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

Abstract

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.

Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas

“…Animals and yeast have only the meiotic-specific homolog SPO11-1. The ancestral eukaryote may have contained 3 SPO11/TOP6A homologs (the meiosis-specific SPO11-1 and SPO11-2, and the non-meiotic TOP6A and TOP6B proteins) (66). Similar to diatoms (many of which are known to undergo a sexual cycle) and to red algae, Micromonas and Ostreococcus both appeared to have lost SPO11-1 but retained SPO11-2 as well as the non-meiotic TOP6A and TOP6B.…”

“…In plants, absence of these leads to a dwarf phenotype and impairs endo-reduplication (59)(60)(61)(62). Genes for TOP6A and TOP6B are found in many eukaryotes and they were perhaps present in the ancestral eukaryotic cell (66). Plants also have several RECA paralogs, some chloroplast-targeted and some mitochondrion-targeted.…”

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

“…Analysis of the resulting sequence indicates that Smed-spo11 encodes a 300-aa protein containing six of the seven highly conserved regions characteristic of SPO11 orthologs ( Fig. S7) (38). To study the timing and spatial control of DSB formation in planarian meiosis, we needed to identify a protein that marks the sites of DSB formation.…”

Novel Nucleotide Sequence Motifs That Produce Hotspots of Meiotic Recombination inSchizosaccharomyces pombe

“…These hotspots coincide with the formation of DNA double-strand breaks (DSBs) in both the fission and budding yeasts and likely many other organisms (Sun et al 1989;Cao et al 1990;Fan et al 1995;Cervantes et al 2000;Mahadevaiah et al 2001;Petes 2001;Steiner et al 2002;Young et al 2002;Cromie et al 2007). Formation of DSBs requires a number of different proteins, including Spo11 (Rec12 in Schizosaccharomyces pombe), a widely conserved protein among eukaryotes that has the active site for cleaving the phosphodiester backbone (Keeney et al 1997;Cervantes et al 2000;Malik et al 2007). After the formation of DSBs, the two broken ends of the DNA initiate recombination by invading intact homologous DNA to form joint molecules, which can be resolved to produce both crossover and noncrossover exchanges (Pâques and Haber 1999).…”