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Comments on Seidel, Hannah et al. (2009) International Worm Meeting "Balancing selection maintains paternal-effect-by-zygotic incompatibility among C. elegans wild isolates." (0)
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Seidel, Hannah, Rockman, Matthew, Ailion, Michael, & Kruglyak, Leonid (2009). Balancing selection maintains paternal-effect-by-zygotic incompatibility among C. elegans wild isolates presented in International Worm Meeting. Unpublished information; cite only with author permission.
C. elegans strains Bristol (N2) and Hawaii (CB4856) exhibit a paternal-effect-by-zygotic incompatibility involving two genes - peel-1 and zeel-1. peel-1 and zeel-1 interact like a toxin and an antidote: peel-1 is a paternal-effect gene that induces developmental arrest in embryos that do not inherit the zygotically expressed gene zeel-1. peel-1 and zeel-1 are located adjacent to one another in the Bristol genome, and Hawaii carries a deletion spanning both genes. We have cloned peel-1 and zeel-1 by transgenic complementation. peel-1 encodes a predicted transmembrane protein with no homology to any gene in any species. peel-1::gfp transcriptional fusions are expressed in spermatocytes, and immunostaining localizes PEEL-1 to the cell membrane of mature sperm. Embryos affected by the paternal-effect lethality arrest paralyzed at the two-fold stage, suggesting that PEEL-1 causes a defect in muscle development or function. zeel-1 encodes a protein homologous to the substrate recognition subunit of an E3 ubiquitin ligase. Unlike most members of its family, ZEEL-1 contains a predicted transmembrane domain, and this transmembrane domain is required for the ability of zeel-1 to rescue the paternal-effect lethality. zeel-1::gfp translational fusions are expressed ubiquitously in the embryo, beginning approximately 4 hours post-fertilization and ending before hatching. The observation that zeel-1 expression does not begin until mid-embryogenesis raises the possibility that sperm-supplied PEEL-1 persists for several hours after fertilization. The zeel-1/peel-1 incompatibility is not specific to a cross between Bristol and Hawaii. We have genotyped a large panel of wild strains at the zeel-1/peel-1 locus and found that approximately two thirds of strains carry zeel-1 and peel-1 (like Bristol), whereas the remaining strains carry a deletion of the genes (like Hawaii). The Bristol- and Hawaii-like haplotypes exhibit elevated sequence divergence, and the allele frequency spectrum at the locus is indicative of balancing selection. We propose that balancing selection acting on zeel-1, peel-1, or a tightly linked locus preserves both haplotypes in the population despite the lethality caused by their interaction.