The synaptonemal complex imposes crossover interference and heterochiasmy inArabidopsis

Abstract

Meiotic crossovers (COs) have intriguing patterning properties, including CO interference, the tendency of COs to be well-spaced along chromosomes, and heterochiasmy, the marked difference in male and female CO rates. During meiosis, transverse filaments transiently associate the axes of homologous chromosomes, a process called synapsis that is essential for CO formation in many eukaryotes. Here, we describe the spatial organization of the transverse filaments in Arabidopsis (ZYP1) and show it to be evolutionary conserved. We show that in the absence of ZYP1 (zyp1a zyp1b null mutants), chromosomes associate in pairs but do not synapse. Unexpectedly, in absence of ZYP1, CO formation is not prevented but increased. Furthermore, genome-wide analysis of recombination revealed that CO interference is abolished, with the frequent observation of close COs. In addition, heterochiasmy was erased, with identical CO rates in males and females. This shows that the tripartite synaptonemal complex is dispensable for CO formation and has a key role in regulating their number and distribution, imposing CO interference and heterochiasmy.

Meiosis Progression and Recombination in Holocentric Plants: What Is Known?

“…For instance, in barley it was reported that dramatic reduction of normal levels of ZYP1 by RNAi also drastically reduce CO formation (Barakate et al, 2014). However, in the case of Arabidopsis and rice a malfunctioning SC does not affect recombination and may even increase CO frequency and abolish CO interference (Wang et al, 2010;Capilla-Perez et al, 2021;France et al, 2021). In both holocentric Rhynchospora and Luzula it was shown that they apparently have conserved SC structures as immunostaining with SC proteins showed the conserved pattern for monocentric species (Cabral et al, 2014;Heckmann et al, 2014).…”

From Microscopy to Nanoscopy: Defining an Arabidopsis thaliana Meiotic Atlas at the Nanometer Scale

“…proteins one important caveat needs to be taken into consideration: the measurements could yield deviating results depending on the primary antibody used for the analysis. This is because each primary antibody might recognize different epitopes of the same protein, and this can be resolved at a resolution of 30 nm, as shown in a recent publication (Capilla-Perez et al, 2021). Furthermore, an additional variation is added to the measurements if the combination of primary and secondary antibodies, which is roughly 30 nm long, is taken into account.…”

“…COs are formed in the context of the meiotic axes and the synaptonemal complex (SC) and physically link homologous chromosomes to enable correct segregation. The SC is a protein structure that builds on the axes, tightly connects homologous chromosomes and is required for inter-homolog recombination and interference ( Zickler and Kleckner, 1999 ; Kleckner, 2006 ; Mercier et al, 2015 ; Smith and Nambiar, 2020 ; Capilla-Perez et al, 2021 ; France et al, 2021 ). The repair of the residual breaks yields NCO products, possibly via synthesis-dependent strand-annealing, intersister recombination, or non-homologous end-joining ( Higgins et al, 2004 ; Chen et al, 2008 ; Mancera et al, 2008 ; Sims et al, 2019 ).…”

“…Meiocytes of plants lacking axis proteins, such as ASY1 and ASY3, never fully synapse ( Caryl et al, 2000 ; Ferdous et al, 2012 ) and full pachytene stages are also not observed in cohesion-deficient mutants like scc3 and rec8 ( Bai et al, 1999 ; Chelysheva et al, 2005 ). Similarly, complete synapsis is not observed when the transverse filament ZYP1 proteins are depleted or absent ( Higgins et al, 2005 ; Osman et al, 2006 ; Capilla-Perez et al, 2021 ; France et al, 2021 ). During wild-type pachytene (and up to diakinesis), ZMM proteins MSH4/5 and HEI10, as well as MLH1/3, localize to CO sites and form around 9–11 bright foci per nucleus, corresponding to the average number of chiasmata.…”

“…COs are formed in the context of the meiotic axes and the synaptonemal complex (SC) and physically link homologous chromosomes to enable correct segregation. The SC is a protein structure that builds on the axes, tightly connects homologous chromosomes and is required for inter-homolog recombination and interference (Zickler and Kleckner, 1999;Kleckner, 2006;Mercier et al, 2015;Smith and Nambiar, 2020;Capilla-Perez et al, 2021;France et al, 2021).…”