The vertebrate makorin ubiquitin ligase gene family has been shaped by large-scale duplication and retroposition from an ancestral gonad-specific, maternal-effect gene

BMC Genomics. 2010;11(1):721 DOI 10.1186/1471-2164-11-721

 

Journal Homepage

Journal Title: BMC Genomics

ISSN: 1471-2164 (Online)

Publisher: BMC

LCC Subject Category: Technology: Chemical technology: Biotechnology | Science: Biology (General): Genetics

Country of publisher: United Kingdom

Language of fulltext: English

Full-text formats available: PDF, HTML

 

AUTHORS

Volff Jean-Nicolas
Baroiller Jean-Francois
Galiana-Arnoux Delphine
D'Cotta Helena
Darras Amandine
Böhne Astrid

EDITORIAL INFORMATION

Blind peer review

Editorial Board

Instructions for authors

Time From Submission to Publication: 17 weeks

 

Abstract | Full Text

<p>Abstract</p> <p>Background</p> <p>Members of the makorin <it>(mkrn) </it>gene family encode RING/C3H zinc finger proteins with U3 ubiquitin ligase activity. Although these proteins have been described in a variety of eukaryotes such as plants, fungi, invertebrates and vertebrates including human, almost nothing is known about their structural and functional evolution.</p> <p>Results</p> <p>Via partial sequencing of a testis cDNA library from the poeciliid fish <it>Xiphophorus maculatus</it>, we have identified a new member of the <it>makorin </it>gene family, that we called <it>mkrn4</it>. In addition to the already described <it>mkrn1 </it>and <it>mkrn2</it>, <it>mkrn4 </it>is the third example of a makorin gene present in both tetrapods and ray-finned fish. However, this gene was not detected in mouse and rat, suggesting its loss in the lineage leading to rodent murids. <it>Mkrn2 </it>and <it>mkrn4 </it>are located in large ancient duplicated regions in tetrapod and fish genomes, suggesting the possible involvement of ancestral vertebrate-specific genome duplication in the formation of these genes. Intriguingly, many <it>mkrn1 </it>and <it>mkrn2 </it>intronless retrocopies have been detected in mammals but not in other vertebrates, most of them corresponding to pseudogenes. The nature and number of zinc fingers were found to be conserved in Mkrn1 and Mkrn2 but much more variable in Mkrn4, with lineage-specific differences. RT-qPCR analysis demonstrated a highly gonad-biased expression pattern for <it>makorin </it>genes in medaka and zebrafish (ray-finned fishes) and amphibians, but a strong relaxation of this specificity in birds and mammals. All three <it>mkrn </it>genes were maternally expressed before zygotic genome activation in both medaka and zebrafish early embryos.</p> <p>Conclusion</p> <p>Our analysis demonstrates that the <it>makorin </it>gene family has evolved through large-scale duplication and subsequent lineage-specific retroposition-mediated duplications in vertebrates. From the three major vertebrate <it>mkrn </it>genes, <it>mkrn4 </it>shows the highest evolutionary dynamics, with lineage-specific loss of zinc fingers and even complete gene elimination from certain groups of vertebrates. Comparative expression analysis strongly suggests that the ancestral E3 ubiquitin ligase function of the single copy <it>mkrn </it>gene before duplication in vertebrates was gonad-specific, with maternal expression in early embryos.</p>