Analysis of the impact of the absence of RAD51 strand exchange activity in Arabidopsis meiosis

PLoS One. 2017 Aug 10;12(8):e0183006. doi: 10.1371/journal.pone.0183006. eCollection 2017.

Abstract

The ploidy of eukaryote gametes must be halved to avoid doubling of numbers of chromosomes with each generation and this is carried out by meiosis, a specialized cell division in which a single chromosomal replication phase is followed by two successive nuclear divisions. With some exceptions, programmed recombination ensures the proper pairing and distribution of homologous pairs of chromosomes in meiosis and recombination defects thus lead to sterility. Two highly related recombinases are required to catalyse the key strand-invasion step of meiotic recombination and it is the meiosis-specific DMC1 which is generally believed to catalyse the essential non-sister chromatid crossing-over, with RAD51 catalysing sister-chromatid and non-cross-over events. Recent work in yeast and plants has however shown that in the absence of RAD51 strand-exchange activity, DMC1 is able to repair all meiotic DNA breaks and surprisingly, that this does not appear to affect numbers of meiotic cross-overs. In this work we confirm and extend this conclusion. Given that more than 95% of meiotic homologous recombination in Arabidopsis does not result in inter-homologue crossovers, Arabidopsis is a particularly sensitive model for testing the relative importance of the two proteins-even minor effects on the non-crossover event population should produce detectable effects on crossing-over. Although the presence of RAD51 protein provides essential support for the action of DMC1, our results show no significant effect of the absence of RAD51 strand-exchange activity on meiotic crossing-over rates or patterns in different chromosomal regions or across the whole genome of Arabidopsis, strongly supporting the argument that DMC1 catalyses repair of all meiotic DNA breaks, not only non-sister cross-overs.

MeSH terms

  • Arabidopsis / cytology*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chromatids / genetics
  • Chromatids / metabolism
  • DNA Breaks*
  • DNA Repair
  • Homologous Recombination
  • Meiosis
  • Rad51 Recombinase / genetics
  • Rad51 Recombinase / metabolism*
  • Recombination, Genetic

Substances

  • Arabidopsis Proteins
  • Rad51 Recombinase

Grants and funding

This work was funded by the European Commission Marie-Sklodowska Actions (FP7-PEOPLE-2013-ITN. COMREC. 606956), the Centre National de la Recherche Scientifique, Institut National de la Sante et de la Recherche Medicale, and the Universite Clermont Auvergne. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.