Meiosis is a specialized type of cell division that reduces chromosome number by half, resulting in the production of genetically diverse haploid gametes, so that fertilization during sexual reproduction restores diploidy. This process occurs in two stages: meiosis I, in which homologous chromosomes are partitioned, and meiosis II, in which sister chromatid are segregated. The regulation of meiosis is crucial for ensuring that both genetic recombination and chromosome segregation occur accurately. Errors in human meiosis are associated with birth defects, such as Down and Turner syndromes, infertility and miscarriages, underscoring the importance of understanding meiosis to human health (Hassold and Hunt, 2001).

During prophase I, homologous chromosomes pair and this pairing is stabilized through a process called synapsis, in which a protein structure called the synaptonemal complex (SC) holds homologs together. This close association between homologs during synapsis facilitates crossover formation, the process in which double-strand breaks (DSBs) are deliberately introduced into the genome, repaired by meiosis-specific mechanisms that exchange DNA between homologous chromosomes and generate the chiasmata, or linkage, that promotes accurate meiotic chromosome segregation. Therefore, disruptions in pairing, synapsis, or recombination prevents the formation of chiasmata and can lead to meiotic errors such as nondisjunction, resulting in aneuploid gametes.

In addition to the fundamental role that recombination plays in ensuring accurate chromosome segregation, crossover recombination accomplishes another important function: it generates new haplotypes for natural selection to act upon to drive evolution. Thus, to assure a random assortment of alleles on a population level, the distribution of crossovers may be as tightly regulated as their number (Veller et al., 2019). The significance of controlling both crossover number and distribution is clearly illustrated by the existence of mechanisms such as crossover assurance, in which every pair of homologous chromosomes gets at least one crossover; crossover homeostasis, in which the number of crossovers remains relatively invariant even if the number of recombination precursors change; and crossover interference, in which the presence of a crossover inhibits the formation of a crossover nearby (Gray and Cohen, 2016). DSBs typically vastly outnumber crossovers in most organisms and are introduced gradually throughout early prophase (Joshi et al., 2015; Woglar and Villeneuve, 2018). Therefore, to accomplish this precise level of control, meiotic crossover recombination and the decision about which DSBs become crossover-eligible intermediates, and eventually, which crossover-eligible intermediates get designated as crossovers, is implemented progressively throughout meiotic prophase (Cole et al., 2012; Joshi et al., 2015; Morgan et al., 2021; Yokoo et al., 2012). In many systems, transitions from DSBs to crossover-eligible intermediates, and crossover-eligible intermediates to crossovers, can be molecularly and/or cytologically monitored.

PCH-2, also known as TRIP13 in mammals, is an evolutionarily ancient AAA-ATPase that plays a significant role in regulating meiosis across different organisms, including Mus musculus (mice), Saccharomyces cerevisiae (budding yeast), Drosophila melanogaster (fruit flies), and Caenorhabditis elegans (worms) (Bhalla, 2023). PCH-2 and its orthologs structurally remodel a family of proteins with HORMA domains (HORMADs) to control their function (Gu et al., 2022). HORMADs participate in a variety of signaling events and can exist in at least three structurally distinct conformations: a ‘closed’ conformation, which they adopt when they bind a short peptide sequence in their own protein sequence or another protein (also called a closure motif) and their C-terminus wraps around this motif to stabilize the interaction; an ‘open’ conformation when unbound, in which their C-terminus is discretely tucked against the HORMA domain; and an ‘extended’ conformation, which is an intermediate between the two (Gu et al., 2022). PCH-2 and its orthologs convert the closed version of HORMADs to the open or extended versions, playing an important role in recycling HORMADs during signaling. During meiosis, closed versions of meiotic HORMADs assemble on chromosomes to form meiotic chromosome axes, which are essential for pairing, synapsis, and recombination between homologous chromosomes (Kim et al., 2014). The remodeling of meiotic HORMADs by PCH-2 to an ‘open’ or ‘extended’ conformation is thought to reduce the levels of HORMADs on chromosomes (Börner et al., 2008; Cuacos et al., 2021; Lambing et al., 2015; Wojtasz et al., 2009) and/or increase their dynamic association and dissociation (Russo et al., 2023), modulating and coordinating homolog pairing, synapsis and recombination during prophase.

