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The meiotic cohesin subunit REC8 contributes to multigenic adaptive evolution of autopolyploid meiosis in Arabidopsis arenosa [1]

['Chris Morgan', 'John Innes Centre', 'Norwich', 'United Kingdom', 'Emilie Knight', 'Kirsten Bomblies', 'Plant Evolutionary Genetics', 'Institute Of Plant Molecular Biology', 'Department Of Biology', 'Eth Zürich']

Date: 2022-09 

Genome duplication, which leads to polyploidy, poses challenges to the meiotic segregation of the now-multiple homologous chromosome copies. Genome scan data showed previously that adaptation to polyploid meiosis in autotetraploid Arabidopsis arenosa is likely multigenic, involving genes encoding interacting proteins. But what does this really mean? Functional follow-up studies to genome scans for multigenic traits remain rare in most systems, and thus many mysteries remain about the “functional architecture” of polygenic adaptations. Do different genes all contribute subtle and additive progression towards a fitness optimum, or are there more complex interactions? We previously showed that derived alleles of genes encoding two interacting meiotic axis proteins (ASY1 and ASY3) have additive functional consequences for meiotic adaptation. Here we study derived versus ancestral alleles of the meiotic cohesin subunit REC8, which has roles in chromatin condensation, recruiting the axes, and other critical functions in meiosis. We use genetic and cytological approaches to assess the functional effects of REC8 diploid versus tetraploid alleles, as well as their interaction with ancestral versus derived alleles of ASY1 and ASY3. We show that homozygotes for derived (tetraploid) REC8 alleles have significantly fewer unpaired univalents, a common problem in neotetraploids. Interactions with ASY1 and ASY3 are complex, with the genes in some cases affecting distinct traits, and additive or even antagonistic effects on others. These findings suggest that the road to meiotic adaptation in A. arenosa was perhaps neither straight nor smooth.

Genome duplication, which results in polyploidy, is fairly common in eukaryotes, especially plants, and has been linked to adaptation and speciation in nature, as well as increased yield and stress resilience in crops. Yet, newly formed polyploids face many challenges. To understand more fully how polyploids evolve and adapt, or to more efficiently utilize them in crop improvement, it is important that we learn what it really takes to be polyploid. As part of a longer-term effort to characterizing the multigenic adaptations to polyploid chromosome segregation, here we functionally characterize the effect in meiosis of ancestral versus derived alleles of one gene under selection in a polyploid, as well as its interactions with two other genes. The at-times complex interactions we discover provide insights into what seems to have been a sometimes-rocky path to multigenic adaptation.

Introduction

Our understanding of the genetic architecture of adaptation has benefitted greatly from improvements in whole genome sequencing, which have made it possible to undertake so-called “genome scans” for selection. This ability, in turn, opens the opportunity to study the genetic basis of adaptation from a “reverse genetics” perspective, where we start from identifying genes with signatures of selection, and use these to try to understand what traits they affect and why they might have been important in adaptation [1–3]. This reverse approach complements the forward phenotype-based approach, and has the potential to provide novel insights into the molecular basis of adaptation, especially for non-obvious, or multigenic traits. Nevertheless, challenges remain [4], and functional follow-up to test the effects of the genes with evidence of selection remain rare in most systems, especially for multigenic traits, which are particularly laborious and high-risk. We know from theory and empirical studies that multigenic adaptation should be common [5–9], a notion which genome scan data, including our own [10–12], generally support. However, while genome scans have already provided insights into the genetic architecture of multigenic adaptation, we know comparatively less about what can be thought of as the “functional architecture” of multigenic adaptation. How strong are the effects of individual loci when multiple loci are under selection? Do selected alleles act additively, synergistically, or even antagonistically? Do they have overlapping pleiotropic functions, or do they contribute independently to different aspects of adaptive traits?

Over the last decade, Arabidopsis arenosa has emerged as a model organism for studying the molecular basis of adaptation (e.g. [13,14]), among other things to whole genome duplication (WGD), which gives rise to polyploidy [10–12,15–17]. Genome scans to investigate adaptation to polyploidy have provided evidence that multiple genes encoding meiosis proteins are among the loci showing the strongest evidence of selection in the polyploid A. arenosa lineage [10–12,17]. This is hypothesized to reflect the fact that WGD poses a serious threat to fertility and genome integrity, by presenting novel challenges to chromosome pairing and segregation during meiosis [18–20].

