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

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...

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Published inThe New phytologist Vol. 219; no. 4; pp. 1421 - 1432
Main Authors Graus, Dorothea, Konrad, Kai R., Bemm, Felix, Patir Nebioglu, Meliha Görkem, Lorey, Christian, Duscha, Kerstin, Güthoff, Tilman, Herrmann, Johannes, Ferjani, Ali, Cuin, Tracey Ann, Roelfsema, M. Rob G., Schumacher, Karin, Neuhaus, H. Ekkehard, Marten, Irene, Hedrich, Rainer
Format Journal Article
LanguageEnglish
Published England New Phytologist Trust 01.09.2018
Wiley Subscription Services, Inc
John Wiley and Sons Inc
Subjects
Acidification
Adenosine triphosphatase
Capacity
Cell death
Cell Death - drug effects
Cell Membrane - drug effects
Cell Membrane - metabolism
cell viability
Depolarization
Diphosphates - metabolism
electrodes
enzyme activity
functional properties
gene overexpression
Growth conditions
H-transporting ATP synthase
Hydrogen-Ion Concentration
hydrolysis
Hyperactivity
image analysis
Imaging techniques
Inorganic Pyrophosphatase - metabolism
Isoenzymes - metabolism
Leaves
Membrane potential
Membrane Potentials - drug effects
Mesophyll Cells - drug effects
Mesophyll Cells - enzymology
Necrosis
Negative feedback
Nicotiana - drug effects
Nicotiana - enzymology
Nicotiana benthamiana
pH effects
Photosynthesis
Plant Epidermis - cytology
Plant Epidermis - drug effects
plasma membrane
plasma membrane voltage
proton pump
proton pump currents
Proton Pumps - metabolism
proton-motive force
Protonmotive force
Protons
Pumping
Pyrophosphatase
Salinity
Salinity effects
Salinity tolerance
salt
salt stress
Salt tolerance
sodium
Sodium Chloride - pharmacology
Solute transport
Solutes
Stress, Physiological - drug effects
Transgenic plants
vacuolar pH
Vacuolar Proton-Translocating ATPases - metabolism
vacuolar proton‐ATPase (V‐ATPase)
vacuolar proton‐pyrophosphatase (V‐PPase)
vacuoles
Vacuoles - enzymology
salt
vacuolar proton-pyrophosphatase (V-PPase)
cell death
vacuolar pH
vacuolar proton-ATPase (V-ATPase)
proton pump currents
plasma membrane voltage
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Abstract 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.
AbstractList 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.
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 PP i 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.
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.
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.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.
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.
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 PP 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.
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.
Author Kai R. Konrad
Tilman Güthoff
H. Ekkehard Neuhaus
Kerstin Duscha
Ali Ferjani
Karin Schumacher
M. Rob G. Roelfsema
Felix Bemm
Tracey Ann Cuin
Meliha Görkem Patir Nebioglu
Dorothea Graus
Christian Lorey
Johannes Herrmann
Irene Marten
Rainer Hedrich
AuthorAffiliation 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
6 Tasmanian Institute of Agriculture University of Tasmania Hobart TAS 7001 Australia
4 Plant Physiology University Kaiserslautern Postfach 3049 Kaiserslautern D‐67653 Germany
3 Centre for Organismal Studies Developmental Biology of Plants Ruprecht‐Karls‐University of Heidelberg Im Neuenheimer Feld 230 Heidelberg 69120 Germany
5 Department of Biology Tokyo Gakugei University Nukui Kitamachi 4‐1‐1 Koganei‐shi Tokyo 184‐8501 Japan
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– name: 1 Institute for Molecular Plant Physiology and Biophysics University of Würzburg Julius von‐Sachs Platz 2 Würzburg D‐97082 Germany
– name: 5 Department of Biology Tokyo Gakugei University Nukui Kitamachi 4‐1‐1 Koganei‐shi Tokyo 184‐8501 Japan
– name: 3 Centre for Organismal Studies Developmental Biology of Plants Ruprecht‐Karls‐University of Heidelberg Im Neuenheimer Feld 230 Heidelberg 69120 Germany
– name: 6 Tasmanian Institute of Agriculture University of Tasmania Hobart TAS 7001 Australia
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  givenname: Christian
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  fullname: Duscha, Kerstin
  organization: Plant Physiology University Kaiserslautern Postfach 3049 Kaiserslautern D‐67653 Germany
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  surname: Güthoff
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  organization: Institute for Molecular Plant Physiology and Biophysics University of Würzburg Julius von‐Sachs Platz 2 Würzburg D‐97082 Germany
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  surname: Hedrich
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  organization: Institute for Molecular Plant Physiology and Biophysics University of Würzburg Julius von‐Sachs Platz 2 Würzburg D‐97082 Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29938800$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords salt
vacuolar proton-pyrophosphatase (V-PPase)
cell death
vacuolar pH
vacuolar proton-ATPase (V-ATPase)
proton pump currents
plasma membrane voltage
Language English
License Attribution
2018 The Authors. New Phytologist © 2018 New Phytologist Trust.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet The membrane-bound proton-pumping pyrophosphatase (V-PPase), together with the V-type H+-ATPase, generates the proton motive force that drives vacuolar...
