New cellular functions and developmental processes can evolve by modifying existing genes or creating novel genes. Novel genes can arise not only via duplication or mutation but also by acquiring foreign DNA, also called horizontal gene transfer (HGT). Here we show that HGT likely contributed to the creation of a novel gene indispensable for reproduction in some insects. Long considered a novel gene with unknown origin, oskar has evolved to fulfil a crucial role in insect germ cell formation. Our analysis of over 100 insect Oskar sequences suggests that Oskar arose de novo via fusion of eukaryotic and prokaryotic sequences. This work shows that highly unusual gene origin processes can give rise to novel genes that can facilitate evolution of novel developmental mechanisms.
All data are available in the main text or the supplementary materials.
- Leo Blondel
- Cassandra G Extavour
- Tamsin E M Jones
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
- Antonis Rokas, Vanderbilt University, United States
© 2020, Blondel et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Imaging experiments reveal the complex and dynamic nature of the transcriptional hubs associated with Notch signaling.
Cylicins are testis-specific proteins, which are exclusively expressed during spermiogenesis. In mice and humans, two Cylicins, the gonosomal X-linked Cylicin 1 (Cylc1/CYLC1) and the autosomal Cylicin 2 (Cylc2/CYLC2) genes, have been identified. Cylicins are cytoskeletal proteins with an overall positive charge due to lysine-rich repeats. While Cylicins have been localized in the acrosomal region of round spermatids, they resemble a major component of the calyx within the perinuclear theca at the posterior part of mature sperm nuclei. However, the role of Cylicins during spermiogenesis has not yet been investigated. Here, we applied CRISPR/Cas9-mediated gene editing in zygotes to establish Cylc1- and Cylc2-deficient mouse lines as a model to study the function of these proteins. Cylc1 deficiency resulted in male subfertility, whereas Cylc2-/-, Cylc1-/yCylc2+/-, and Cylc1-/yCylc2-/- males were infertile. Phenotypical characterization revealed that loss of Cylicins prevents proper calyx assembly during spermiogenesis. This results in decreased epididymal sperm counts, impaired shedding of excess cytoplasm, and severe structural malformations, ultimately resulting in impaired sperm motility. Furthermore, exome sequencing identified an infertile man with a hemizygous variant in CYLC1 and a heterozygous variant in CYLC2, displaying morphological abnormalities of the sperm including the absence of the acrosome. Thus, our study highlights the relevance and importance of Cylicins for spermiogenic remodeling and male fertility in human and mouse, and provides the basis for further studies on unraveling the complex molecular interactions between perinuclear theca proteins required during spermiogenesis.