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The Xenopus Primordial Germ Cell Transcriptome: Unexpected Role for sox7 in Early PGC Development

ABSTRACT: Xenopus primordial germ cells (PGCs) are determined by the presence of maternally derived germ plasm. Germ plasm components both protect PGCs from somatic differentiation and begin a unique gene expression program. Segregation of the germline from the endodermal lineage occurs during gastrulation and PGCs subsequently initiate zygotic transcription. However, the gene-networks that operate to both preserve the potential for totipotency and promote germline differentiation are poorly understood. Here, we utilized RNA-sequencing analysis to comprehensively interrogate PGC and neighboring endoderm cell RNAs after lineage segregation. We identified 1,865 transcripts enriched in PGCs compared to endoderm cells. Over 50% of maternal, vegetally-enriched transcripts were enriched in the PGC transcriptome, including sox7. PGC-directed sox7 knockdown and over-expression studies revealed an early requirement for sox7 in proper germ plasm localization, zygotic transcription, and PGC number. We identified oct60 as the most highly expressed and enriched OCT3/4 homologue in PGCs. Lastly, we compared the Xenopus PGC transcriptome with human PGC transcripts and showed that 80% of transcripts are conserved, identifying Xenopus as a relevant model system for understanding the gene-networks necessary for human germline development.

ORGANISM(S): Xenopus laevis

PROVIDER: GSE102047 | GEO | 2017/08/01

SECONDARY ACCESSION(S): PRJNA396491

REPOSITORIES: GEO

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Project description:Background: During the maternal-to-zygotic transition (MZT) vast changes in the embryonic transcriptome are produced by a combination of two processes: elimination of maternally provided mRNAs and synthesis of new transcripts from the zygotic genome. Previous genome-wide analyses of the MZT have been restricted to whole embryos. Here we report the first such analysis for primordial germ cells (PGCs), the progenitors of the germ-line stem cells. Results: We purified PGCs from Drosophila embryos, defined their proteome and transcriptome, and assessed the content, scale and dynamics of their MZT. Transcripts encoding proteins that implement particular types of biological functions group into nine distinct expression profiles, reflecting coordinate control at the transcriptional and posttranscriptional levels. mRNAs encoding germ-plasm components and cell-cell signaling molecules are rapidly degraded while new transcription produces mRNAs encoding the core transcriptional and protein synthetic machineries. The RNA-binding protein, Smaug, is essential for the PGC MZT, clearing transcripts encoding proteins that regulate stem cell behavior, transcriptional and posttranscriptional processes. Computational analyses suggest that Smaug and AU-rich element binding-proteins function independently to control transcript elimination. Conclusion: The scale of the MZT is similar in the soma and PGCs. However, the timing and content of their MZTs differ, reflecting the distinct developmental imperatives of these cell types. The PGC MZT is delayed relative to that in the soma, likely because relief of PGC-specific transcriptional silencing is required for zygotic genome activation as well as for efficient maternal transcript clearance. There are 26 samples in total, including 1-to-3 hour, 3-to-5 hour, 5-to-7 hour PGCs in wild type and smaug mutant flies and 1-to-3 hour somatic cells in wild type flies. Except for the 1-to-3 hour and 3-to-5 hour smaug mutant PGCs which have three replicates, all the other samples have four replicates.

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The Xenopus Primordial Germ Cell Transcriptome: Unexpected Role for sox7 in Early PGC Development

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