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Plant and Cell Physiology Advance Access originally published online on May 29, 2008
Plant and Cell Physiology 2008 49(7):1039-1055; doi:10.1093/pcp/pcn082
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© The Author 2008. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Plant Inner Membrane Anion Channel (PIMAC) Function in Plant Mitochondria

Maura Nicoletta Laus1,2, Mario Soccio1,2, Daniela Trono3, Luigi Cattivelli3 and Donato Pastore1,2,*

1 Dipartimento di Scienze Agro-ambientali, Chimica e Difesa Vegetale, Facoltà di Agraria, Università degli Studi di Foggia, Via Napoli, 25, 71100 Foggia, Italy
2 Centro di Ricerca Interdipartimentale BIOAGROMED, Università degli Studi di Foggia, Via Napoli, 52, 71100 Foggia, Italy
3 CRA-Centro di Ricerca per la Cerealicoltura, S.S. 16, Km 675, 71100 Foggia, Italy

*Corresponding author: E-mail, d.pastore{at}unifg.it; Fax, +39-0881589342.


  Abstract

To date, the existence of the plant inner membrane anion channel (PIMAC) has been shown only in potato mitochondria, but its physiological role remains unclear. In this study, by means of swelling experiments in K+ and ammonium salts, we characterize a PIMAC-like anion-conducting pathway in mitochondria from durum wheat (DWM), a monocotyledonous species phylogenetically far from potato. DWM were investigated since they possess a very active potassium channel (PmitoKATP), so implying a very active matching anion uniport pathway and, possibly, a coordinated function. As in potato mitochondria, the electrophoretic uptake of chloride and succinate was inhibited by matrix [H+], propranolol, and tributyltin, and was insensitive to Mg2+, N,N'-dicyclohexylcarbodiimide (DCCD) and mercurials, thus showing PIMAC's existence in DWM. PIMAC actively transports dicarboxylates, oxodicarboxylates, tricarboxylates and Pi. Interestingly, a novel mechanism of swelling in ammonium salts of isolated plant mitochondria is reported, based on electrophoretic anion uptake via PIMAC and ammonium uniport via PmitoKATP. PIMAC is inhibited by physiological compounds, such as ATP and free fatty acids, by high electrical membrane potential ({Delta}{Psi}), but not by acyl-CoAs or reactive oxygen species. PIMAC was found to cooperate with dicarboxylate carrier by allowing succinate uptake that triggers succinate/malate exchange in isolated DWM. Similar results were obtained using mitochondria from the dicotyledonous species topinambur, so suggesting generalization of results. We propose that PIMAC is normally inactive in vivo due to ATP and {Delta}{Psi} inhibition, but activation may occur in mitochondria de-energized by PmitoKATP (or other dissipative systems) to replace or integrate the operation of classical anion carriers.

Keywords: Anion transport - Durum wheat mitochondria - Inner membrane anion channel - Jerusalem artichoke mitochondria - Potassium channel

Abbreviations: {Delta}{Psi}, electrical membrane potential; BSA, bovine serum albumin; DCCD, N,N'-dicyclohexylcarbodiimide; DWM, durum wheat mitochondria; FCCP, carbonyl cyanide p-trifluoromethoxyphenylhydrazone; FFAs, free fatty acids; IMAC, inner membrane anion channel; JAM, Jerusalem artichoke mitochondria; LA, linoleic acid; MDS, malate detecting system; NEM, N-ethylmaleimide; O2·–, superoxide anion; PIMAC, plant inner membrane anion channel; PmitoKATP, ATP-sensitive plant mitochondrial potassium channel; PUCP, plant uncoupling protein; PVP, polyvinylpyrrolidone; ROS, reactive oxygen species; SHAM, salicylhydroxamate; TBT, tributyltin.

(Received April 30, 2008; Accepted May 23, 2008)
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