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Lineage-independent retrotransposition of UTP14 associated with male fertility has occurred multiple times throughout mammalian evolution.

ABSTRACT: In mammals, gamete production is essential for reproductive success. This is particularly true for males where large quantities of sperm are produced to fertilize a limited number of eggs released by the female. Because of this, new genes associated with increased spermatogenic efficiency have been accumulating throughout the evolution of therian mammals. Many of these new genes are testis-specific retrotransposed copies of housekeeping genes located on the X chromosome. Of particular interest are retrotransposed copies of UTP14 that are present in many distantly related eutherian mammals. Analysis of genomic data available in ENSEMBL indicates that these UTP14 retrogenes have arisen independently in the various eutherian clades. They represent an interesting aspect of evolution whereby new homologues of UTP14 have become independently fixed in multiple mammalian lineages due to the reproductive advantage that may be conferred to males. Surprisingly, these genes may also be lost, even after being present within a lineage for millions of years. This phenomenon may potentially be used to delineate evolutionary trees in closely related groups of mammals, particularly in the case of South American primates. Studying these retrogenes will yield new insights into the evolutionary history of male gamete production and the phylogeny of eutherian mammals.

SUBMITTER: Rohozinski J

PROVIDER: S-EPMC5750009 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Lineage-independent retrotransposition of UTP14 associated with male fertility has occurred multiple times throughout mammalian evolution.

Rohozinski Jan J

Royal Society open science 20171220 12

In mammals, gamete production is essential for reproductive success. This is particularly true for males where large quantities of sperm are produced to fertilize a limited number of eggs released by the female. Because of this, new genes associated with increased spermatogenic efficiency have been accumulating throughout the evolution of therian mammals. Many of these new genes are testis-specific retrotransposed copies of housekeeping genes located on the X chromosome. Of particular interest a ...[more]

PMID: 29308242

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Project description:BACKGROUND:VNTR (Variable Number of Tandem Repeats) composite retrotransposons - SVA (SINE-R-VNTR-Alu), LAVA (LINE-1-Alu-VNTR-Alu), PVA (PTGR2-VNTR-Alu) and FVA (FRAM-VNTR-Alu) - are specific to hominoid primates. Their assembly, the evolution of their 5' and 3' domains, and the functional significance of the shared 5' Alu-like region are well understood. The central VNTR domain, by contrast, has long been assumed to represent a more or less random collection of 30-50 bp GC-rich repeats. It is only recently that it attracted attention in the context of regulation of SVA expression. RESULTS:Here we provide evidence that the organization of the VNTR is non-random, with conserved repeat unit (RU) arrays at both the 5' and 3' ends of the VNTRs of human, chimpanzee and orangutan SVA and gibbon LAVA. The younger SVA subfamilies harbour highly organized internal RU arrays. The composition of these arrays is specific to the human/chimpanzee and orangutan lineages, respectively. Tracing the development of the VNTR through evolution we show for the first time how tandem repeats evolve within the constraints set by a functional, non-autonomous non-LTR retrotransposon in two different families - LAVA and SVA - in different hominoid lineages. Our analysis revealed that a microhomology-driven mechanism mediates expansion/contraction of the VNTR domain at the DNA level. Elements of all four VNTR composite families have been shown to be mobilized by the autonomous LINE1 retrotransposon in trans. In case of SVA, key determinants of mobilization are found in the 5' hexameric repeat/Alu-like region. We now demonstrate that in LAVA, by contrast, the VNTR domain determines mobilization efficiency in the context of domain swaps between active and inactive elements. CONCLUSIONS:The central domain of VNTR composites evolves in a lineage-specific manner which gives rise to distinct structures in gibbon LAVA, orangutan SVA, and human/chimpanzee SVA. The differences observed between the families and lineages are likely to have an influence on the expression and mobilization of the elements.

Dataset Information

Lineage-independent retrotransposition of UTP14 associated with male fertility has occurred multiple times throughout mammalian evolution.

Publications

Lineage-independent retrotransposition of UTP14 associated with male fertility has occurred multiple times throughout mammalian evolution.

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