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MBE Advance Access originally published online on October 5, 2007
Molecular Biology and Evolution 2007 24(12):2827-2841; doi:10.1093/molbev/msm217
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Protist Homologs of the Meiotic Spo11 Gene and Topoisomerase VI reveal an Evolutionary History of Gene Duplication and Lineage-Specific Loss

Shehre-Banoo Malik*,1, Marilee A. Ramesh{dagger},1, Alissa M. Hulstrand* and John M. Logsdon, Jr.*

* Department of Biological Sciences, Roy J. Carver Center for Comparative Genomics, University of Iowa
{dagger} Department of Biology, Roanoke College

E-mail: john-logsdon{at}uiowa.edu.

Accepted for publication September 27, 2007.

Spo11 is a meiotic protein of fundamental importance as it is a conserved meiosis-specific transesterase required for meiotic recombination initiation in fungi, animals, and plants. Spo11 is homologous to the archaebacterial topoisomerase VIA (Top6A) gene, and its homologs are broadly distributed among eukaryotes, with some eukaryotes having more than one homolog. However, the evolutionary relationships among these genes are unclear, with some debate as to whether eukaryotic homologs originated by lateral gene transfer. We have identified and characterized protist Spo11 homologs by degenerate polymerase chain reaction (PCR) and sequencing and by analyses of sequences from public databases. Our phylogenetic analyses show that Spo11 homologs evolved by two ancient eukaryotic gene duplication events prior to the last common ancestor of extant eukaryotes, resulting in three eukaryotic paralogs: Spo11-1, Spo11-2, and Spo11-3. Spo11-1 orthologs encode meiosis-specific proteins and are distributed broadly among eukaryotic lineages, though Spo11-1 is absent from some protists. This absence coincides with the presence of Spo11-2 orthologs, which are meiosis-specific in Arabidopsis and are found in plants, red algae, and some protists but absent in animals and fungi. Spo11-3 encodes a Top6A subunit that interacts with topoisomerase VIB (Top6B) subunits, which together play a role in vegetative growth in Arabidopsis. We identified Spo11-3 (Top6A) and Top6B homologs in plants, red algae, and a few protists, establishing a broader distribution of these genes among eukaryotes, indicating their likely vertical descent followed by lineage-specific loss.

Key Words: Spo11 • meiosis • recombination • evolution • recombination initiation • phylogeny • eukaryotes

1 Equal contributions to this work.

Andrew Roger, Associate Editor


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