The E3 ubiquitin ligase DESYNAPSIS1 regulates synapsis and recombination in rice meiosis.

Lijun Ren,Yi Shen,Ding Tang,Na Mu,Yafei Li,Yangzi Zhao,Tingting Zhao,Guijie Du,Zhukuan Cheng,Shuying Yang

doi:10.1016/j.celrep.2021.109941

Abstract

Synaptonemal complex (SC) assembly and homologous recombination, the most critical events during prophase I, are the prerequisite for faithful meiotic chromosome segregation. However, the underlying regulatory mechanism remains largely unknown. Here, we reveal that a functional RING finger E3 ubiquitin ligase, DESYNAPSIS1 (DSNP1), plays significant roles in SC assembly and homologous recombination during rice meiosis. In the dsnp1 mutant, homologous synapsis is discontinuous and aberrant SC-like polycomplexes occur independent of coaligned homologous chromosomes. Accompanying the decreased foci of HEI10, ZIP4, and MER3 on meiotic chromosomes, the number of crossovers (COs) decreases dramatically in dsnp1 meiocytes. Furthermore, the absence of central elements largely restores the localization of non-ZEP1 ZMM proteins and the number of COs in the dsnp1 background. Collectively, DSNP1 stabilizes the canonical tripartite SC structure along paired homologous chromosomes and further promotes the formation of COs.

Highlights

Meiosis consists of two successive cell divisions following a single round of DNA replication, which achieves the generation of haploid gametes from diploid parental cells during sexual reproduction
Map-based cloning and characterization of DSNP1 To identify genes involved in meiosis, a set of rice sterile mutants were identified from the self-fertilized progeny of 60Co g-radiation-treated Guangluai 4, an indica rice variety
Since homologous pairing was impaired in dsnp1 meiocytes, we investigated the number of gH2AX foci to explore whether DSB formation was affected in the mutant

Summary

Introduction

Meiosis consists of two successive cell divisions following a single round of DNA replication, which achieves the generation of haploid gametes from diploid parental cells during sexual reproduction. SPO11, and its accessory proteins catalyze the formation of programmed DSBs, which is a prerequisite for homologous recombination in meiosis (Borde and Lichten, 2014). The DSB ends are resected and further processed by several nucleases and helicases to generate extended 30 single-strand DNA (ssDNA) overhangs (Symington, 2016). These exposed ssDNAs are successively coated by replication protein A (RPA) and loaded by two conserved recombinases RAD51 and DMC1 to form nucleofilaments, which are responsible for homology search and the formation of double Holliday junction (dHJ) (Marini et al, 2019). To maintain physical links between homologous chromosomes during metaphase I, the obligatory COs are guaranteed by a group of proteins referred to as ZMM (ZIP1, ZIP2, ZIP3, ZIP4, MSH4, MSH5, and MER3) (Lynn et al, 2007)

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Conclusion