patch‐clamp, impalement electrodes and pH imaging. NbVHP overexpression led to higher vacuolar proton currents and vacuolar acidification. After 3 d in salt‐untreated conditions, V‐PPase‐overexpressing leaves showed a drop in photosynthetic capacity, plasma membrane depolarization and eventual leaf necrosis. Salt, however, rescued NbVHP‐hyperactive cells from cell death. Furthermore, a salt‐induced rise in V‐PPase but not of V‐ATPase pump currents was detected in nontransformed plants. The results indicate that under normal growth conditions, plants need to regulate the V‐PPase pump activity to avoid hyperactivity and its negative feedback on cell viability. Nonetheless, V‐PPase proton pump function becomes increasingly important under salt stress for generating the pH gradient necessary for vacuolar proton‐coupled Na+ sequestration.

Funder

Deutsche Forschungsgemeinschaft

Publisher

Wiley

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