The challenges polyploids face in meiotic segregation of the additional chromosome copies may be particularly acute in autopolyploids, which are formed from within-species WGD, and thus possess multiple, equally similar homologous copies of each chromosome [21,22]. During diploid meiosis, the formation of crossovers (COs) between pairs of homologous chromosomes is essential for promoting the stable segregation of homologs during anaphase I, as well as for introducing genetic diversity within offspring [23]. In most organisms, CO maturation is facilitated by formation of the meiotic axis and synaptonemal complex, proteinaceous structures that organise chromosomes into threadlike arrays of chromatin loops and synapse homologous axes together along their length, respectively [24,25]. In autopolyploids, due to the presence of more than two copies of each homolog, synapsis and subsequent CO formation can occur between multiple homologs simultaneously, creating linkages called multivalents. These structures are associated with an increased risk of chromosome mis-segregation and can lead to the formation of unbalanced, or even inviable gametes [20,22]. In a recent study, we found that polyploid meiotic stabilization is likely attributable, at least in part, to a strengthening of crossover interference or an increase in its efficiency of propagation along the chromosomes, which in turn helps reduce the number of multivalents and unpaired univalents [16]. We hypothesized that this could result from stiffening of axial element structures, which may explain why the meiotic axis proteins ASY1 and ASY3 show evidence of selection in A. arenosa autotetraploids [10,11]. We also found that established polyploids had shorter synaptonemal complexes and fewer crossovers than neopolyploids; likely all of these features function together to stabilize polyploid chromosome pairing and segregation [16].

The genome scans done for adaptation to WGD in A. arenosa demonstrated that at least eight essential meiosis genes are under strong selection in naturally established populations of autotetraploid A. arenosa, suggesting that meiotic adaptation in the polyploid lineage is an example of multigenic adaptation [10,11]. Of the multiple meiotic genes putatively under selection in the tetraploid, all are known to encode proteins that directly or indirectly interact, and are all known from mutant studies in other species to regulate related processes relevant to chromosome pairing and segregation that clearly represent challenges for polyploid meiosis. We already showed that derived alleles for genes encoding two meiotic axis proteins, ASY1 and ASY3 (homologs of Hop1 and Red1 in S. cerevisiae), affect multiple traits associated with tetraploid meiotic stability, such as reduced multivalent frequency and reduced axis length [15]. The derived alleles of ASY1 and ASY3 have primarily additive effects, though ASY1 has a generally stronger effect than ASY3 [15]. This additivity is perhaps unsurprising, given that ASY1 and ASY3 are directly-interacting critical components of the chromosome axis [26,27]. What the derived alleles of the remaining genes showing evidence of selection do, and whether or not they also contribute additively to the same phenotypes, remained untested.

In this study, we continue the task of understanding this multigenic adaptation by investigating the functional role of the derived (tetraploid-specific) allele of the meiotic cohesin subunit REC8 in the stabilisation of autotetraploid meiosis. This is motivated by the fact that REC8 is an essential component of meiosis known to affect relevant traits like axis assembly, axis / synaptonemal complex length and crossover frequency [16–19,28–31]. Moreover, REC8 is known to directly interact with the axis components and to recruit them to the chromosomes [32]. We also previously showed that REC8 might have been one of the oldest selective sweeps in tetraploid A. arenosa, likely predating selection on ASY3, and maybe even ASY1 [12]. This makes it especially interesting to understand its functional effects as it might have been a “frontline” player in the early adaptation of the polyploid lineage. We bred established tetraploid lines of A. arenosa that are homozygous for the ancestral, diploid alleles of REC8 in an otherwise tetraploid background. Since REC8 interacts with the axis proteins to ensure correct formation of the meiotic axis, we also studied the genetic interaction of derived alleles of REC8 with those of ASY1 and ASY3.

We find that one of the strongest associations with the derived, tetraploid allele of REC8 is a reduced frequency of undesirable metaphase I univalents, which neotetraploids have significantly more of than evolved tetraploids do [16]. Otherwise, we find generally subtle quantitative effects on several other meiotic traits. Interactions between the ancestral vs. derived alleles of REC8 with the ancestral vs. derived alleles of axis proteins are complex. Sometimes their effects are independent, whilst for other traits they are additive, and even sometimes antagonistic. Based on our findings, we propose a multi-step, multi-gene model that may explain the evolution of enhanced tetraploid meiotic stability in A. arenosa, in which the derived allele of REC8 may have been selected initially to reduce univalent frequency. The subsequent evolution of derived alleles at ASY1 and then ASY3 modified additional traits, including reducing multivalent rate, and have both additive and antagonistic interactions with the derived allele of REC8. We also recognize an alternate possibility, namely that REC8 may be under selection primarily to maintain interactions with other proteins that are evolving functional novelty.

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[1] Url: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010304

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