Joint inhibition of mitochondrial complex IV and alternative oxidase by genetic or chemical means represses chloroplast transcription in Arabidopsis

Abstract

Changes in the functional state of mitochondria have profound effects on other cellular compartments. Genome-wide expression analysis of Arabidopsis rps10 mutants with an RNAi-silenced expression of mitoribosomal S10 protein has revealed extensive transcriptional reprogramming. A meta-analysis comparing expression datasets of 25 mitochondrial perturbations showed a high similarity of the aox1a:rpoTmp mutant , which is defective in the alternative oxidase (AOX1a) and dual-targeted mitochondrial and plastid RNA polymerase (RPOTmp), to rps10 . Both rps10 and aox1a:rpoTmp showed a significantly decreased electron flux through both the cytochrome and the alternative respiratory pathways, and a markedly decreased the expression of nuclear-encoded components of the chloroplast transcription machinery. In line with this, a decreased level of plastid transcripts was observed in rps10 and aox1a:rpoTmp , which was reflected in a reduced rate of chloroplast transcription. Chemical treatment of wild-type seedlings with respiratory inhibitors showed that only simultaneous and direct inhibition of complex IV and AOX activity decreased the level of plastid transcripts. Taken together, both chemical and genetic studies show that the limitation of the activity of two mitochondrial terminal oxidases, complex IV and AOX, negatively impacts chloroplast transcription. Salicylic acid and oxygen are discussed as putative mediators of the signalling pathway between mitochondria, nucleus and chloroplasts. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

Mitochondrial ATP Synthase Subunit d, a Component of the Peripheral Stalk, is Essential for Growth and Heat Stress Tolerance inArabidopsis thaliana

“…Primers of MGE1, ATPd, ATPδ, ATPβ and sHSP23.6 were designed with Primer Premier 5 program. Primers of OM66, ANAC013, SOT12, AOX1a, AOX1b, AOX1c, UPOX1, NBD4, sHSP23.5 and ACT were previously described (Clifton et al , 2005; Geisler et al , 2012; Kerchev et al , 2014; Zhang et al , 2014; Wu et al , 2019; Adamowicz-Skrzypkowska et al , 2020). qRT-PCR was performed with 2 × RealStar Green Power Mixture (gene star) in a QuantStudio 3 Real-Time PCR System (Applied Biosystems).…”

Degradation of mitochondrial alternative oxidase in the appendices of Arum maculatum

“…Mitochondrial retrograde regulation was first reported in Saccharomyces cerevisiae in which it was shown that perturbed respiratory function activates a retrograde pathway that regulates gene expression and thereby alters cellular metabolism [61]. The AOX genes represent the pre-eminent example of this system in plants [29,36,37,41]. In A. thaliana, the transcription of AtAOX1a has been shown to be strongly negatively regulated by ABI4 [38], but to be inducible by latent transcriptional factors including NAC17 [62,63].…”

“…AOX has also been shown to be regulated in a retrograde manner [30][31][32][33][34][35][36][37]. For instance, the transcription factor ABI4 acts as a repressor of AOX1a, which is depressed under rotenone treatment [38,39].…”

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

“…ANAC017 loss-of-function mutants showed increased susceptibility when grown on UPR mt -inducing media, while ANAC017 overexpression lines were more resistant. Another study in this issue performed whole-genome transcriptome studies on knock-down lines of another Arabidopsis mitochondrial ribosomal protein, RPS10 [175], which is also interesting as a model for UPR mt in plants. Here, the ANAC017 regulon was strongly induced, and the analysis showed that the only common differentially regulated genes between doxycycline treatment, mrpl1 and rps10 mutants were well-known AA-induced ANAC017 target genes (e.g.…”

“…ANAC017 loss-of-function mutants showed increased susceptibility when grown on UPR mt -inducing media, while ANAC017 overexpression lines were more resistant. Another study in this issue performed whole-genome transcriptome studies on knock-down lines of another Arabidopsis mitochondrial ribosomal protein, RPS10 [175], which is also interesting as a model for UPR mt in plants.…”