Origins and evolution of the recA / RAD51 gene family: Evidence for ancient gene duplication and endosymbiotic gene transfer

Abstract

The bacterial recA gene and its eukaryotic homolog RAD51 are important for DNA repair, homologous recombination, and genome stability. Members of the recA͞RAD51 family have functions that have differentiated during evolution. However, the evolutionary history and relationships of these members remains unclear. Homolog searches in prokaryotes and eukaryotes indicated that most eubacteria contain only one recA. However, many archaeal species have two recA͞RAD51 homologs (RADA and RADB), and eukaryotes possess multiple members (RAD51, RAD51B, RAD51C, RAD51D, DMC1, XRCC2, XRCC3, and recA). Phylogenetic analyses indicated that the recA͞RAD51 family can be divided into three subfamilies: (i) RAD␣, with highly conserved functions; (ii) RAD␤, with relatively divergent functions; and (iii) recA, functioning in eubacteria and eukaryotic organelles. The RAD␣ and RAD␤ subfamilies each contain archaeal and eukaryotic members, suggesting that a gene duplication occurred before the archaea͞eukaryote split. In the RAD␣ subfamily, eukaryotic RAD51 and DMC1 genes formed two separate monophyletic groups when archaeal RADA genes were used as an outgroup. This result suggests that another duplication event occurred in the early stage of eukaryotic evolution, producing the DMC1 clade with meiosisspecific genes. The RAD␤ subfamily has a basal archaeal clade and five eukaryotic clades, suggesting that four eukaryotic duplication events occurred before animals and plants diverged. The eukaryotic recA genes were detected in plants and protists and showed strikingly high levels of sequence similarity to recA genes from proteobacteria or cyanobacteria. These results suggest that endosymbiotic transfer of recA genes occurred from mitochondria and chloroplasts to nuclear genomes of ancestral eukaryotes.origins of meiosis and eukaryotes ͉ phylogenetic analysis ͉ recombination ͉ DNA repair ͉ organellar genes D NA double-strand breaks (DSBs) can occur either spontaneously during DNA replication or by exogenous DNAdamaging agents. Efficient repair of DSBs is critical for genomic stability and cellular viability (1). A major DSB repair pathway is homologous recombination, which is also critical for meiosis and generation of genetic diversity. Among the best known recombination genes are the Escherichia coli recA gene and its eukaryotic homologs RAD51s (2, 3). recA encodes a DNA-dependent ATPase that binds to single-stranded DNA and promotes strand invasion and exchange between homologous DNA molecules (4). The two eukaryotic recA homologs, RAD51 and DMC1, were first discovered in the budding yeast Saccharomyces cerevisiae and are structurally and functionally similar to the E. coli recA gene (5, 6).Homologs of recA and RAD51 have then been identified in many prokaryotes and eukaryotes. In eubacteria, only one recA gene has been previously reported in each species (7). Unlike eubacteria, several archaeal species have two recA͞RAD51-like genes, called RADA and RADB (Table 1, which is published as supporting information on the PNAS web site) (8, 9)....

The plant‐specific CDKB 1‐ CYCB 1 complex mediates homologous recombination repair in Arabidopsis

“…RAD51 and its homologs build a small gene family in Arabidopsis similar to other eukaryotes (Lin et al , 2006). Previous studies revealed hypersensitivity of mutants in Arabidopsis RAD51 family members to DNA‐cross‐linking agents such as cisplatin and mitomycin C, as seen, for example, by a reduced number of true leaves formed in rad51b and rad51c mutants in comparison with the wild type (Osakabe et al , 2002, 2005; Bleuyard & White, 2004; Abe et al , 2005; Bleuyard et al , 2005; Li et al , 2005; Charbonnel et al , 2010).…”

Genomic drift and copy number variation of sensory receptor genes in humans

“…It seems to have occurred also in the evolution of Ig genes (S. Das, M. Nozawa, J. Klein, and M. Nei, unpublished work). However, genomic drift appears to be less important in genes controlling the basic cellular process such as DNA repair and homologous recombination (38) or genes controlling the characters in the early stage of development. For example, the number of Hox genes concerned with the formation of body pattern of animals is Ϸ40 in most tetrapod species (39,40).…”

The Ectocarpus genome and the independent evolution of multicellularity in brown algae

“…Along similar lines, there is evidence that, compared to unicellular organisms, multicellular organisms have tended to retain a more complete Rad51 family, which encodes DNA repair proteins including members with important roles during meiosis 25 . This is also the case in the stramenopiles, where Ectocarpus has a markedly more complete Rad51 gene family than the other sequenced members of the group (Supplementary Information 2.3.12).…”