Summary The membrane‐bound proton‐pumping pyrophosphatase (V‐PPase), together with the V‐type H+‐ATPase, generates the proton motive force that drives vacuolar...
The membrane‐bound proton‐pumping pyrophosphatase (V‐PPase), together with the V‐type H + ‐ATPase, generates the proton motive force that drives vacuolar...
The membrane-bound proton-pumping pyrophosphatase (V-PPase), together with the V-type H -ATPase, generates the proton motive force that drives vacuolar...
The membrane‐bound proton‐pumping pyrophosphatase (V‐PPase), together with the V‐type H+‐ATPase, generates the proton motive force that drives vacuolar...
The membrane-bound proton-pumping pyrophosphatase (V-PPase), together with the V-type H+ -ATPase, generates the proton motive force that drives vacuolar...
The membrane‐bound proton‐pumping pyrophosphatase (V‐PPase), together with the V‐type H⁺‐ATPase, generates the proton motive force that drives vacuolar...
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StartPage 1421
SubjectTerms Acidification
Adenosine triphosphatase
Capacity
Cell death
Cell Death - drug effects
Cell Membrane - drug effects
Cell Membrane - metabolism
cell viability
Depolarization
Diphosphates - metabolism
electrodes
enzyme activity
functional properties
gene overexpression
Growth conditions
H-transporting ATP synthase
Hydrogen-Ion Concentration
hydrolysis
Hyperactivity
image analysis
Imaging techniques
Inorganic Pyrophosphatase - metabolism
Isoenzymes - metabolism
Leaves
Membrane potential
Membrane Potentials - drug effects
Mesophyll Cells - drug effects
Mesophyll Cells - enzymology
Necrosis
Negative feedback
Nicotiana - drug effects
Nicotiana - enzymology
Nicotiana benthamiana
pH effects
Photosynthesis
Plant Epidermis - cytology
Plant Epidermis - drug effects
plasma membrane
plasma membrane voltage
proton pump
proton pump currents
Proton Pumps - metabolism
proton-motive force
Protonmotive force
Protons
Pumping
Pyrophosphatase
Salinity
Salinity effects
Salinity tolerance
salt
salt stress
Salt tolerance
sodium
Sodium Chloride - pharmacology
Solute transport
Solutes
Stress, Physiological - drug effects
Transgenic plants
vacuolar pH
Vacuolar Proton-Translocating ATPases - metabolism
vacuolar proton‐ATPase (V‐ATPase)
vacuolar proton‐pyrophosphatase (V‐PPase)
vacuoles
Vacuoles - enzymology
Title High V-PPase activity is beneficial under high salt loads, but detrimental without salinity
URI https://www.jstor.org/stable/90024014
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.15280
https://www.ncbi.nlm.nih.gov/pubmed/29938800
https://www.proquest.com/docview/2083599704
https://www.proquest.com/docview/2059050486
https://www.proquest.com/docview/2153621809
https://pubmed.ncbi.nlm.nih.gov/PMC6099232
Volume 219
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