Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates
- Columbia University, United States
- Centro de Investigaciones Científicas de las Huastecas "Aguazarca", Mexico
Abstract
Studies of highly diverged species have revealed two mechanisms by which meiotic recombination is directed to the genome—through PRDM9 binding or by targeting promoter-like features—that lead to dramatically different evolutionary dynamics of hotspots. Here, we identify PRDM9 orthologs from genome and transcriptome data in 225 species. We find the complete PRDM9 ortholog across distantly related vertebrates but, despite this broad conservation, infer a minimum of six partial and three complete losses. Strikingly, taxa carrying the complete ortholog of PRDM9 are precisely those with rapid evolution of its predicted binding affinity, suggesting that all domains are necessary for directing recombination. Indeed, as we show, swordtail fish carrying only a partial but conserved ortholog share recombination properties with PRDM9 knock-outs.
Data availability
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Xiphophorus birchmanni and Xiphophorus malinche RNAseq data Raw sequence readsPublicly available at the NCBI BioProject (accession no: PRJNA358086).
Article and author information
Author details
Funding
National Institutes of Health (R01 GM83098)
- Molly Przeworski
National Science Foundation (DDIG DEB-1405232)
- Molly Schumer
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Animals used for this study were handled according to the approved institutional animal care and use committee (IACUC) protocol AUP# - IACUC 2013-0168 of Texas A&M University. All individuals used for dissections were first treated with MS-222 for anesthesia to minimize suffering before being euthanized.
Reviewing Editor
- Bernard de Massy, Institute of Human Genetics, CNRS UPR 1142, France
Publication history
- Received: December 10, 2016
- Accepted: June 3, 2017
- Accepted Manuscript published: June 6, 2017 (version 1)
- Version of Record published: July 20, 2017 (version 2)
Copyright
© 2017, Baker 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.
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Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates
eLife 6:e24133.
https://doi.org/10.7554/eLife.24133
Further reading
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- Genetics and Genomics
The ways in which recombination sites are determined during meiosis are becoming clearer following a phylogenomic analysis for 225 different species.
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- Evolutionary Biology
- Genetics and Genomics
The accidental endogenization of viral elements within eukaryotic genomes can occasionally provide significant evolutionary benefits, giving rise to their long-term retention, that is, to viral domestication. For instance, in some endoparasitoid wasps (whose immature stages develop inside their hosts), the membrane-fusion property of double-stranded DNA viruses have been repeatedly domesticated following ancestral endogenizations. The endogenized genes provide female wasps with a delivery tool to inject virulence factors that are essential to the developmental success of their offspring. Because all known cases of viral domestication involve endoparasitic wasps, we hypothesized that this lifestyle, relying on a close interaction between individuals, may have promoted the endogenization and domestication of viruses. By analyzing the composition of 124 Hymenoptera genomes, spread over the diversity of this clade and including free-living, ecto, and endoparasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses, in comparison with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often endogenized and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Second, our analysis indicates that the rate at which dsDNA viruses are endogenized is higher in endoparasitoids than in ectoparasitoids or free-living hymenopterans, which also translates into more frequent events of domestication. Hence, these results are consistent with the hypothesis that the endoparasitoid lifestyle has facilitated the endogenization of dsDNA viruses, in turn, increasing the opportunities of domestications that now play a central role in the biology of many endoparasitoid lineages.
