Abstract
Plant mitochondria signal to the nucleus leading to altered transcription of nuclear genes by a process called mitochondrial retrograde regulation (MRR). MRR is implicated in metabolic homeostasis and responses to stress conditions. Mitochondrial reactive oxygen species (mtROS) are a MRR signaling component, but whether all MRR requires ROS is not established. Inhibition of the cytochrome respiratory pathway by antimycin A (AA) or the TCA cycle by monofluoroacetate (MFA), each of which initiates MRR, can increase ROS production in some plant cells. We found that for AA and MFA applied to leaves of soil-grown Arabidopsis thaliana plants, ROS production increased with AA, but not with MFA, allowing comparison of transcript profiles under different ROS conditions during MRR. Variation in transcript accumulation over time for eight nuclear encoded mitochondrial protein genes suggested operation of both common and distinct signaling pathways between the two treatments. Consequences of mitochondrial perturbations for the whole transcriptome were examined by microarray analyses. Expression of 1316 and 606 genes was altered by AA and MFA, respectively. A subset of genes was similarly affected by both treatments, including genes encoding photosynthesis-related proteins. MFA treatment resulted in more down-regulation. Functional gene category (MapMan) and cluster analyses showed that genes with expression levels affected by perturbation from AA or MFA inhibition were most similarly affected by biotic stresses such as pathogens. Overall, the data provide further evidence for the presence of mtROS-independent MRR signaling, and support the proposed involvement of MRR and mitochondrial function in plant responses to biotic stress.
Highlights
Plant mitochondria and chloroplasts communicate with the cell nucleus to modify nuclear gene expression so that organelle and cell properties can be adjusted as metabolism and the environment change
The mitochondrial electron transport chain (mtETC) inhibitor antimycin A (AA) increased Reactive oxygen species (ROS) production by Arabidopsis leaves, but the TCA cycle inhibitor MFA had no detectable effect on ROS levels
Despite the clear difference in the observed ROS levels, both mitochondrial perturbations quickly resulted in increased NEMP gene expression, most likely to begin mitochondrial adjustments to the restrictions
Summary
Plant mitochondria and chloroplasts communicate with the cell nucleus to modify nuclear gene expression so that organelle and cell properties can be adjusted as metabolism and the environment change. This signaling is termed mitochondrial retrograde regulation (MRR) [1], [2]. In addition to mtROS, mitochondrial calcium has been identified as a likely MRR signaling component [10]. Whether mtROS, calcium and/or other molecules are necessary for all MRR, which nuclear genes are affected by MRR, and how much MRR contributes to the response of plants to environmental stresses are subjects of ongoing study
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