Unknown,Transcriptomics,Genomics,Proteomics

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Transcriptome analysis of sexual dimorphism in the somatic gonadal precursor cells of Caenorhabditis elegans

ABSTRACT: The Caenorhabditis elegans somatic gonad was the first organ to have its cell lineage determined, and the gonadal lineages of the two sexes differ greatly in their pattern of cell divisions, cell migration and cell types. Despite much study, the genetic pathways that direct early gonadal development and establish its sexual dimorphism remain largely unknown, with just a handful of regulatory genes identified from genetic screens. To help define the genetic networks that regulate gonadal development, we employed cell-specific RNA-seq. We identified transcripts present in Z1/Z4 or Z1/Z4 daughter cells in each sex at the onset of somatic gonadal sexual differentiation. For comparison, transcripts were identified in whole animals at both time points. Pairwise comparisons of samples identified several hundred gonad-enriched transcripts, including most known Z1/Z4-enriched mRNAs, and reporter analysis confirmed the effectiveness of this approach. Prior to the Z1/Z4 division few sex-biased Z1/Z4 transcripts were detectable, but less than six hours later, we identified more than 250 sex-biased transcripts in the Z1/Z4 daughters, of which about a third were enriched in the somatic gonad cells compared to cells from whole animals. This indicates that a robust sex-biased developmental program, some of it gonad-specific, initiates in these cells around the time of the first Z1/Z4 division. Cell-specific analysis also identified approximately 70 previously unannotated mRNA isoforms that are enriched in Z1/Z4 or their daughters. Our data suggest that early sex differentiation in the gonad is controlled by a relatively small suite of differentially expressed genes, even after dimorphism has become apparent. 20 total sample: two time points, two sexes, and gonadal cells or whole animals. The earlier time point was collected in triplicate and was harvested 9.5 hours after starved, hatched L1s were fed. The later time point was collected in duplicate and was harvested 15 hour after starved, hatched L1 were fed. Replicates of either dissociated whole animals or gonadal cells (Z1/Z4 or Z1/Z4 daughter) from both male and hermaphrodites were harvested for each time point.

ORGANISM(S): Caenorhabditis elegans

SUBMITTER: Mary Kroetz

PROVIDER: E-GEOD-71772 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Project description:Gonad is a bipotential tissue that depending on the genetic and environmental inputs its final phenotype will be determined. Gonadal development is a very complex process because from an undifferentiated gonad the future testis or ovary will be formed. To better understand the complexity of the gonad plasticity throughout development we explored the transcriptomic landscape of gonads from undifferentiated to juvenile fish. For this study we have used turbot (Scophthalmus maximus) that presents one of the most remarkable sexual dimorphism in cultured fish species. With the aim of identifying gene patterns for each gonad developmental stages a microarray species-specific enriched by reproduction- and immune-related genes was assessed. Further genes with sex-differential mRNA expression were mapped in the sex- and growth-QTL (quantitative trait loci) markers. Data revealed that gonadal transcriptome prevail in front of fish biometry as it was possible to classify gonads according to sexual development status by using gene expression profiles rather than their age or size. The same classification was observed with a selection of a subset of reproduction-related genes showing the importance of gene profiles for each of the developing gonadal stage. Overall microarray data showed the importance of the level of expression (intensity) rather than the number of genes found in each development period. Larger numbers of differentially expressed genes (DEG) were found in the differentiating gonads when compared to ovaries and much smaller number resulted when compared to testis. However, more number of DEG was found in testis when compared to ovaries. The earliest presence of cyp19a1a, the key female sex differentiation gene, was found at 90 dpf together with its transcription factor foxl2 showing at the same time a positive correlation with other genes related to extracellular matrix (ecm2), immune system (irf5) or methylation (sall1). The presence of male-related genes like sox9 was evidenced at early developmental stages (70 and 90 dpf) while expression of dmrt3 started not earlier than 150 dpf, coinciding when larger number of male-related genes were found. All developmental stages presented genes related to immune system and epigenetic mechanisms revealing their importance during gonadal development. Sex-QTLs showed larger amount of sex-differential transcripts in the linkage group 6 and 21 both in males and females but transcripts mapped near growth-QTLs were only found in females. Here it is presented the first assessment of the expression profiles observed in the gonads at different developmental stages by identifying genes responsible for male or female traits. It has been identified gene clusters for each developmental stages and gene network interactions for each sexual phenotype. The expression of known male and female-related genes were precisely described throughout gonadal development as well as the expression of other genes with an unknown reproduction function which have been identified for the first time during sexual development process. In addition, it was possible to localize some of these genes on the sex- and growth-QTLs. The data presented here can help to better understand the reproduction system in cultured fish species and improved selection breeding programs to increase their productivity.

