Repair of DNA double-strand breaks in plant meiosis: role of eukaryotic RecA recombinases and their modulators

Abstract

Homologous recombination (HR) during meiosis is crucial for the DNA double-strand breaks (DSBs) repair that promotes the balanced segregation of homologous chromosomes and enhances genetic variation. In most eukaryotes, two recombinases RAD51 and DMC1 form nucleoprotein filaments on single-stranded DNA generated at DSB sites and play a central role in the meiotic DSB repair and genome stability. These nucleoprotein filaments perform homology search and DNA strand exchange to initiate repair using homologous template-directed sequences located elsewhere in the genome. Multiple factors can regulate the assembly, stability, and disassembly of RAD51 and DMC1 nucleoprotein filaments. In this review, we summarize the current understanding of the meiotic functions of RAD51 and DMC1 and the role of their positive and negative modulators. We discuss the current models and regulators of homology searches and strand exchange conserved during plant meiosis. Manipulation of these repair factors during plant meiosis also holds a great potential to accelerate plant breeding for crop improvements and productivity.

DMC1 attenuates RAD51-mediated recombination in Arabidopsis

“…However, more recent work in budding yeast and mouse suggested that RAD51 and DMC1 homofilaments do load on both DSB ends resulting in mixed recombinase filaments [21–23]. This mixed recombinase filament organization has been reconstituted in vitro [24] and has thus become the favored model for recombinase loading [16, 17, 23–27]. The RAD51/DMC1-DNA nucleoprotein filament is the active molecular species in searching for and invading a homologous DNA template by the 3’-ended DNA strand(s) [16, 17, 26, 27].…”

“…This mixed recombinase filament organization has been reconstituted in vitro [24] and has thus become the favored model for recombinase loading [16,17,[23][24][25][26][27]. The RAD51/DMC1-DNA nucleoprotein filament is the active molecular species in searching for and invading a homologous DNA template by the 3'-ended DNA strand(s) [16,17,26,27].…”

“…This mixed recombinase filament organization has been reconstituted in vitro [24] and has thus become the favored model for recombinase loading [16,17,[23][24][25][26][27]. The RAD51/DMC1-DNA nucleoprotein filament is the active molecular species in searching for and invading a homologous DNA template by the 3'-ended DNA strand(s) [16,17,26,27]. This process is the core of the meiotic recombination pathway and results in the formation of a joint recombination intermediate, which can be resolved to yield non-crossover (NCO) or crossover (CO) products [1,2,28].…”

“…The pair of DNA ends formed are resected by nucleases [12], which remove SPO11 and generate long 3 single-stranded DNA overhangs (ssDNA), which are bound by the heterotrimeric protein RPA to protect the ssDNA and prevent formation of secondary structures [13][14][15]. The specialized RAD51 and DMC1 recombinases are then loaded onto the ssDNA to form right-handed helical nucleoprotein filaments [16,17]. Earlier studies have proposed that recombinase loading occurs asymmetrically, with RAD51 and DMC1 making separate homofilaments on opposite ends of a break [18][19][20].…”

“…The copyright holder for this preprint (which this version posted July 5, 2022. ; https://doi.org/10.1101/2022.07.05.498790 doi: bioRxiv preprint vitro [24] and has thus become the favored model for recombinase loading [16,17,[23][24][25][26][27].…”