Meiotic chromosome axis remodelling is critical for meiotic recombination inBrassica rapa

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 on 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 to WT. 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 programs.

The proteome of developing barley anthers during meiotic prophase I

“…The main role of Replication Protein A2A (RPA2A), DNA replication licensing factor MCM7, and Replication Factor C5 (RFC) is the DNA replication preceding meiosis I ( Elmayan et al , 2005 ; Evrin et al , 2009 ; Xia et al , 2010 ) while RADiation-sensitive52 (RAD52) initiates homologous recombination ( Samach et al , 2011 ) and ATP-dependent DNA helicase 2 subunit KU80 is involved in the non-homologous DNA end joining (NHEJ) necessary for double-strand break repair ( West et al , 2002 ). HvASY1 abundance in our experiment was unique ( Figs 1 , 3B ) and consistent with the published studies showing high ASY1 dynamics and implication in multiple meiotic processes including synapsis, axis morphogenesis, and coordinating the activity of other members of the homologous recombination machinery ( Armstrong et al , 2002 ; Nonomura et al , 2004 ; Sanchez-Moran et al , 2007 ; Cuacos et al , 2021 ).…”

Bipartite recruitment of PCH2 and COMET to the synaptonemal complex drives chromosome axis reconstruction leading to crossover restriction

“…The finding that the incomplete removal of ASY1 does not necessarily lead to compromised chromosome coalignment/synapsis and chromosome missegregation as seen in pch2 mutants (Lambing et al , 2015; Cuacos et al , 2021) indicates that the meiotic defects of pch2 mutants are not only due to a defective release of ASY1. However, the meiotic defects of pch2 mutants still appear to be largely related to ASY1 since PCH2 is also required for the efficient nuclear targeting of ASY1 in early prophase and hence promotes meiotic recombination and synapsis (Yang et al , 2020a; Cuacos et al , 2021).…”

The conserved AAA-ATPase PCH-2 distributes its regulation of meiotic prophase events by remodeling multiple meiotic HORMADs inC. elegans

“…First, PCH-2’s orthologs localize to sites associated with synapsis initiation and recombination in budding yeast and plants (Joshi et al, 2009; Lambing et al, 2015), suggesting a role at these sites. Further, despite PCH-2’s depletion or redistribution of meiotic HORMADs from chromosomes upon synapsis in some systems, meiotic HORMADs are not completely removed (Borner et al, 2008; Cuacos et al, 2021; Lambing et al, 2015; Wojtasz et al, 2009), suggesting roles for both meiotic HORMADs and PCH-2 even when chromosomes are synapsed. Given that the gradual implementation of crossover formation partially overlaps with when chromosomes are synapsed in budding yeast, plants and mice (Capilla-Perez et al, 2021; Cole et al, 2012; Joshi, Brown, Bishop, & Borner, 2015; Morgan et al, 2021), we propose that PCH-2’s presence on synapsed chromosomes contributes to controlling the number and location of crossovers, as observed in C. elegans (Deshong et al, 2014).…”

“…However, meiotic HORMADs are not removed from chromosomes upon synapsis in all systems, such as in C. elegans (Couteau et al, 2004; Couteau & Zetka, 2005; Goodyer et al, 2008; Martinez-Perez & Villeneuve, 2005). Further, PCH-2 and its orthologs localize to meiotic chromosomes prior to synapsis in budding yeast, plants and C. elegans (Cuacos et al, 2021; Deshong et al, 2014; Joshi et al, 2009; Lambing et al, 2015; San-Segundo & Roeder, 1999). These data raise the important question of whether remodeling of meiotic HORMADs plays additional roles during meiotic prophase.…”