Dataset Information

Cell Non-autonomous Function of daf-18/PTEN in the Somatic Gonad Coordinates Somatic Gonad and Germline Development in C. elegans Dauer Larvae.

ABSTRACT: C. elegans larvae integrate environmental information and developmental decisions [1-3]. In favorable conditions, worms develop rapidly and continuously through four larval stages into reproductive adulthood. However, if conditions are unfavorable through the second larval stage, worms enter dauer diapause, a state of global and reversible developmental arrest in which precursor cells remain quiescent and preserve developmental potential, anticipating developmental progression if conditions improve. Signaling from neurons, hypodermis, and intestine regulate the appearance and behavior of dauer larvae and many aspects of developmental arrest of the non-gonadal soma [1, 4, 5]. Here, we show that the decision of somatic gonad blast cells (SGBs) and germline stem cells (GSCs) to be quiescent or progress developmentally is regulated differently from the non-gonadal soma: daf-18/PTEN acts non-autonomously within the somatic gonad to maintain developmental quiescence of both SGBs and GSCs. Our analysis suggests that daf-18 acts in somatic gonad cells to produce a "pro-quiescence" signal (or signals) that acts inter se and between the somatic gonad and the germline. The inferred signal does not require DAF-2/insulin receptor or maintain quiescence of the nearby sex myoblasts, and developmental progression in daf-18(0) does not require dafachronic acids. Abrogating quiescence in dauer results in post-dauer sterility. Our results implicate the somatic gonad as an endocrine organ to synchronize somatic gonad and germline development during dauer diapause and recovery, and our finding that PTEN acts non-autonomously to control blast cell quiescence may be relevant to its function as a tumor suppressor in mammals and to combating parasitic nematodes.

SUBMITTER: Tenen CC

PROVIDER: S-EPMC6486834 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Cell Non-autonomous Function of daf-18/PTEN in the Somatic Gonad Coordinates Somatic Gonad and Germline Development in C. elegans Dauer Larvae.

Tenen Claudia C CC Greenwald Iva I

Current biology : CB 20190228 6

C. elegans larvae integrate environmental information and developmental decisions [1-3]. In favorable conditions, worms develop rapidly and continuously through four larval stages into reproductive adulthood. However, if conditions are unfavorable through the second larval stage, worms enter dauer diapause, a state of global and reversible developmental arrest in which precursor cells remain quiescent and preserve developmental potential, anticipating developmental progression if conditions impr ...[more]

PMID: 30827916

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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.

Project description:BackgroundAscaris suum (large roundworm of pigs) is a parasitic nematode that causes substantial losses to the meat industry. This nematode is suitable for biochemical studies because, unlike C. elegans, homogeneous tissue samples can be obtained by dissection. It has large sperm, produced in great numbers that permit biochemical studies of sperm motility. Widespread study of A. suum would be facilitated by more comprehensive genome resources and, to this end, we have produced a gonad transcriptome of A. suum.ResultsTwo 454 pyrosequencing runs generated 572,982 and 588,651 reads for germline (TES) and somatic (VAS) tissues of the A. suum gonad, respectively. 86% of the high-quality (HQ) reads were assembled into 9,955 contigs and 69,791 HQ reads remained as singletons. 2.4 million bp of unique sequences were obtained with a coverage that reached 16.1-fold. 4,877 contigs and 14,339 singletons were annotated according to the C. elegans protein and the Kyoto Encyclopedia of Genes and Genomes (KEGG) protein databases. Comparison of TES and VAS transcriptomes demonstrated that genes participating in DNA replication, RNA transcription and ubiquitin-proteasome pathways are expressed at significantly higher levels in TES tissues than in VAS tissues. Comparison of the A. suum TES transcriptome with the C. elegans microarray dataset identified 165 A. suum germline-enriched genes (83% are spermatogenesis-enriched). Many of these genes encode serine/threonine kinases and phosphatases (KPs) as well as tyrosine KPs. Immunoblot analysis further suggested a critical role of phosphorylation in both testis development and spermatogenesis. A total of 2,681 A. suum genes were identified to have associated RNAi phenotypes in C. elegans, the majority of which display embryonic lethality, slow growth, larval arrest or sterility.ConclusionsUsing deep sequencing technology, this study has produced a gonad transcriptome of A. suum. By comparison with C. elegans datasets, we identified sets of genes associated with spermatogenesis and gonad development in A. suum. The newly identified genes encoding KPs may help determine signaling pathways that operate during spermatogenesis. A large portion of A. suum gonadal genes have related RNAi phenotypes in C. elegans and, thus, might be RNAi targets for parasite control.

Dataset Information

Cell Non-autonomous Function of daf-18/PTEN in the Somatic Gonad Coordinates Somatic Gonad and Germline Development in C. elegans Dauer Larvae.

Publications

Cell Non-autonomous Function of daf-18/PTEN in the Somatic Gonad Coordinates Somatic Gonad and Germline Development in C. elegans Dauer Larvae.

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