Homologous genetic recombination as an intrinsic dynamic property of a DNA structure induced by recA/rad51-family proteins: A possible advantage of DNA over RNA as genomic material

Takehiko Shibata, Taro Nishinaka, Tsutomu Mikawa, Hideki Aihara, Hitoshi Kurumizaka, Shigeyuki Yokoyama, Yutaka Ito

Research output: Contribution to journalArticle

55 Scopus citations

Abstract

Heteroduplex joints are general intermediates of homologous genetic recombination in DNA genomes. A heteroduplex joint is formed between a single-stranded region (or tail), derived from a cleaved parental double-stranded DNA, and homologous regions in another parental double-stranded DNA, in a reaction mediated by the RecA/Rad51-family of proteins. In this reaction, a RecA/Rad51-family protein first forms a filamentous complex with the single-stranded DNA, and then interacts with the double-stranded DNA in a search for homology. Studies of the three-dimensional structures of single-stranded DNA bound either to Escherichia coli RecA or Saccharomyces cerevisiae Rad51 have revealed a novel extended DNA structure. This structure contains a hydrophobic interaction between the 2′ methylene moiety of each deoxyribose and the aromatic ring of the following base, which allows bases to rotate horizontally through the interconversion of sugar puckers. This base rotation explains the mechanism of the homology search and base-pair switch between double-stranded and single-stranded DNA during the formation of heteroduplex joints. The pivotal role of the 2′ methylene-base interaction in the heteroduplex joint formation is supported by comparing the recombination of RNA genomes with that of DNA genomes. Some simple organisms with DNA genomes induce homologous recombination when they encounter conditions that are unfavorable for their survival. The extended DNA structure confers a dynamic property on the otherwise chemically and genetically stable double-stranded DNA, enabling gene segment rearrangements without disturbing the coding frame (i.e., protein-segment shuffling). These properties may give an extensive evolutionary advantage to DNA.

Original languageEnglish (US)
Pages (from-to)8425-8432
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume98
Issue number15
DOIs
StatePublished - Jul 17 2001
Externally publishedYes

Keywords

  • Base-pair switch
  • Homologous pairing
  • NMR
  • Strand exchange
  • Three-dimensional molecular structure

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