Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin

Nicola Tomasi; Tobias Kretzschmar; Luca Espen; Laure Weisskopf; Anja Thoe Fuglsang; Michael Palmgren; Günter Neumann; Zeno Varanini; Roberto Pinton; Enrico Martinoia; Stefano Cesco

doi:10.1111/j.1365-3040.2009.01938.x

Plasma membrane H⁺-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin

Nicola Tomasi, Tobias Kretzschmar, Luca Espen, Laure Weisskopf, Anja Thoe Fuglsang, Michael Palmgren, Günter Neumann, Zeno Varanini, Roberto Pinton, Enrico Martinoia, Stefano Cesco

80 Citations (Scopus)

Abstract

ABSTRACT

White lupin (Lupinus albus L.) is able to grow on soils with

sparingly available phosphate (P) by producing specialized

structures called cluster roots.To mobilize sparingly soluble

P forms in soils, cluster roots release substantial amounts of

carboxylates and concomitantly acidify the rhizosphere.The

relationship between acidification and carboxylate exudation

is still largely unknown. In the present work,we studied

the linkage between organic acids (malate and citrate) and

proton exudations in cluster roots of P-deficient white lupin.

After the illumination started, citrate exudation increased

transiently and reached a maximum after 5 h. This effect

was accompanied by a strong acidification of the external

medium and alkalinization of the cytosol, as evidenced by in

vivo nuclear magnetic resonance (NMR) analysis. Fusicoccin,

nuclear magnetic resonance (NMR) analysis. Fusicoccin,an activator of the plasmamembrane (PM)H+-ATPase,

stimulated citrate exudation, whereas vanadate, an inhibitor

of the H+-ATPase, reduced citrate exudation. The burst of

citrate exudation was associated with an increase in expression

of theLHA1PMH+-ATPase gene,an increased amount

of H+-ATPase protein, a shift in pH optimum of the enzymeand post-translational modification of an H

++-ATPase

protein involving binding of activating 14-3-3 protein.Taken

together, our results indicate a close link in cluster roots of

P-deficient white lupin between the burst of citrate exudation

and PM H+-ATPase-catalysed proton efflux.

Original language	English
Journal	Plant, Cell and Environment
Volume	32
Issue number	5
Pages (from-to)	465-475
Number of pages	11
ISSN	0140-7791
DOIs	https://doi.org/10.1111/j.1365-3040.2009.01938.x
Publication status	Published - 2009

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@article{a27347a0d2ae11dea1f3000ea68e967b,

title = "Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin",

abstract = "ABSTRACTWhite lupin (Lupinus albus L.) is able to grow on soils withsparingly available phosphate (P) by producing specializedstructures called cluster roots.To mobilize sparingly solubleP forms in soils, cluster roots release substantial amounts ofcarboxylates and concomitantly acidify the rhizosphere.Therelationship between acidification and carboxylate exudationis still largely unknown. In the present work,we studiedthe linkage between organic acids (malate and citrate) andproton exudations in cluster roots of P-deficient white lupin.After the illumination started, citrate exudation increasedtransiently and reached a maximum after 5 h. This effectwas accompanied by a strong acidification of the externalmedium and alkalinization of the cytosol, as evidenced by in vivo nuclear magnetic resonance (NMR) analysis. Fusicoccin,nuclear magnetic resonance (NMR) analysis. Fusicoccin,an activator of the plasmamembrane (PM)H+-ATPase, stimulated citrate exudation, whereas vanadate, an inhibitorof the H+-ATPase, reduced citrate exudation. The burst of citrate exudation was associated with an increase in expressionof theLHA1PMH+-ATPase gene,an increased amount of H+-ATPase protein, a shift in pH optimum of the enzymeand post-translational modification of an H++-ATPase protein involving binding of activating 14-3-3 protein.Takentogether, our results indicate a close link in cluster roots ofP-deficient white lupin between the burst of citrate exudationand PM H+-ATPase-catalysed proton efflux.",

author = "Nicola Tomasi and Tobias Kretzschmar and Luca Espen and Laure Weisskopf and Fuglsang, {Anja Thoe} and Michael Palmgren and G{\"u}nter Neumann and Zeno Varanini and Roberto Pinton and Enrico Martinoia and Stefano Cesco",