Despite being discovered as a pachytene checkpoint component in 1999 (San-Segundo and Roeder, 1999), the conserved meiotic role of the PCH-2/HORMAD module has been difficult to characterize, in part, we have argued, because of the evolutionary innovation that is an inherent aspect of sexual reproduction (Bhalla, 2023). Moreover, in some systems, such as budding yeast and plants (Herruzo et al., 2021; Yang et al., 2020), PCH-2 orthologs not only remodel meiotic HORMADs on meiotic chromosomes but also perform this function in the cytoplasm to make meiotic HORMADs available for their role(s) in meiotic nuclei. This dual role can complicate functional analyses, particularly in pch-2 null mutants. However, all meiotic systems exhibit defects in the number and distribution of crossovers when PCH-2 function is abrogated by mutation (Deshong et al., 2014; Joshi et al., 2009; Joyce and McKim, 2009; Lambing et al., 2015; Roig et al., 2010; Zanders and Alani, 2009). Unfortunately, the lack of a clear pattern when analyzing these defects in recombination in pch-2 mutants has contributed to an inability to develop a unified, integrated model of PCH-2 function in the field.

In C. elegans, meiotic HORMADs localize to meiotic chromosomes independently of PCH-2 (Deshong et al., 2014). Moreover, the progressive implementation of meiotic recombination can be cytologically monitored in meiotic nuclei that are organized both spatially and temporally in the C. elegans germline (Woglar and Villeneuve, 2018; Yokoo et al., 2012). Here, we exploit this system to show that PCH-2 is required to control the number and distribution of crossovers by antagonizing their formation. This antagonism produces different consequences depending on the stage of meiotic prophase. In early meiotic prophase, PCH-2 inhibits DSBs from becoming crossover-eligible intermediates, ensuring that crossovers are more widely distributed than sites of initial DSB formation and/or homolog interactions. Later in meiotic prophase, PCH-2 is responsible for winnowing the numbers of crossover-eligible intermediates on synapsed chromosomes, contributing to the designation of crossovers and ultimately, crossover assurance. Genetic analysis demonstrates that PCH-2’s regulation of crossover-eligible intermediates is through one of three essential meiotic HORMADs, HIM-3. Finally, we link PCH-2’s effect on early DSBs in early meiotic prophase to cell cycle stage, demonstrating that both limit early DSBs from becoming crossovers. We propose that PCH-2’s remodeling of HIM-3 on meiotic chromosomes destabilizes crossover-eligible intermediates throughout meiotic prophase, contributing to the progressive implementation of meiotic recombination to control the number and distribution of crossovers, also known as crossover control.

We have shown that PCH-2 antagonizes crossover formation throughout meiotic prophase (Figures 2—4) and that this regulation occurs through one of the three essential meiotic HORMADs in C. elegans, HIM-3 (Figure 4). We propose that PCH-2 remodels HIM-3 on meiotic chromosomes to destabilize crossover-eligible intermediates, visualized in our experiments as GFP-MSH-5 foci, thus limiting which DSBs will become crossovers (Figure 7). However, this antagonism has different consequences depending on when during meiotic prophase it occurs, underscoring the importance of temporal regulation of these events. During leptotene/zygotene, when CHK-2 activity is high (Kim et al., 2015; Zhang et al., 2023) and PCH-2 is present as foci on chromosomes (Deshong et al., 2014), PCH-2 prevents crossover formation at some sites of initial DSB formation and early homolog interactions (Figure 7B). In this way, PCH-2 promotes a wider distribution of crossovers across the genome (Figure 1). In pachytene, when CHK-2 activity has decreased (Kim et al., 2015; Zhang et al., 2023) and PCH-2 is localized to the SC (Deshong et al., 2014), PCH-2 winnows crossover-eligible intermediates marked by GFP-MSH-5, ensuring their designation, colocalization with COSA-1 and crossover assurance (Figure 7B). When there are defects in recombination, such as partial synapsis (Deshong et al., 2014), changes in karyotype (Patel et al., 2023), or too few DSBs (Figure 5), PCH-2 persists on the SC to prevent designation, guarantee crossover assurance and some degree of homeostasis, independent of an additional feedback mechanism that increases DSB formation (Patel et al., 2023). That persistence of PCH-2 also disrupts crossover interference in two of these situations (Deshong et al., 2014; Patel et al., 2023) strongly suggests that crossover interference is mechanistically linked to assurance and homeostasis. For example, PCH-2’s persistence on the SC may maintain an extended period of competency for interhomolog repair, as has been observed in mutants defective in crossover recombination (Rosu et al., 2011).

Figure 7

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him-3^R93Y;pch-2 double mutants have stronger crossover assurance than either single mutant but less than wildtype animals (Russo et al., 2023), a phenotype which can now be explained by the behavior of GFP::MSH-5 foci in these double mutants (Figure 4C and D). We have shown that HIM-3^R93Y mutant protein can adopt the closed conformation and loads on meiotic chromosomes similar to wildtype HIM-3 (Russo et al., 2023). In vitro analysis shows that HIM-3^R93Y binds its closure motif with reduced affinity, likely affecting its ability to adopt the closed conformation in vivo (Figure 7A; Russo et al., 2023). The proposed role of PCH-2 in meiosis is to remodel meiotic HORMADs from the closed conformation to the extended one (Figure 7A), regulating their association with chromosomes (Bhalla, 2023). However, since meiotic HORMADs are not visibly depleted from chromosomes during meiotic progression in C. elegans (Couteau et al., 2004; Couteau and Zetka, 2005; Goodyer et al., 2008; Martinez-Perez and Villeneuve, 2005), this genetic interaction supports a role for PCH-2 in temporarily reducing the occupancy of meiotic HORMADs on meiotic chromosomes, destabilizing interactions with partner proteins that modulate the progression and fidelity of meiotic recombination (Russo et al., 2023). Thus, PCH-2’s remodeling of HIM-3 would disrupt protein–protein interactions that underlie crossover-eligible intermediates, destabilizing them and reducing their number on chromosomes, contributing to crossover control (Figure 7B). Since meiotic HORMADs are essential for meiotic chromosome axis structure and function, our data therefore support a role for the meiotic axis in crossover control, as suggested by previous reports (Chu et al., 2024; Girard et al., 2023; Lambing et al., 2020; Nabeshima et al., 2004). However, the disassembly of crossover-eligible intermediates would also release pro-crossover factors present at these sites, such as MSH-5, to concentrate at other, more stable sites on the SC, facilitating designation during synapsis (Girard et al., 2023; Yokoo et al., 2012). In this way, PCH-2’s mechanism of action may reconcile current competing models of crossover control (Girard et al., 2023). Moreover, these results raise the possibility that this behavior of PCH-2 and/or meiotic HORMADs might be regulated by post-translational modifications associated with crossover control, such as ubiquitination, SUMOylation, and phosphorylation (Gray and Cohen, 2016).

Given that mutation of PCH-2 produces changes in the number and distribution of crossovers across multiple model systems, we argue that controlling crossover distribution and number is the conserved role of PCH-2 in meiosis (Bhalla, 2023). We have previously proposed that the conserved role of PCH-2 is to coordinate meiotic recombination with synapsis, explaining its role in the pachytene checkpoint (Bhalla, 2023). With these results, we further refine this model. Early in meiotic prophase, PCH-2 remodels meiotic HORMADs to prevent some DSBs from becoming crossover-eligible intermediates, widening the recombination landscape beyond early homolog interactions and/or sites that tend to be more favorable for DSB formation, also known as ‘hot spots’. For example, this may explain the localization of TRIP13, the PCH-2 ortholog in mice, to telomeres (Chotiner et al., 2024), sites that experience early homolog interactions due to the organization of meiotic chromosomes in the bouquet formation (Scherthan et al., 1996). This antagonism may also expand the regions of the genome that initiate synapsis in organisms that use DSBs to accomplish this event. This possibility is supported by the observation that loss of TRIP13 in mammals produce meiotic chromosomes that exhibit partial asynapsis (Roig et al., 2010), particularly near regions that may act as barriers to SC polymerization (Brown et al., 2005; Roig et al., 2010). Limiting which DSBs become crossover-eligible intermediates in early meiotic prophase also ensures that meiotic recombination overlaps with synapsis, either completely, as in C. elegans (Yokoo et al., 2012) or partially, as in budding yeast, plants and mice (Capilla-Pérez et al., 2021; Cole et al., 2012; Joshi et al., 2015; Morgan et al., 2021). Once synapsis is complete, PCH-2 continues to remodel meiotic HORMADs on chromosomes to control the gradual implementation of crossover number and distribution, reinforcing the important role that synapsis plays in mediating crossover control (Durand et al., 2022; Libuda et al., 2013).

Unexpectedly, the inability to reduce the number of crossover-eligible intermediates in pch-2 mutants, as visualized by GFP::MSH-5 foci, does not produce extra crossovers but a loss of crossover assurance in C. elegans (Figure 4), a somewhat counterintuitive result. One interpretation of these data is that crossover-eligible intermediates may be more numerous but absent from some chromosomes in pch-2 mutants, explaining the loss of crossover assurance. Since the absence of crossover intermediates in C. elegans is accompanied by premature desynapsis of individual chromosomes (Machovina et al., 2016; Pattabiraman et al., 2017) and chromosomes in pch-2 mutants delay desynapsis (Deshong et al., 2014), we do not favor this interpretation. Instead, we propose that having too many crossover-eligible intermediates can be as deleterious to crossover assurance as having too few (Figure 7B). This possibility is further supported by the loss of crossover assurance we detect in irradiated wildtype worms, which is exacerbated in pch-2 mutants (Figure 2).

This phenomenon, where crossover-eligible intermediates need to be winnowed to some threshold number to ensure crossover assurance, may explain the loss of crossover assurance also observed in Trip13-deficient mice (Roig et al., 2010) and on small chromosomes in budding yeast (Chakraborty et al., 2017). Alternatively, the counterintuitive relationship between the number of crossover-eligible precursors and crossover assurance in pch-2 mutants we observe might reflect an additional layer of regulation during crossover formation specific to C. elegans. Since C. elegans chromosomes are holocentric, crossovers play an additional role organizing chromosomes for the ordered release of sister chromatid cohesion during meiosis I (Martinez-Perez et al., 2008; Nabeshima et al., 2005) and extra crossovers can be deleterious to accurate chromosome segregation (Hollis et al., 2020). By contrast, in Arabidopsis, a system that appears to be able to tolerate an extraordinarily high number of crossovers with little to no effect on chromosome segregation (Durand et al., 2022), PCH2’s inability to localize to the SC produces an increase in crossover formation, as visualized by both MLH1 foci and the formation of chiasmata (Yang et al., 2022). Once again, an overarching theme that becomes apparent in our model is that PCH-2 may play a common role in different systems, with dramatic variations in phenotypic consequences given species-specific requirements and constraints.

We were not surprised to see high numbers of double crossovers on almost every chromosome in our genetic analysis of recombination in wildtype worms, given our previous analysis (Deshong et al., 2014). However, we were surprised to see that the majority of them were found near PCs and sites of synapsis initiation, suggesting a relationship between early homolog interactions and the formation of double crossovers. When we revisited our previous data, we observed similar patterns. In addition, we do not detect these double crossovers cytologically in C. elegans, even when using the OLLAS::COSA-1 reporter, which has been reported to identify double crossovers in spermatogenesis not visualized by GFP::COSA-1 (Cahoon et al., 2023). Crossovers that are cytologically marked by COSA-1 are known as class I crossovers, which depend on pro-crossover factors such as MSH-5 and ZHP-3, rely on synapsis, and exhibit crossover control (Gray and Cohen, 2016). These data raise the intriguing possibility that these double crossovers are the product of the alternate, class II, pathway of crossover formation, which relies on a different suite of proteins, does not respond to crossover control, does not depend on synapsis, and contributes to varying degrees in different model systems (Gray and Cohen, 2016; Youds et al., 2010). Thus, based on the close, functional relationship that exists between class I crossovers and synapsis and the apparent antagonistic relationship that exists between class II crossovers and synapsis, important corollaries of our model may be that PCH-2 specifically coordinates recombination with synapsis to promote class I crossovers, limit class II crossovers and that class II crossovers are more likely to form early in meiosis, prior to synapsis. Therefore, variations in the contribution of the class II crossover pathways to crossover recombination and the degree of cross-talk between class I and II pathways among model systems might reflect the degree to which crossover formation overlaps with synapsis (Bhalla, 2023; Gray and Cohen, 2016; Yokoo et al., 2012). Furthermore, these corollaries are entirely consistent with PCH-2’s absence from the genome of fission yeast and Tetrahymena (Kops et al., 2020; Wu and Burgess, 2006), both systems in which chromosomes do not undergo meiotic synapsis, crossovers do not exhibit interference and all crossovers are dependent on the class II pathway (Hollingsworth and Brill, 2004; Lukaszewicz et al., 2013; Wolfe et al., 1976). However, this aspect of the model needs to be formally tested.

Our results also have some additional important implications about the regulation of DSB formation across the genome in C. elegans. It is formally possible that PCH-2 controls DSB distribution. However, the complexity of recombination defects in pch-2 mutants argues against this possibility. Instead, we explain the shift in the recombination landscape away from the central regions of chromosomes and toward PC ends in pch-2 mutants (Figure 1) as a result of early DSBs becoming crossovers at the expense of later DSBs. This explanation is better supported by the panel of defects observed in pch-2 mutants: DSBs introduced early in meiosis become crossover eligible intermediates and crossovers (Figures 2—4) and while the number of DSBs is constant, DNA repair is accelerated (Deshong et al., 2014). Moreover, this explanation suggests that when DSBs happen in meiotic prophase affects where they happen in the genome. Specifically, we propose that chromosome arms, which are gene poor, receive DSBs early during (or even throughout) DSB formation and the center of chromosomes, which are gene rich, receive DSBs later. The shift in recombination to the center of chromosomes when defects in meiosis prolong DSB formation provides further support to this possibility (Carlton et al., 2006; Deshong et al., 2014). A similar regulation of the timing of DSB formation has been demonstrated in budding yeast, where the DSB landscape across the whole genome expands when time in prophase is increased (López Ruiz et al., 2024) and small, highly recombinogenic, chromosomes, get more DSBs later in meiotic prophase (Murakami et al., 2020; Subramanian et al., 2019). However, this temporal regulation has not been reported previously in C. elegans and suggests that this phenomenon is more widely conserved. This expansion of the DSB landscape in C. elegans to include the center regions of chromosomes later in meiosis may be a deliberate attempt for recombination to create new haplotypes for evolution to act on, despite the relative paucity of DSBs and the observation that they can result in chromosome missegregation (Altendorfer et al., 2020).

Finally, our work raises some important questions about the functional role(s) of DSBs in meiosis, aside from their contributions to crossover formation. Hicks and colleagues were the first to report that early DSBs do not contribute to crossover formation in C. elegans (Hicks et al., 2022). Here we show that these early DSBs are prevented from becoming crossovers by both PCH-2 activity and cell cycle stage, specifically in leptotene/zygotene, when homologs are initiating pairing and synapsis. In budding yeast, similar, early-occurring DSBs have been characterized as ‘scout DSBs’ because of their preference for repair from sister chromatids, versus homologous chromosomes, and their proposed role in contributing to homolog pairing (Borde and de Massy, 2015; Joshi et al., 2015). The homolog bias that these ‘scout DSBs’ do display seems dependent on budding yeast PCH2 (Joshi et al., 2015) but interpreting this experiment is complicated by the fact that Pch2 is also required to make the budding yeast meiotic HORMAD, Hop1, available for its loading onto meiotic chromosomes (Herruzo et al., 2021).

In contrast to budding yeast, C. elegans does not rely on DSBs to promote homolog pairing and initiate synapsis (Dernburg et al., 1998); in worms, cis-acting sites called PCs are essential for homolog pairing and synapsis (MacQueen et al., 2005). There is certainly some support in the literature for DSBs playing a role in supporting pairing and synapsis in C. elegans (Guo et al., 2022; Mlynarczyk-Evans et al., 2013; Roelens et al., 2015). However, if these early DSBs were contributing to pairing and synapsis, we would expect to see a genetic interaction between htp-3^H96Y and pch-2 mutations in the installation of GFP::MSH-5 in the transition zone; we previously reported that htp-3^H96Y suppresses the acceleration of pairing and synapsis of pch-2 mutants, particularly when PC function is compromised (Russo et al., 2023). Instead, we favor the possibility that these early DSBs are generated to amplify the signaling of DNA damage kinases to prime them for their role in recombination, a role that has also been proposed for ‘scout’ DSBs (Joshi et al., 2015). That ATM-1, a conserved DNA damage kinase that is downstream of CHK-2 in C. elegans, relies on DSBs for full activity, supports this proposed, conserved role (Yu et al., 2023).

Our work provides an important framework to finally understand the role of PCH-2 in controlling the number and distribution of crossovers, a role that we argue is its conserved role. While specific details may vary across systems, we propose that PCH-2 remodels meiotic HORMADs throughout meiotic prophase to destabilize crossover-eligible precursors, coordinating meiotic recombination with synapsis, contributing to the progressive implementation of meiotic recombination, guaranteeing crossover assurance, interference and homeostasis, and explaining its function as a pachytene checkpoint component.

The numerical data used to generate each figure is provided.

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Author details

1. Bhumil Patel

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

2. Maryke Grobler

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Conceptualization, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

3. Alberto Herrera

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Data curation, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

4. Elias Logari

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Data curation, Investigation

   Competing interests

   No competing interests declared

5. Valery Ortiz

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

6. Needhi Bhalla

   Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, United States

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   nbhalla@ucsc.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6859-0073

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