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Polyploidization is frequently associated with increased transposable element (TE) content. However, what drives TE dynamics following whole genome duplication (WGD) and the evolutionary implications remain unclear. Here, we leverage whole-genome resequencing data available for ~300 individuals of Arabidopsis arenosa , a well characterized natural diploid-autotetraploid plant species, to address these questions. Based on 43,176 TE insertions we detect in these genomes, we demonstrate that relaxed purifying selection rather than transposition bursts is the main driver of TE over-accumulation after WGD. Furthermore, the increased pool of TE insertions in tetraploids is especially enriched within or near environmentally responsive genes. Notably, we show that the major flowering-time repressor gene FLC is disrupted by a TE insertion specifically in the rapid-cycling tetraploid lineage that colonized mainland railways. Together, our findings indicate that tetrasomy leads to an enhanced accumulation of genic TE insertions, some of which likely contribute to local adaptation. Why transposable elements (TEs) accumulate in polyploids and the evolutionary implications remain unclear. Here, the authors show that following whole genome duplication, relaxed purifying selection is the main driver of TE over-accumulation, which provides variants for rapid local adaptation.

In most organisms, the number and distribution of crossovers that occur during meiosis are tightly controlled. All chromosomes must receive at least one ‘obligatory crossover’ and crossovers are prevented from occurring near one another by ‘crossover interference’. However, the mechanistic basis of this phenomenon of crossover interference has remained mostly mysterious. Using quantitative super-resolution cytogenetics and mathematical modelling, we investigate crossover positioning in the Arabidopsis thaliana wild-type, an over-expressor of the conserved E3 ligase HEI10, and a hei10 heterozygous line. We show that crossover positions can be explained by a predictive, diffusion-mediated coarsening model, in which large, approximately evenly-spaced HEI10 foci grow at the expense of smaller, closely-spaced clusters. We propose this coarsening process explains many aspects of Arabidopsis crossover positioning, including crossover interference. Consistent with this model, we also demonstrate that crossover positioning can be predictably modified in vivo simply by altering HEI10 dosage, with higher and lower dosage leading to weaker and stronger crossover interference, respectively. As HEI10 is a conserved member of the RING finger protein family that functions in the interference-sensitive pathway for crossover formation, we anticipate that similar mechanisms may regulate crossover positioning in diverse eukaryotes. Crossover numbers and positions are tightly controlled but the mechanism involved is still obscure. Here, the authors, using quantitative super-resolution cytogenetics and mathematical modelling, show that diffusion mediated coarsening of HEI10, an E3-ligase domain containing protein, may explain meiotic crossover positioning in Arabidopsis.

Meiosis is unusual among cell divisions in shuffling genetic material by crossovers among homologous chromosomes and partitioning the genome into haploid gametes. Crossovers are critical for chromosome segregation in most eukaryotes, but are also an important factor in evolution, as they generate novel genetic combinations. The molecular mechanisms that underpin meiotic recombination and chromosome segregation are well conserved across kingdoms, but are also sensitive to perturbation by environment, especially temperature. Even subtle shifts in temperature can alter the number and placement of crossovers, while at greater extremes, structural failures can occur in the linear axis and synaptonemal complex structures which are essential for recombination and chromosome segregation. Understanding the effects of temperature on these processes is important for its implications in evolution and breeding, especially in the context of global warming. In this review, we first summarize the process of meiotic recombination and its reliance on axis and synaptonemal complex structures, and then discuss effects of temperature on these processes and structures. We hypothesize that some consistent effects of temperature on recombination and meiotic thermotolerance may commonly be two sides of the same coin, driven by effects of temperature on the folding or interaction of key meiotic proteins. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