year = "2009",

doi = "10.1111/j.1365-3040.2009.01938.x",

language = "English",

volume = "32",

pages = "465--475",

journal = "Plant, Cell and Environment",

issn = "0140-7791",

publisher = "Wiley-Blackwell",

number = "5",

}

TY - JOUR

T1 - Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin

AU - Tomasi, Nicola

AU - Kretzschmar, Tobias

AU - Espen, Luca

AU - Weisskopf, Laure

AU - Fuglsang, Anja Thoe

AU - Palmgren, Michael

AU - Neumann, Günter

AU - Varanini, Zeno

AU - Pinton, Roberto

AU - Martinoia, Enrico

AU - Cesco, Stefano

PY - 2009

Y1 - 2009

N2 - ABSTRACTWhite lupin (Lupinus albus L.) is able to grow on soils withsparingly available phosphate (P) by producing specializedstructures called cluster roots.To mobilize sparingly solubleP forms in soils, cluster roots release substantial amounts ofcarboxylates and concomitantly acidify the rhizosphere.Therelationship between acidification and carboxylate exudationis still largely unknown. In the present work,we studiedthe linkage between organic acids (malate and citrate) andproton exudations in cluster roots of P-deficient white lupin.After the illumination started, citrate exudation increasedtransiently and reached a maximum after 5 h. This effectwas accompanied by a strong acidification of the externalmedium and alkalinization of the cytosol, as evidenced by in vivo nuclear magnetic resonance (NMR) analysis. Fusicoccin,nuclear magnetic resonance (NMR) analysis. Fusicoccin,an activator of the plasmamembrane (PM)H+-ATPase, stimulated citrate exudation, whereas vanadate, an inhibitorof the H+-ATPase, reduced citrate exudation. The burst of citrate exudation was associated with an increase in expressionof theLHA1PMH+-ATPase gene,an increased amount of H+-ATPase protein, a shift in pH optimum of the enzymeand post-translational modification of an H++-ATPase protein involving binding of activating 14-3-3 protein.Takentogether, our results indicate a close link in cluster roots ofP-deficient white lupin between the burst of citrate exudationand PM H+-ATPase-catalysed proton efflux.

AB - ABSTRACTWhite lupin (Lupinus albus L.) is able to grow on soils withsparingly available phosphate (P) by producing specializedstructures called cluster roots.To mobilize sparingly solubleP forms in soils, cluster roots release substantial amounts ofcarboxylates and concomitantly acidify the rhizosphere.Therelationship between acidification and carboxylate exudationis still largely unknown. In the present work,we studiedthe linkage between organic acids (malate and citrate) andproton exudations in cluster roots of P-deficient white lupin.After the illumination started, citrate exudation increasedtransiently and reached a maximum after 5 h. This effectwas accompanied by a strong acidification of the externalmedium and alkalinization of the cytosol, as evidenced by in vivo nuclear magnetic resonance (NMR) analysis. Fusicoccin,nuclear magnetic resonance (NMR) analysis. Fusicoccin,an activator of the plasmamembrane (PM)H+-ATPase, stimulated citrate exudation, whereas vanadate, an inhibitorof the H+-ATPase, reduced citrate exudation. The burst of citrate exudation was associated with an increase in expressionof theLHA1PMH+-ATPase gene,an increased amount of H+-ATPase protein, a shift in pH optimum of the enzymeand post-translational modification of an H++-ATPase protein involving binding of activating 14-3-3 protein.Takentogether, our results indicate a close link in cluster roots ofP-deficient white lupin between the burst of citrate exudationand PM H+-ATPase-catalysed proton efflux.

U2 - 10.1111/j.1365-3040.2009.01938.x

DO - 10.1111/j.1365-3040.2009.01938.x

M3 - Journal article

C2 - 19183296

SN - 0140-7791

VL - 32

SP - 465

EP - 475

JO - Plant, Cell and Environment

JF - Plant, Cell and Environment

IS - 5

ER -

Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin

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Plasma membrane H⁺-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin