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

Adamowicz-Skrzypkowska, Aleksandra ; Kwasniak-Owczarek, Malgorzata ; Van Aken, Olivier LU ; Kazmierczak, Urszula and Janska, Hanna (2020) In Philosophical Transactions of the Royal Society B: Biological Sciences 375(1801).
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... (More)

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’.

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author
organization
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type
Contribution to journal
publication status
published
subject
keywords
Alternative oxidase, Arabidopsis thaliana, Chloroplast transcription, Complex IV, Low oxygen signalling, NEP and PEP
in
Philosophical Transactions of the Royal Society B: Biological Sciences
volume
375
issue
1801
article number
20190409
publisher
Royal Society
external identifiers
  • pmid:32362248
  • scopus:85085122509
ISSN
0962-8436
DOI
10.1098/rstb.2019.0409
language
English
LU publication?
yes
id
a36e29d6-ae5a-459a-a62f-90269adfb904
date added to LUP
2020-06-12 13:09:18
date last changed
2020-07-08 05:17:04
@article{a36e29d6-ae5a-459a-a62f-90269adfb904,
  abstract     = {<p>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’.</p>},
  author       = {Adamowicz-Skrzypkowska, Aleksandra and Kwasniak-Owczarek, Malgorzata and Van Aken, Olivier and Kazmierczak, Urszula and Janska, Hanna},
  issn         = {0962-8436},
  language     = {eng},
  month        = {06},
  number       = {1801},
  publisher    = {Royal Society},
  series       = {Philosophical Transactions of the Royal Society B: Biological Sciences},
  title        = {Joint inhibition of mitochondrial complex IV and alternative oxidase by genetic or chemical means represses chloroplast transcription in Arabidopsis},
  url          = {http://dx.doi.org/10.1098/rstb.2019.0409},
  doi          = {10.1098/rstb.2019.0409},
  volume       = {375},
  year         = {2020},
}