SPE-44 Implements Sperm Cell Fate

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Abstract
The sperm/oocyte decision in the hermaphrodite germline of Caenorhabditis elegans provides a powerful model for the characterization of stem cell fate specification and differentiation. The germline sex determination program that governs gamete fate has been well studied, but direct mediators of cell-type-specific transcription are largely unknown. We report the identification of spe-44 as a critical regulator of sperm gene expression. Deletion of spe-44 causes sperm-specific defects in cytokinesis, cell cycle progression, and organelle assembly resulting in sterility. Expression of spe-44 correlates precisely with spermatogenesis and is regulated by the germline sex determination pathway. spe-44 is required for the appropriate expression of several hundred sperm-enriched genes. The SPE-44 protein is restricted to the sperm-producing germline, where it localizes to the autosomes (which contain sperm genes) but is excluded from the transcriptionally silent X chromosome (which does not). The orthologous gene in other Caenorhabditis species is similarly expressed in a sex-biased manner, and the protein likewise exhibits autosome-specific localization in developing sperm, strongly suggestive of an evolutionarily conserved role in sperm gene expression. Our analysis represents the first identification of a transcriptional regulator whose primary function is the control of gamete-type-specific transcription in this system. Stem cells give rise to the variety of specialized cell types within an organism. The decision to adopt a particular cell fate, a process known as specification or determination, requires the coordinated expression of all of the genes needed for that specialized cell to develop and function properly. Understanding the mechanisms that govern these patterns of gene expression is critical to our understanding of stem cell fate specification. We study this process in a nematode species that makes both sperm and eggs from the same stem cell population. We have identified a gene, named spe-44, that is required for the proper expression of sperm genes (but not egg genes). Mutation in spe-44 produces sterile sperm with developmental defects. spe-44 is controlled by factors that govern the sperm/egg decision, and its function in controlling sperm gene expression appears to be conserved in other nematode species.

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