Arabidopsis calcium-binding mitochondrial carrier proteins as potential facilitators of mitochondrial ATP-import and plastid SAM-import

Abstract

Edited by Michael R. SussmanKeywords: Chloroplast Mitochondria Mitochondrial carrier protein Calcium-binding ATP-phosphate carrier SAM transporter a b s t r a c t Chloroplasts and mitochondria are central to crucial cellular processes in plants and contribute to a whole range of metabolic pathways. The use of calcium ions as a secondary messenger in and around organelles is increasingly appreciated as an important mediator of plant cell signaling, enabling plants to develop or to acclimatize to changing environmental conditions. Here, we have studied the four calcium-dependent mitochondrial carriers that are encoded in the Arabidopsis genome. An unknown substrate carrier, which was previously found to localize to chloroplasts, is proposed to present a calcium-dependent S-adenosyl methionine carrier. For three predicted ATP/ phosphate carriers, we present experimental evidence that they can function as mitochondrial ATP-importers.

Functional characterization and organ distribution of three mitochondrial ATP–Mg/Pi carriers in Arabidopsis thaliana

“…Binding of radioactive Ca 2+ to AtAPC1, AtAPC2 and AtAPC3 has already been demonstrated [23]. Here the effect of Ca 2+ and of the divalent ion chelators EGTA and EDTA in de-ionized ultrapure water on the transport rates of AtAPC1, AtAPC2 and AtAPC3 was investigated (Fig.…”

“…The Arabidopsis proteins AtAPC1, AtAPC2 and AtAPC3 (encoded by At5g61810, At5g51050 and At5g07320, respectively) share the highest sequence identity with the human APCs and, as their human counterparts, contain Ca 2+ -binding EF hands in their N-terminal domains [11,23]. APC2 is the closest human homologue of AtAPC1, AtAPC2 and AtAPC3 with 39%, 38% and 38% overall identical residues, respectively (Supplementary Table S1).…”

“…In A. thaliana three APCs have been predicted on the basis of sequence similarity [11], mitochondrial localization and ability to partly complement the growth defect of the yeast Sal1 (APC) null mutant [23]. However, these three proteins have not been functionally characterized hitherto.…”

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

“…This also includes amino acid and nitrogen metabolism, for example, at the level of nitrate reductase (NR) activity or amino acids fueling the citric acid cycle. Such conditions could even lead to ATP import by mitochondria, mediated by Ca 2+ -regulated importers (Stael et al, 2011). Following the submergence-induced hypoxia, the subsequent exposure to oxygen during reoxygenation produces a burst of ROS.…”

The EF-Hand Ca2+ Binding Protein MICU Choreographs Mitochondrial Ca2+ Dynamics in Arabidopsis

“…In mammals, mitochondrial Ca 2+ can modulate the activity of different tricarboxylic acid cycle dehydrogenases, coupling overall mitochondrial energy output to demand or trigger apoptosis in extreme cases (Griffiths and Rutter, 2009). In plants, Ca 2+ binding EF-hand proteins, including a glutamate dehydrogenase, a family of MCF ATP/P i transporters (APC1-3), and two alternative NAD(P)H dehydrogenases (NDB1 and NDB2), localize to mitochondria and show Ca 2+ -dependent activity (although the latter are regulated by Ca 2+ from the intermembrane space side of the inner mitochondrial membrane; Møller et al, 1981;Rasmusson and Møller, 1991;Turano et al, 1997;Geisler et al, 2007;Stael et al, 2011;Monné et al, 2015). Furthermore, the EF-hand protein LETM1 and the calmodulin-like protein CML30 have recently been found to be localized in mitochondria, and additional proteins with Ca 2+ binding motifs have been detected in proteomic data sets of plant mitochondria (Chigri et al, 2012;Zhang et al, 2012;Salvato et al, 2014).…”