Defining the Mitochondrial Stress Response in Arabidopsis thaliana

Abstract

To obtain a global overview of how mitochondria respond to stress, we aimed to define the plant mitochondrial stress response (MSR). By combining a set of 1196 Arabidopsis thaliana genes that putatively encode mitochondrial proteins with 16 microarray experiments on stress-related conditions, 45 nuclear encoded genes were defined as widely stress-responsive. Using green fluorescent protein (GFP) fusion assays, the mitochondrial targeting of a large number of these proteins was tested, confirming in total 26 proteins as mitochondrially targeted. Several of these proteins were observed to be dual targeted to mitochondria and plastids, including the small heat shock proteins sHSP23.5 and sHSP23.6. In addition to the well defined stress components of mitochondria, such as alternative oxidases, nicotinamide adenine dinucleotide (NAD(P)H) dehydrogenases, and heat shock proteins, a variety of other proteins, many with unknown function, were identified. The mitochondrial carrier protein family was over-represented in the stress-responsive genes, suggesting that stress induces altered needs for metabolite transport across the mitochondrial inner membrane. Although the genes encoding many of these proteins contain common cis-acting regulatory elements, it was apparent that a number of distinct regulatory processes or signals likely triggered the MSR. Therefore, these genes provide new model systems to study mitochondrial retrograde regulation, in addition to the widely used alternative oxidase model. Additionally, as changes in proteins responsive to stress did not correlate well with changes at a transcript level, it suggests that post-transcriptional mechanisms also play an important role in defining the MSR.

Decreasing Electron Flux through the Cytochrome and/or Alternative Respiratory Pathways Triggers Common and Distinct Cellular Responses Dependent on Growth Conditions

“…Again, because this response is evident irrespective of whether the AOX or the cytochrome pathway is restricted, the overall mitochondrial respiratory capacity seems to play an integral role in signaling growth or defense. The concept of mitochondrial signaling has been proposed by a variety of groups (ArnholdtSchmitt et al, 2006;Clifton et al, 2006;Van Aken et al, 2009a, 2009bVanlerberghe et al, 2009). This study strongly implies that, under environmental stress and with restricted respiratory capacity, signals from mitochondria play an important role to constrain growth and activate stress responses.…”

“…Inhibition of the mitochondrial ATP synthase by oligomycin treatment resulted in transcript changes that overlapped with many of the changes usually seen in plants impaired in the electron transport chain (Geisler et al, 2012). Other meta-analyses of transcriptome changes upon perturbation of mitochondrial function have drawn similar conclusions from detecting widespread changes associated with ROS signaling (Van Aken et al, 2009a, 2009bUmbach et al, 2012;Van Aken and Whelan, 2012). Notably, although perturbation of mitochondrial function results in transcriptome changes affecting many cellular processes, its impact is significantly higher on genes encoding mitochondrial proteins (Van Aken and Whelan, 2012).…”

“…NAC013 is a marker for mitochondrial dysfunction (Schwarzländer et al, 2012), and it is induced by H 2 O 2 (Inzé et al, 2012). Evidence that this transcription factor is mediating a response can be seen by analyzing the transcript abundance of genes for mitochondrial proteins that have been previously defined as being responsive to stress (Van Aken et al, 2009a, 2009bVan Aken and Whelan, 2012). To a great extent, these transcripts were induced in aox1a:rpoTmp in standard growth conditions (Supplemental Table S5A).…”

How do plants make mitochondria?

“…Analysis of protein and transcript changes in response to individual stresses reveal that under any individual stress, there can be from tens to hundreds of changes (Clifton et al 2006;Van Aken et al 2009;Schwarzlander et al 2012;Tan et al 2012), but common changes in a number of stresses is relatively small. Apart from the components of the alternative respiratory chain (Clifton et al 2005), various components associated with protein import also appear to change under stress (Lister et al 2004).…”

“…It has become clear that mitochondria are not merely passive player(s) that respond to changes in the cellular environment, but rather that they can trigger these changes Van Aken et al 2009;Vanlerberghe et al 2009). While the concept of mitochondrial-to-nuclear signaling has been studied from the point of view of regulation of mitochondrial components, the identity of the molecular components that sense mitochondrial function and relay these signals to the nucleus remains unknown.…”