Dataset Information

Inter-generational nuclear crosstalk links the control of gene expression to programmed genome rearrangement during the Paramecium sexual cycle.

ABSTRACT: Multinucleate cells are found in many eukaryotes, but how multiple nuclei coordinate their functions is still poorly understood. In the cytoplasm of the ciliate Paramecium tetraurelia, two micronuclei (MIC) serving sexual reproduction coexist with a somatic macronucleus (MAC) dedicated to gene expression. During sexual processes, the MAC is progressively destroyed while still ensuring transcription, and new MACs develop from copies of the zygotic MIC. Several gene clusters are successively induced and switched off before vegetative growth resumes. Concomitantly, programmed genome rearrangement (PGR) removes transposons and their relics from the new MACs. Development of the new MACs is controlled by the old MAC, since the latter expresses genes involved in PGR, including the PGM gene encoding the essential PiggyMac endonuclease that cleaves the ends of eliminated sequences. Using RNA deep sequencing and transcriptome analysis, we show that impairing PGR upregulates key known PGR genes, together with ∼600 other genes possibly also involved in PGR. Among these genes, 42% are no longer induced when no new MACs are formed, including 180 genes that are co-expressed with PGM under all tested conditions. We propose that bi-directional crosstalk between the two coexisting generations of MACs links gene expression to the progression of MAC development.

SUBMITTER: Bazin-Gelis M

PROVIDER: S-EPMC10711438 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Inter-generational nuclear crosstalk links the control of gene expression to programmed genome rearrangement during the Paramecium sexual cycle.

Bazin-Gélis Mélanie M Eleftheriou Evangelia E Zangarelli Coralie C Lelandais Gaëlle G Sperling Linda L Arnaiz Olivier O Bétermier Mireille M

Nucleic acids research 20231201 22

Multinucleate cells are found in many eukaryotes, but how multiple nuclei coordinate their functions is still poorly understood. In the cytoplasm of the ciliate Paramecium tetraurelia, two micronuclei (MIC) serving sexual reproduction coexist with a somatic macronucleus (MAC) dedicated to gene expression. During sexual processes, the MAC is progressively destroyed while still ensuring transcription, and new MACs develop from copies of the zygotic MIC. Several gene clusters are successively induc ...[more]

PMID: 37953377

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Project description:Longitudinal studies focusing on lifetime reproductive success (LRS) have been used to measure individual breeding performance and identify commonalities among successful breeders. By extending the focus to subsequent generations we identify a proportion of high-quality individuals that contribute disproportionately to the population over multiple generations. We used 23 years of yellow-eyed penguin (Megadyptes antipodes) breeding data from one breeding area to identify the proportion of individual birds that raised successful breeders, which in turn raised offspring. We explored which life-history components influenced LRS, as this knowledge would enable conservation resources to be focused on high-performing individuals in this endangered population. From 2,147 birds marked as chicks, 370 (17.2%) survived to adulthood and recruited to their natal location, of which 219 (10.2%) fledged offspring: 124 (56.6%) of the 219 birds produced offspring that recruited as breeders. Only 102 birds (4.8% of 2,147) fledged first-generation offspring that in turn fledged offspring (second-generation offspring, or grand-offspring). We found that ∼25% of the birds that survived to breed had above-average LRS as well as above-average numbers of grand-offspring, and were more likely to have produced first-generation chicks that recruited and also produced above-average numbers of second-generation chicks. Our findings suggest that there is a core of "super-breeders" that contribute disproportionately to the population over successive generations. Lifespan and age-at-first-breeding were correlated with LRS. We suggest that traits of birds relating to longevity, health (e.g., immunocompetence) and fitness could be examined to identify potential links with high LRS and inter-generational fecundity. "Super-breeders" appear to consistently achieve high LRS and long lifespans in a stochastic environment, demonstrating greater resilience in the face of extreme events.

Dataset Information

Inter-generational nuclear crosstalk links the control of gene expression to programmed genome rearrangement during the Paramecium sexual cycle.

Publications

Inter-generational nuclear crosstalk links the control of gene expression to programmed genome rearrangement during the Paramecium sexual cycle.

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