Meiotic chromosome axis remodelling is critical for meiotic recombination in Brassica rapa.

Maria Cuacos,F Christopher H Franklin,Eugenio Sanchez-Moran,Stefan Heckmann,Miguel Pachon-Penalba,Christophe Lambing,Susan J Armstrong,Ian R Henderson,Kim Osman

doi:10.1093/jxb/erab035

Abstract

Meiosis generates genetic variation through homologous recombination (HR) that is harnessed during breeding. HR occurs in the context of meiotic chromosome axes and the synaptonemal complex. To study the role of axis remodelling in crossover (CO) formation in a crop species, we characterized mutants of the axis-associated protein ASY1 and the axis-remodelling protein PCH2 in Brassica rapa. asy1 plants form meiotic chromosome axes that fail to synapse. CO formation is almost abolished, and residual chiasmata are proportionally enriched in terminal chromosome regions, particularly in the nucleolar organizing region (NOR)-carrying chromosome arm. pch2 plants show impaired ASY1 loading and remodelling, consequently achieving only partial synapsis, which leads to reduced CO formation and loss of the obligatory CO. PCH2-independent chiasmata are proportionally enriched towards distal chromosome regions. Similarly, in Arabidopsis pch2, COs are increased towards telomeric regions at the expense of (peri-) centromeric COs compared with the wild type. Taken together, in B. rapa, axis formation and remodelling are critical for meiotic fidelity including synapsis and CO formation, and in asy1 and pch2 CO distributions are altered. While asy1 plants are sterile, pch2 plants are semi-sterile and thus PCH2 could be an interesting target for breeding programmes.

Highlights

Meiosis is a specialized cell division in sexually reproducing organisms shuffling maternal and paternal genomes through homologous recombination (HR) and independent assortment of homologous chromosomes.HR is initiated by programmed formation of SPO11catalysed DNA double-strand breaks (DSBs) (Keeney and Kleckner, 1995; Keeney et al, 1997; Neale et al, 2005; Pan et al, 2011)
CO formation is almost abolished, and residual chiasmata are proportionally enriched in terminal chromosome regions, in the nucleolar organizing region (NOR)-carrying chromosome arm. pch2 plants show impaired ASY1 loading and remodelling, achieving only partial synapsis, which leads to reduced CO formation and loss of the obligatory CO
We found that chiasma frequency in pch2 did not significantly deviate from a Poisson-predicted distribution [χ 2(pch2-9)=14.70, P=0.26, n=98)] (Fig. 5), revealing a random distribution of chiasmata between cells.To identify whether interference-sensitive class I COs form in pch2, we performed immunolocalization of HEI10 together with ZYP1 (Fig. 6B)

Summary

Introduction

Meiosis is a specialized cell division in sexually reproducing organisms shuffling maternal and paternal genomes through homologous recombination (HR) and independent assortment of homologous chromosomes. HR is initiated by programmed formation of SPO11catalysed DNA double-strand breaks (DSBs) (Keeney and Kleckner, 1995; Keeney et al, 1997; Neale et al, 2005; Pan et al, 2011). DSBs undergo a series of transitions, being. COs are restricted to chromosome ends, inhibiting access to traits residing in ‘cold’ regions or creating ‘linkage drag’; modulating CO number and distribution is of interest for plant breeding (Phillips et al, 2013; Choulet et al, 2014; Li et al, 2015; Demirci et al, 2017; Lambing and Heckmann, 2018; Dreissig et al, 2019)

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Conclusion