The impact of impaired mitochondrial function on retrograde signalling: a meta-analysis of transcriptomic responses

Abstract

Mitochondria occupy a central position in cellular metabolism. Their protein complement must therefore be dynamically adjusted to the metabolic demands of the cell. As >95% of mitochondrial proteins are encoded by nuclear DNA, regulation of the mitochondrial proteome requires signals that sense the status of the organelle and communicate it back to the nucleus. This is referred to as retrograde signalling. Mitochondria are tightly integrated into the network of cellular processes, and the output of mitochondrial retrograde signalling therefore not only feeds back to the mitochondrion, but also regulates functions across the cell. A number of transcriptomic studies have assessed the role of retrograde signalling in plants. However, single studies of a specific mitochondrial dysfunction may also measure secondary effects in addition to the specific transcriptomic output of mitochondrial signals. To gain an improved understanding of the output and role of mitochondrial retrograde signalling, a meta-analysis of 11 transcriptomic data sets from different models of plant mitochondrial dysfunction was performed. Comparing microarray data from stable mutants and short-term chemical treatments revealed unique features and commonalities in the responses that are under mitochondrial retrograde control. In particular, a common regulation of transcripts of the following functional categories was observed: plant-pathogen interactions, protein biosynthesis, and light reactions of photosynthesis. The possibility of a novel mode of interorganellar signalling, in which the mitochondrion influences processes in the plastid and other parts of the cell, is discussed.

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

“…A meta-analysis of 11 transcriptome signatures of different mitochondrial functions revealed common responses in genes for the functional categories of plant-pathogen interactions, light reactions of photosynthesis, and protein synthesis (Schwarzländer et al, 2012). However, it was also noticeable that distinct changes did occur depending on the target of the mutation or chemical inhibition (e.g.…”

FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis

“…The functional groups included Protein Synthesis and Protein Degradation, consistent with the observed induction of autophagy. Together with Photosynthesis and Photosynthetic Light Reactions, which were also significantly regulated, this functional group set was identified previously by meta-analysis of multiple transcriptomic data sets (Schwarzländer et al, 2012a) as being a general indicator for mitochondrial dysfunction. In addition to these classes, we also observed regulation of Abiotic Stress, Redox, and Tricarboxylic Acid Cycle ( Table I) that can be clearly linked to mitochondrial dysfunction.…”

“…friendly displays numerous indicators of stress, such as an increased number of dead root cells, increased number and size of acidic compartments, tentatively identified as autolysosomes, and the increased frequency of mitochondrial membrane potential pulses. Further evidence for friendly being affected by stress is displayed on the transcriptomic level, including significant regulation of functional gene groups previously identified as targets of mitochondrial dysfunction and oxidative stress (Schwarzländer et al, 2012a). Lack of the D. melanogaster FRIENDLY ortholog in the clu mutant also leads to mitochondrial oxidative stress as measured by strongly decreased aconitase activity (Sen et al, 2013).…”

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).…”