Key Points Post-zygotic genetic incompatibility can ensue when hybridization brings together gene products that no longer function properly together in the same genome, thus reducing gene flow among incompatible genotypes. In plants, numerous forms of postzygotic genetic incompatibilities exist, including hybrid sterility, cytoplasmic male sterility and hybrid necrosis or weakness. Hybrid necrosis is a common type of incompatibility found in F 1 progeny of many crosses within species and between species, which suggests it could be a model for understanding factors that are important at various stages in the processes of genetic differentiation, and perhaps speciation. Classical and newly described cases of hybrid necrosis generally involve two-locus interactions that are similar to Dobzhansky–Muller interactions. The observation that hybrid necrosis is characterized by a recurring suite of characteristics that are similar to phenotypes associated with oxidative stress, such as yellowing, wilting, cell death and tissue necrosis, in multiple taxa, indicates a common underlying mechanism might be responsible. Hybrid necrosis has been described many times during the past 80 years; one common theme that has emerged is a strong association between hybrid necrosis and selection for disease resistance, which suggest that causal alleles might evolve repeatedly in response to common external pressures, such as host–pathogen conflict. In one case of mild autonecrosis, the causal genes have been identified; one is a disease-resistance ( R ) gene, implicating this diverse and rapidly evolving class of genes in plant hybrid incompatibility, and suggesting that hybrid necrosis is akin to an autoimmune response. Other types of hybrid failure that are due to F 1 weakness in plants might be caused by factors as varied as stresses in the physical environment, hormonal aberrations and genome-integrated viruses. Identifying the evolutionary pressures that contribute to divergence or genetic incompatibility remains an important goal with implications for speciation, and hybrid necrosis, given its prevalence in the plant kingdom, could provide a particularly good model for understanding such processes. Reduction in gene flow between varieties is part of the process of speciation. One underappreciated reason for such a reduction is hybrid necrosis — when the hybrid offspring have phenotypes that resemble the results of pathogen attack and environmental stress. Ecological factors, hybrid sterility and differences in ploidy levels are well known for contributing to gene-flow barriers in plants. Another common postzygotic incompatibility, hybrid necrosis, has received comparatively little attention in the evolutionary genetics literature. Hybrid necrosis is associated with a suite of phenotypic characteristics that are similar to those elicited in response to various environmental stresses, including pathogen attack. The genetic architecture is generally simple, and complies with the Bateson–Dobzhansky–Muller model for hybrid incompatibility between species. We survey the extensive literature on this topic and present the hypothesis that hybrid necrosis can result from autoimmunity, perhaps as a pleiotropic effect of evolution of genes that are involved in pathogen response.

Whole-genome duplication (WGD), which leads to polyploidy, is implicated in adaptation and speciation. But what are the immediate effects of WGD and how do newly polyploid lineages adapt to them? With many studies of new and evolved polyploids now available, along with studies of genes under selection in polyploids, we are in an increasingly good position to understand how polyploidy generates novelty. Here, I will review consistent effects of WGD on the biology of plants, such as an increase in cell size, increased stress tolerance and more. I will discuss how a change in something as fundamental as cell size can challenge the function of some cell types in particular. I will also discuss what we have learned about the short- to medium-term evolutionary response to WGD. It is now clear that some of this evolutionary response may ‘lock in’ traits that happen to be beneficial, while in other cases, it might be more of an ‘emergency response’ to work around physiological changes that are either deleterious, or cannot be undone in the polyploid context. Yet, other traits may return rapidly to a diploid-like state. Polyploids may, by re-jigging many inter-related processes, find a new, conditionally adaptive, normal.

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.

Meiosis is essential for the fertility of most eukaryotes and its structures and progression are conserved across kingdoms. Yet many of its core proteins show evidence of rapid or adaptive evolution. What drives the evolution of meiosis proteins? How can constrained meiotic processes be modified in response to challenges without compromising their essential functions? In surveying the literature, we found evidence of two especially potent challenges to meiotic chromosome segregation that probably necessitate adaptive evolutionary responses: whole-genome duplication and abiotic environment, especially temperature. Evolutionary solutions to both kinds of challenge are likely to involve modification of homologous recombination and synapsis, probably via adjustments of core structural components important in meiosis I. Synthesizing these findings with broader patterns of meiosis gene evolution suggests that the structural components of meiosis coevolve as adaptive modules that may change in primary sequence and function while maintaining three-dimensional structures and protein interactions. The often sharp divergence of these genes among species probably reflects periodic modification of entire multiprotein complexes driven by genomic or environmental changes. We suggest that the pressures that cause meiosis to evolve to maintain fertility may cause pleiotropic alterations of global crossover rates. We highlight several important areas for future research.

