The Arabidopsis HEI10 Is a New ZMM Protein Related to Zip3

Abstract

In numerous species, the formation of meiotic crossovers is largely under the control of a group of proteins known as ZMM. Here, we identified a new ZMM protein, HEI10, a RING finger-containing protein that is well conserved among species. We show that HEI10 is structurally and functionally related to the yeast Zip3 ZMM and that it is absolutely required for class I crossover (CO) formation in Arabidopsis thaliana. Furthermore, we show that it is present as numerous foci on the chromosome axes and the synaptonemal complex central element until pachytene. Then, from pachytene to diakinesis, HEI10 is retained at a limited number of sites that correspond to class I COs, where it co-localises with MLH1. Assuming that HEI10 early staining represents an early selection of recombination intermediates to be channelled into the ZMM pathway, HEI10 would therefore draw a continuity between early chosen recombination intermediates and final class I COs.

Author Summary

During meiosis two successive chromosomal divisions follow a single S phase, resulting in the formation of four haploid cells, each with half of the parental genetic material. This ploidy reduction occurs during the first meiotic division, when homologous chromosomes (paternal and maternal) are separated from each other. For this to happen, homologous chromosomes associate in bivalents, where each chromosome is linked to its homologue by chiasmata. These chiasmata reflect the formation of crossovers (COs), one of the manifestations of the exchange of genetic material occurring during homologous recombination. In most species, the final number of COs represents only a small proportion of all meiotic recombination events (4% in Arabidopsis thaliana). The mechanisms that drive the choice of recombination intermediates that will mature into COs are still unknown. In this study, we identified the HEI10 protein that is present as numerous foci on chromosome axes during early meiotic prophase and is retained until the end of prophase at a limited number of sites corresponding to COs. We also showed that HEI10 is necessary for the formation of most of the COs. HEI10 is therefore a good candidate for a ZMM protein involved in generating continuity between chosen early recombination intermediates and final COs.