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Functional interaction between the RNA exosome and the sirtuin deacetylase Hst3 maintains transcriptional homeostasis.

ABSTRACT: Eukaryotic cells maintain an optimal level of mRNAs through unknown mechanisms that balance RNA synthesis and degradation. We found that inactivation of the RNA exosome leads to global reduction of nascent mRNA transcripts, and that this defect is accentuated by loss of deposition of histone variant H2A.Z. We identify the mRNA for the sirtuin deacetylase Hst3 as a key target for the RNA exosome that mediates communication between RNA degradation and transcription machineries. These findings reveal how the RNA exosome and H2A.Z function together to control a deacetylase, ensuring proper levels of transcription in response to changes in RNA degradation.

SUBMITTER: Bryll AR

PROVIDER: S-EPMC8763048 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:In chloroplasts, homeostasis of the proteome maintained by protein synthesis, importation, and degradation is critical to the development of chloroplasts. The caseinolytic protease complex component CLPC1, a member of the HSP100 family of chaperones, not only facilitates the translocation of pre-proteins into chloroplasts, but also mediates protein degradation via its associated caseinolytic protease complex (CLPPs). Although CLPC1 has been shown to affect the abundance of some chloroplast proteins, its overall functions and coordination with other protease systems in maintaining proteome homeostasis have not been fully elucidated. Its possible roles in gene expression are also unclear. Here we used the iTRAQ technique to profile the chloroplast proteomes of the clpc1 mutant and its various complementation lines. Whereas proteins involved in photosynthesis were found to be dramatically decreased in the clcp1 mutant, many involved in chloroplast transcription and translation were increased. Expression of the full-length CLPC1 protein, but not of the N-terminal truncated form (ΔN), in clpc1 restored the level of most of these proteins to that of the wild type. Interestingly, the ΔN complementation line could also restore certain proteins to the wild type level. We found that nearly half of previously suggested candidate substrates of the CLPS1, another CLPP component, were mis-regulated in clpc1, indicating that CLPC1 greatly affects CLPS1 targets. We provide the first experimental evidence to show that CLPC1 profoundly affects gene transcription in chloroplasts. Sense transcripts of many chloroplast genes are up-regulated whereas antisense transcripts down-regulated in the clpc1 mutant. We propose that this altered transcript landscape is a result of the transcription and degradation dynamics conditioned by the changed proteomic profile in the mutant. Our study reveals that CLPC1 and likely the CLPP proteasome complex have a greater than previously recognized role in coordinating and maintaining the proteome and transcriptome homeostasis in chloroplasts.

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Functional interaction between the RNA exosome and the sirtuin deacetylase Hst3 maintains transcriptional homeostasis.

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