Spatially structured plant populations with diverse adaptations provide powerful models to investigate evolution. Human-generated ruderal habitats are abundant and low-competition, but are challenging for plants not adapted to them. Ruderal habitats also sometimes form networked corridors (e.g. roadsides and railways) that allow rapid long-distance spread of successfully adapted variants. Here we use transcriptomic and genomic analyses, coupled with genetic mapping and transgenic follow-up, to understand the evolution of rapid cycling during adaptation to railway sites in autotetraploid Arabidopsis arenosa. We focus mostly on a hybrid population that is likely a secondary colonist of a railway site. These mountain railway plants are phenotypically similar to their cosmopolitan cousins. We thus hypothesized that colonization primarily involved the flow of adaptive alleles from the cosmopolitan railway variant. But our data shows that it is not that simple: while there is evidence of selection having acted on introgressed alleles, selection also acted on rare standing variation, and new mutations may also contribute. Among the genes we show have allelic divergence with functional relevance to flowering time are known regulators of flowering, including FLC and CONSTANS. Prior implications of these genes in weediness and rapid cycling supports the idea that these are \"evolutionary hotspots\" for these traits. We also find that one of two alleles of CONSTANS under selection in the secondary colonist was selected from rare standing variation in mountain populations, while the other was introgressed from the cosmopolitan railway populations. The latter allele likely arose in diploid populations over 700km away, highlighting how ruderal populations could act as allele conduits and thus influence local adaptation.

Polyploidy, which arises from genome duplication, has occurred throughout the history of eukaryotes, though it is especially common in plants. The resulting increased size, heterozygosity, and complexity of the genome can be an evolutionary opportunity, facilitating diversification, adaptation and the evolution of functional novelty. On the other hand, when they first arise, polyploids face a number of challenges, one of the biggest being the meiotic pairing, recombination and segregation of the suddenly more than two copies of each chromosome, which can limit their fertility. Both for developing polyploidy as a crop improvement tool (which holds great promise due to the high and lasting multi-stress resilience of polyploids), as well as for our basic understanding of meiosis and plant evolution, we need to know both the specific nature of the challenges polyploids face, as well as how they can be overcome in evolution. In recent years there has been a dramatic uptick in our understanding of the molecular basis of polyploid adaptations to meiotic challenges, and that is the focus of this review.

Serpentine barrens represent extreme hazards for plant colonists. These sites are characterized by high porosity leading to drought, lack of essential mineral nutrients, and phytotoxic levels of metals. Nevertheless, nature forged populations adapted to these challenges. Here, we use a population-based evolutionary genomic approach coupled with elemental profiling to assess how autotetraploid Arabidopsis arenosa adapted to a multichallenge serpentine habitat in the Austrian Alps. We first demonstrate that serpentine-adapted plants exhibit dramatically altered elemental accumulation levels in common conditions, and then resequence 24 autotetraploid individuals from three populations to perform a genome scan. We find evidence for highly localized selective sweeps that point to a polygenic, multitrait basis for serpentine adaptation. Comparing our results to a previous study of independent serpentine colonizations in the closely related diploid Arabidopsis lyrata in the United Kingdom and United States, we find the highest levels of differentiation in 11 of the same loci, providing candidate alleles for mediating convergent evolution. This overlap between independent colonizations in different species suggests that a limited number of evolutionary strategies are suited to overcome the multiple challenges of serpentine adaptation. Interestingly, we detect footprints of selection in A. arenosa in the context of substantial gene flow from nearby off-serpentine populations of A. arenosa, as well as from A. lyrata. In several cases, quantitative tests of introgression indicate that some alleles exhibiting strong selective sweep signatures appear to have been introgressed from A. lyrata. This finding suggests that migrant alleles may have facilitated adaptation of A. arenosa to this multihazard environment.