A Mutation of the Mitochondrial ABC Transporter Sta1 Leads to Dwarfism and Chlorosis in the Arabidopsis Mutant starik

Abstract

A mutation in the Arabidopsis gene STARIK leads to dwarfism and chlorosis of plants with an altered morphology of leaf and cell nuclei. We show that the STARIK gene encodes the mitochondrial ABC transporter Sta1 that belongs to a subfamily of Arabidopsis half-ABC transporters. The severity of the starik phenotype is suppressed by the ectopic expression of the STA2 homolog; thus, Sta1 function is partially redundant. Sta1 supports the maturation of cytosolic Fe/S protein in ⌬ atm1 yeast, substituting for the ABC transporter Atm1p. Similar to Atm1p-deficient yeast, mitochondria of the starik mutant accumulated more nonheme, nonprotein iron than did wild-type organelles. We further show that plant mitochondria contain a putative L -cysteine desulfurase. Taken together, our results suggest that plant mitochondria possess an evolutionarily conserved Fe/S cluster biosynthesis pathway, which is linked to the intracellular iron homeostasis by the function of Atm1p-like ABC transporters. INTRODUCTIONABC transporters constitute one of the largest protein families with diverse functions in membrane transport. The designation of ABC transporter recognizes a highly conserved ATP binding cassette, which is the most characteristic feature of this superfamily. These proteins mediate the relatively specific, active transmembrane transport of molecules that can range in size from small ions to proteins (reviewed in Higgins, 1992) and utilize the energy of ATP hydrolysis to pump substrates across membranes, usually against a concentration gradient. The typical ABC transporter consists of four domains. Two of these domains are hydrophobic, and each comprises six membrane-spanning segments. The transmembrane domains are believed to form a channel and to determine the specificity of the transporter. The other two domains are located at the periphery of the membrane and couple ATP hydrolysis to the transport process.The ABC transporter Atm1p of budding yeast mitochondria represents a "half-transporter" in which one transmembrane and one ATP binding domain are expressed in a single polypeptide (Leighton and Schatz, 1995). Atm1p is localized in the mitochondrial inner membrane and is believed to function as an exporter, because its ABC domains face the mitochondrial matrix. The ATM1 loss-of-function results in respiration-deficient mitochondria that lack cytochromes (Leighton and Schatz, 1995; Kispal et al., 1997) and that tend to loose their DNA (Leighton and Schatz, 1995). These pleiotropic effects of the Atm1p deficiency are generally attributed to the fact that in ⌬ atm1 cells, mitochondria accumulate up to 30-fold higher levels of iron than do wild-type organelles (Kispal et al., 1997;Mitsuhashi et al., 2000). The Atm1p transport function appears to be conserved in eukaryotes, and the human mitochondrial ABC transporters Abc7 and MTABC3 have been shown to be true functional orthologs of the Atm1p (Csere et al., 1998;Mitsuhashi et al., 2000). The human ABC7 gene has been implicated in hereditary X-linked sideroblastic anemia and a...

Mitochondrial Reactive Oxygen Species. Contribution to Oxidative Stress and Interorganellar Signaling

“…This phenomenon has been studied in yeast, animal cell cultures, and plants (for review, see Butow and Avadhani, 2004;Rhoads and Vanlerberghe, 2004). There are several interesting examples in which nuclear gene expression was altered in plants by mitochondrial dysfunction caused by nuclear mutation or transgenic expression of mitochondrial proteins (Kushnir et al, 2001;Gó mez-Casati et al, 2002;Rhoads et al, 2005). Although not directly demonstrated in these examples, there is evidence for the importance of mtROS in plant MRR.…”

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“…However, for consistency with previous publications, we have adhered to the ATM gene symbols in this paper.) Expression of GFP fusions showed that all three ATM proteins localized to mitochondria (Kushnir et al, 2001;Chen et al, 2007). Arabidopsis ATM3 could functionally complement the yeast atm1 phenotype (Kushnir et al, 2001;Chen et al, 2007), whereas Arabidopsis ATM1 complemented poorly and ATM2 expression was toxic in yeast (Chen et al, 2007).…”

“…Plant cytosol contains homologs of the cytosolic Fe-S assembly proteins that have recently been identified in yeast (Lill and Mü hlenhoff, 2008), including the scaffold protein AtNBP35 (Bych et al, 2008;Kohbushi et al, 2009) and the hydrogenase-like AtNAR1 (Cavazza et al, 2008). It is thought that cytosolic Fe-S cluster assembly is dependent on at least one of the organelles, because the Cys desulfurases that generate sulfur for Fe-S clusters, CpNifS and NFS1, are strictly localized in the plastids and mitochondria, respectively (Kushnir et al, 2001;Frazzon et al, 2007;Van Hoewyk et al, 2007).…”

“…The genes were first identified in Arabidopsis by Kushnir et al (2001) and were named STA2, STA3, and STA1, respectively. (A proposal for a unified nomenclature [Verrier et al, 2008] has suggested the gene symbols AtABCB24, AtABCB23, and AtABCB25 for AtATM1, AtATM2, and AtATM3, respectively.…”