The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine‐sulfinic acid reductase involved in the photooxidative stress response

Abstract

SummaryThe 2-cysteine peroxiredoxins (2-Cys-Prxs) are antioxidants that reduce peroxides through a thiol-based mechanism. During catalysis, these ubiquitous enzymes are occasionally inactivated by the substratedependent oxidation of the catalytic cysteine to the sulfinic acid (-SO 2 H) form, and are reactivated by reduction by sulfiredoxin (Srx), an enzyme recently identified in yeast and in mammal cells. In plants, 2-Cys-Prxs constitute the most abundant Prxs and are located in chloroplasts. Here we have characterized the unique Srx gene in Arabidopsis thaliana (AtSrx) from a functional point of view, and analyzed the phenotype of two AtSrx knockout (AtSrx-) mutant lines. AtSrx is a chloroplastic enzyme displaying sulfinic acid reductase activity, as shown by the ability of the recombinant AtSrx to reduce the overoxidized 2-Cys-Prx form in vitro, and by the accumulation of the overoxidized Prx in mutant lines lacking Srx in vivo. Furthermore, AtSrx mutants exhibit an increased tolerance to photooxidative stress generated by high light combined with low temperature. These data establish that, as in yeast and in mammals, plant 2-Cys-Prxs are subject to substrate-mediated inactivation reversed by Srx, and suggest that the 2-Cys-Prx redox status and sulfiredoxin are parts of a signaling mechanism participating in plant responses to oxidative stress.

Protein cysteine sulfinic acid reductase (sulfiredoxin) as a regulator of cell proliferation and drug response

“…Deletion of yeast Srx reduces the organism's tolerance to H 2 O 2 (Biteau et al, 2003;Bozonet et al, 2005;Vivancos et al, 2005;Demasi et al, 2006). Plant Srx (Arabidopsis thaliana Srx) is also involved in photo-oxidative stress response (Liu et al, 2006;Rey et al, 2007) and mammalian Srx can restore the peroxidase activity of peroxiredoxins (Chang et al, 2004;Jacob et al, 2004;Jonsson et al, 2005;Lee et al, 2005Lee et al, , 2006Woo et al, 2005;Jeong et al, 2006;Rhee et al, 2007). Invaluable information has been gained from structural data of Srx and its interacting partners (Jonsson et al, 2005;Lee et al, 2005Lee et al, , 2006Jonsson et al, 2008).…”

The Dual-Targeted Plant Sulfiredoxin Retroreduces the Sulfinic Form of Atypical Mitochondrial Peroxiredoxin

“…The dual localization of Srx in plants adds a new feature to Srx function and thus differs from the results reported by Liu et al (2006) and Rey et al (2007). The first group deduced, for several plant Srxs, using ChloroP and TargetP programs, that Srx contains an N-terminal chloroplast transit peptide.…”

“…Srx and its target 2-Cys Prx have been localized specifically in the chloroplast from Arabidopsis (Baier and Dietz, 1997; Liu et al, 2006;Rey et al, 2007). However, (1) the conditional mitochondrial localization in mammalia in response to oxidative stress (Noh et al, 2009) and (2) the high probability of dual targeting to chloroplast and mitochondrion in pea predicted by our bioinformatic analysis, stimulated us to investigate the intracellular localization of Srx from pea and Arabidopsis in detail.…”

“…AtSrx linked to GFP fusion protein was only studied in chloroplasts (Liu et al, 2006). Rey et al (2007) also studied the subcellular localization of AtSrx by GFP fusion, in a heterologous system, and concluded that Srx from Arabidopsis is exclusively localized in plastids discarding its presence in mitochondria. GFP with about 27 kD is quite large as compared to the preform of Srx with 14 kD.…”

“…Both proteins have been localized specifically within the chloroplast (Baier and Dietz, 1997;Liu et al, 2006;Rey et al, 2007) and a systematic biochemical characterization of plant Srx has been recently reported (Iglesias-Baena et al, 2010). Plant mitochondria only contain one type of Prx, Prx IIF (Finkemeier et al, 2005;Barranco-Medina et al, 2007;Gama et al, 2007), which belongs to the atypical type II Prx subfamily along with the human Prx V. Thus far, it has been considered that Srx reduces exclusively the sulfinic form of typical 2-Cys Prx (Woo et al, 2005) and there is no reference involving Srx in the reduction of an atypical 2-Cys Prx-SO 2 H.…”