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. 2006 Jul 5;103(27):10328-10333.
doi: 10.1073/pnas.0604232103. Epub 2006 Jun 23.

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

Zhenguo Lin  1   2 , Hongzhi Kong  3 , Masatoshi Nei  4 , Hong Ma  4   1
Affiliations

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

Zhenguo Lin et al. Proc Natl Acad Sci U S A. .

Abstract

The bacterial recA gene and its eukaryotic homolog RAD51 are important for DNA repair, homologous recombination, and genome stability. Members of the recA/RAD51 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 recA/RAD51 homologs (RADA and RADB), and eukaryotes possess multiple members (RAD51, RAD51B, RAD51C, RAD51D, DMC1, XRCC2, XRCC3, and recA). Phylogenetic analyses indicated that the recA/RAD51 family can be divided into three subfamilies: (i) RADalpha, with highly conserved functions; (ii) RADbeta, with relatively divergent functions; and (iii) recA, functioning in eubacteria and eukaryotic organelles. The RADalpha and RADbeta subfamilies each contain archaeal and eukaryotic members, suggesting that a gene duplication occurred before the archaea/eukaryote split. In the RADalpha 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 meiosis-specific genes. The RADbeta 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.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
Schematic diagram of domain structures of representative RecA/RAD51-like proteins, drawn to scale. Domain names are indicated in the figure.
Fig. 2.
Fig. 2.
Phylogenies of the recA/RAD51 gene family. (A) Phylogenetic tree of 66 recA/RAD51-like genes from representative species using the recA/RAD51-domain region. NJ and ML consensus trees were topologically congruent except for one clade, which was not statistically significant. Only NJ percent bootstrap values are presented for each clades with >50%, unless the difference of the values between NJ and ML trees is >5%. The scale bar indicates the number of amino acid substitutions per site. (B) Phylogenetic tree of RAD51-like genes from eukaryotes and archaea constructed by NJ (Poisson correction with gamma parameters).
Fig. 3.
Fig. 3.
Loss of DMC1 and rapid evolution of RAD51 in Caenorhabditis and Anthropoda shown by ML analysis for the RADα subfamily. Percent bootstrap values are given as in Fig. 2. Genes from insects are in red.
Fig. 4.
Fig. 4.
ML tree of recA-like genes from bacteria and eukaryotes. NJ and ML consensus trees are topologically congruent on most clades. Percent bootstrap values are given as in Fig. 2. Major eubacterial taxonomic groups, plants, and protists were indicated and shaded by different background colors.
Fig. 5.
Fig. 5.
A model of the evolutionary history of recA/RAD51 gene family. The gene duplication that occurred before the divergence of archaea and eukaryotes gave rise to two lineages, RADα and RADβ, and, in eubacteria, recA has remained as a single-copy gene. In eukaryotes, both RADα and RADβ genes experienced several duplication events, but, in archaea, they remained as single-copy genes. Eukaryotic recA genes originated from proteobacteria (recAmt) and cyanobacteria (recAcp) recA genes after two separate endosymbiotic events. recAmts were subsequently lost in the ancestors of animals and fungi.
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