Project description:Gonadal sex differentiation – testis versus ovary formation – is a fundamental process required for reproduction and evolution. Reflecting this importance, the embryonic gonads of vertebrate species comprise the same key cell types; germ cells, supporting cells and interstitial steroidogenic cells. Remarkably, the genetic triggers for gonadal sex differentiation vary across species (the SRY gene in mammals, DMRT1 in birds and some turtles, temperature in many reptiles, AMH and various other genes in fishes). Despite this variation, the cell biology of gonadal development was long thought to be largely conserved. Here, we present a comprehensive analysis of gonadal sex differentiation, using the chicken embryo as a model and considering the entire gonad. We sampled over 30,000 cells across several developmental stages, prior, during and after the onset of gonadal sex differentiation. The data provide several new insights into cell lineage specification during vertebrate gonadogenesis. Combining lineage tracing with single cell transcriptomics, the data show that somatic supporting cells of the embryonic chicken gonad do not derive from the coelomic epithelium, in contrast to other vertebrates studied. Instead, the early somatic precursors cells of the gonads in both sexes derive from a DMRT1+/PAX2+/WNT4+/OSR1+ mesenchymal cell population. In particular, PAX2 marks immigrating mesenchymal cells that give rise to the supporting cell lineage. We find a greater complexity of gonadal cell types than previously thought, including the identification of two distinct sub-populations of Sertoli cells in developing testes, and derivation of embryonic steroidogenic cells from a differentiated supporting cell lineage. We provide significantly improved resolution of gonadal cell types and identify several new gonadal marker genes. Altogether, these results indicate that, just as the genetic trigger for sex differs across vertebrate groups, cell lineage specification in the gonad may also vary substantially.

Project description:Embryonic day 13 (E13), E14, and E16 rat testes and ovaries were used for microarray analysis, as well as E13 testis organ cultures that undergo testis morphogenesis and develop seminiferous cords in vitro. A list of 109 genes resulted from a selective analysis for genes present in male gonadal development and with a 1.5-fold change in expression between E13 and E16. Characterization of these 109 genes potentially important for testis development revealed that cytoskeletal-associated proteins, extracellular matrix factors, and signaling factors were highly represented. Throughout the developmental period (E13-E16), sex-enriched transcripts were more prevalent in the male with 34 of the 109 genes having testis-enriched expression during sex determination. In ovaries, the total number of transcripts with a 1.5-fold change in expression between E13 and E16 was similar to the testis, but none of those genes were both ovary enriched and regulated during the developmental period. Genes conserved in sex determination were identified by comparing changing transcripts in the rat analysis herein, to transcripts altered in previously published mouse studies of gonadal sex determination. A comparison of changing mouse and rat transcripts identified 43 genes with species conservation in sex determination and testis development. Profiles of gene expression during E13-E16 rat testis and ovary development are presented and candidate genes for involvement in sex determination and testis differentiation are identified. Analysis of cellular pathways did not reveal any specific pathways involving multiple candidate genes. However, the genes and gene network identified influence numerous cellular processes with cellular differentiation, proliferation, focal contact, RNA localization, and development being predominant. Experiment Overall Design: RNA samples from two different groups of 20-40 pooled gonads for each sample. Embrionic testis and ovaries of age E13, E14, or E16, and E13 testis cultured for three days were compared to each other

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Transcriptome analysis of sexual dimorphism in the somatic gonadal precursor cells of Caenorhabditis elegans

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