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UniProt release 2018_10

Published November 7, 2018

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Sexual reproduction is a great process to diversify the genetic pool and to accelerate evolution. However, it imposes tight constraints for success. First, sperm must meet egg, an unfertilized egg cannot develop. In addition, exactly one sperm cell has to meet one egg, polyspermy is not viable. And to ensure the survival of distinct species, the process has to be strictly species-specific. This requirement is particularly challenging in organisms in which fertilization occurs externally, as is the case for fish.

Looking for factors required for fertilization in vertebrates, Herberg et al. identified a small protein highly expressed in zebrafish (Danio rerio) oocytes. They called the protein Bouncer. Bouncer is located at the cell surface where it is attached to the membrane through a glycosylphosphatidylinositol (GPI) anchor, following cleavage of the C-terminal propeptide.

Bouncer function was investigated in knockout zebrafish. At first glance, the mutant animals did not show any overt phenotype. They were produced at the expected Mendelian rates and developed normally. When fertility was tested, there was no difference between knockout and wild-type males, but knockout females were almost completely sterile. Delivery of sperm into Bouncer-deficient eggs by intracytoplasmic sperm injection restored embryonic development, suggesting that Bouncer was involved in sperm entry during fertilization. Bouncer was indeed shown to promote sperm-egg binding. Could Bouncer play a role in species recognition during fertilization? To test this hypothesis, zebrafish Bouncer knockout eggs expressing the medaka fish (Oryzias latipes) Bouncer ortholog were generated. Medaka sperm cannot normally fertilize zebrafish eggs. Both species split apart some 200 million years ago, much earlier than we did from mice, and they share only 40% sequence identity. Amazingly the transgenic knockout eggs could be fertilized by medaka, but not zebrafish sperm. Fertility rates of individual transgenic medaka Bouncer females were found to correlate with expression levels of medaka Bouncer mRNA in eggs. In conclusion, the small 80-amino acid-long Bouncer protein plays a crucial role in species-specific fertilization. The rescue was not complete. The fertility rate was low, suggesting that other factors likely contribute to species-specific sperm-egg interaction.

Bouncer homologs exist in other vertebrate species. Its closest relative in mammals is the SPACA4 gene. Bouncer/SPACA4 germline-restricted expression was confirmed in all vertebrates tested. However, Bouncer ovary-specific expression was observed only in externally fertilizing animals, such as fish or amphibians; surprisingly, internally fertilizing vertebrates, such as reptiles and mammals, show testis-specific expression. The reason for this difference is not clear and the function of mammalian SPACA4 is not yet known.

As of this release, zebrafish and medaka Bouncer proteins have been annotated and integrated into UniProtKB/Swiss-Prot.

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