Arabidopsis SPO11‐2 functions with SPO11‐1 in meiotic recombination

Abstract

Summary: The Spo11 protein is a eukaryotic homologue of the archaeal DNA topoisomerase VIA subunit (topo VIA). In archaea it is involved, together with its B subunit (topo VIB), in DNA replication. However, most eukaryotes, including yeasts, insects and vertebrates, instead have a single gene for Spo11/topo VIA and no homologues for topo VIB. In these organisms, Spo11 mediates DNA double‐strand breaks that initiate meiotic recombination. Many plant species, in contrast to other eukaryotes, have three homologues for Spo11/topo VIA and one for topo VIB. The homologues in Arabidopsis, AtSPO11‐1, AtSPO11‐2 and AtSPO11‐3, all share 20–30% sequence similarity with other Spo11/topo VIA proteins, but their functional relationship during meiosis or other processes is not well understood. Previous genetic evidence suggests that AtSPO11‐1 is a true orthologue of Spo11 in other eukaryotes and is required for meiotic recombination, whereas AtSPO11‐3 is involved in DNA endo‐reduplication as a part of the topo VI complex. In this study, we show that plants homozygous for atspo11‐2 exhibit a severe sterility phenotype. Both male and female meiosis are severely disrupted in the atspo11‐2 mutant, and this is associated with severe defects in synapsis during the first meiotic division and reduced meiotic recombination. Further genetic analysis revealed that AtSPO11‐1 and AtSPO11‐2 genetically interact, i.e. plants heterozygous for both atspo11‐1 and atspo11‐2 are also sterile, suggesting that AtSPO11‐1 and AtSPO11‐2 have largely overlapping functions. Thus, the three Arabidopsis Spo11 homologues appear to function in two discrete processes, i.e. AtSPO11‐1 and AtSPO11‐2 in meiotic recombination and AtSPO11‐3 in DNA replication.