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The transcriptional signatures of Caenorhabditis elegans dauer larvae

ABSTRACT: Both plasticity and robustness are pervasive features of developmental programs. The dauer in Caenorhabditis elegans is an alternative to the third larval stage of the nematode and is an example of phenotypic plasticity. The dauer is an arrested, hypometabolic state that undergoes dramatic changes in gene expression compared to conspecifics that continue development, and can be induced by several adverse environments or genetic mutations that act as independent and parallel inputs into the larval developmental program. However, given the different genetic or environmental triggers that can induce dauer, gene expression in dauer larvae could be invariant or vary depending on the larvae’s route into dauer entry; this question has not been examined. Here we use RNA-sequencing to characterize gene expression in dauer larvae induced to arrest development in response to different stimuli. By assessing the variance in the expression levels of all genes and computing the Spearman's rank-order correlation of gene expression within several Gene Ontologies (GO) and gene networks, we find that the expression patterns of most genes, except for those that act in specific defense and metabolic pathways, are strongly correlated between the different dauer larvae, suggestive of transcriptional robustness. We speculate that the transcriptional robustness of core dauer pathways allows for the buffering of variation in the expression of genes involved in their response to the environment, allowing the different dauers to be better suited to survive in and exploit different niches.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE274872 | GEO | 2024/08/15

REPOSITORIES: GEO

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Project description:Many tissue-specific stem cells maintain the ability to produce multiple cell types during long periods of non-division, or quiescence. FOXO transcription factors promote quiescence and stem cell maintenance, but the mechanisms by which FOXO proteins promote multipotency during quiescence are still emerging. The single FOXO ortholog in C. elegans, daf-16, promotes entry into a quiescent and stress-resistant larval stage called dauer in response to adverse environmental cues. During dauer, stem and progenitor cells maintain or re-establish multipotency to allow normal development to resume after dauer. We find that during dauer, daf-16/FOXO prevents epidermal stem cells (seam cells) from prematurely adopting differentiated, adult characteristics. In particular, dauer larvae that lack daf-16 misexpress collagens that are normally adult-enriched. Using col-19p::gfp as an adult cell fate marker, we find that all major daf-16 isoforms contribute to opposing col-19p::gfp expression during dauer. By contrast, daf-16(0) larvae that undergo non-dauer development do not misexpress col-19p::gfp. Adult cell fate and the timing of col-19p::gfp expression are regulated by the heterochronic gene network, including lin-41 and lin-29. lin-41 encodes an RNA-binding protein orthologous to LIN41/TRIM71 in mammals, and lin-29 encodes a conserved zinc finger transcription factor. In non-dauer development lin-41 opposes adult cell fate by inhibiting the translation of lin-29, which directly activates col-19 transcription and promotes adult cell fate. We find that during dauer, lin-41 blocks col-19p::gfp expression, but surprisingly, lin-29 is not required in this context. Additionally, daf-16 promotes the expression of lin-41 in dauer larvae. The col-19p::gfp misexpression phenotype observed in dauer larvae with reduced daf-16 requires the downregulation of lin-41, but does not require lin-29. Taken together, this work demonstrates a novel role for daf-16/FOXO as a heterochronic gene that promotes expression of lin-41/TRIM71 to contribute to multipotent cell fate in a quiescent stem cell model.

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The transcriptional signatures of Caenorhabditis elegans dauer larvae

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