Phylogeny, recombination, and mechanisms of stepwise mitochondrial genome reorganization in mantellid frogs from Madagascar.
In Malagasy frogs of the family Mantellidae, the genus Mantella is known to possess highly reorganized mitochondrial (mt) genomes with the following characteristics: 1) some rearranged gene positions, 2) 2 distinct genes and a pseudogene corresponding to the transfer RNA gene for methionine (trnM), and 3) 2 control regions (CRs) with almost identical nucleotide sequences. These unique genomic features were observed concentrated between the duplicated CRs surrounding cytochrome b (cob) and nicotinamide adenine dinucleotide dehydrogenase subunit 2 (cnad2) genes. To elucidate the mechanisms and evolutionary pathway that yielded the derived genome condition, we surveyed the reorganized genomic portion for all 12 mantellid genera. Our results show that the mt genomes of 7 genera retain the ancestral condition. In contrast, adding to Mantella, 4 genera of the subfamily Mantellinae, Blommersia, Guibemantis, Wakea, and Spinomantis, share several derived genomic characters. Furthermore, mt genomes of these mantellines showed additional structural divergences, resulting in different genome conditions between them. The high frequency of genomic reorganization does not correlate with nucleotide substitution rate. The encountered mt genomic conditions also suggest the occurrences of stepwise gene duplication and deletion events during the evolution of mantellines. Simultaneously, the majority of duplication events seems to be mediated by general (homologous) or illegitimate recombination, and general recombination also plays a role in concerted sequence evolution between multiple CRs. Considering our observations and recent conditional evidences, the following outlines can be expected for recombination processes in mt genome reorganization. 1) The CR is the "hot spot" of recombination; 2) highly frequent recombination between CRs may be mediated by a replication fork barrier lying in the CR; 3) general recombination has a potential to cause gene rearrangement in upstream regions of multiple CRs as the results of gene conversion and unequal crossing over processes. Our results also suggest that recombination activity is not a direct cause of convergent gene rearrangement; rather, homoplasious gene rearrangement seems to be mediated by persistence of a copied genomic condition through several lineage splits and subsequent parallel deletions.
Kurabayashi
Atsushi
A
Institute for Amphibian Biology, Graduate School of Science, Hiroshima University, Hiroshima, Japan. kuraba@hiroshima-u.ac.jp
Sumida
Masayuki
M
Yonekawa
Hiromichi
H
Glaw
Frank
F
Vences
Miguel
M
Hasegawa
Masami
M
D000818:Animals; D001001:Anura / Q000145:classification / Q000235:genetics*; D045303:Cytochromes b / Q000235:genetics; D004272:DNA, Mitochondrial / Q000737:chemistry / Q000235:genetics; D019143:Evolution, Molecular; D015321:Gene Rearrangement; D016678:Genome; D008270:Madagascar; D008928:Mitochondria / Q000235:genetics*; D009705:Nucleosides / Q000737:chemistry; D010802:Phylogeny; D012343:RNA, Transfer / Q000235:genetics; D011995:Recombination, Genetic; D012045:Regulatory Sequences, Nucleic Acid
D004272:DNA, Mitochondrial; D009705:Nucleosides; D012343:RNA, Transfer; D045303:Cytochromes b