The John Innes Centre Publications Repository contains details of all publications resulting from our researchers.
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The creation of this publications repository was funded by BBSRC.
Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa
PLoS Genetics (14) e1007510
Publisher's version: 10.1371/journal.pgen.1007510
ID: 59418read more
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 CONSTANSunder 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.
Genetics (208) 1409-1420
Publisher's version: 10.1534/genetics.117.300588
ID: 58069read more
Meiotic recombination shuffles genetic information from sexual species into gametes to create novel combinations in offspring. Thus, recombination is an important factor in inheritance, adaptation and responses to selection. However, recombination is not a static parameter; meiotic recombination rate is sensitive to variation in the environment, especially temperature. That recombination rates change in response to both increases and decreases in temperature was reported in Drosophila a century ago, and since then in several other species. But it is still unclear what the underlying mechanism is, and whether low and high temperature effects are mechanistically equivalent. Here we show that, as in Drosophila, both high and low temperatures increase meiotic crossovers in Arabidopsis thaliana. We show that, from a nadir at 18C, both lower and higher temperatures increase recombination through additional class I – interfering – crossovers. The increase in crossovers at high and low temperatures however appears to be mechanistically at least somewhat distinct, as they differ in their association with the DNA repair protein MLH1. We also find that, in contrast to what has been reported in barley, synaptonemal complex length is negatively correlated with temperature; thus, an increase in chromosome axis length may account for increased crossovers at low temperature in A. thaliana, but cannot explain the increased crossovers observed at high temperature. The plasticity of recombination has important implications for evolution and breeding, and also for interpreting observations of recombination rate variation among natural populations.
Are the effects of elevated temperature on meiotic recombination and thermotolerance linked via the axis and synaptonemal complex?
Philosophical Transactions of the Royal Society B: Biological Sciences (372)
Publisher's version: 10.1098/rstb.2016.0470
ID: 57852read more
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.
Current Opinion in Plant Biology (36) 9-14
Publisher's version: 10.1016/j.pbi.2016.11.018
ID: 55528read more
Large-scale population genomic approaches have very recently been fruitfully applied to the Arabidopsis relatives Arabidopsis halleri, A. lyrata and especially A. arenosa. In contrast to A. thaliana, these species are obligately outcrossing and thus the footprints of natural selection are more straightforward to detect. Furthermore, both theoretical and empirical studies indicate that outcrossers are better able to evolve in response to selection pressure. As a result, recent work in these species serves as a paradigm of population genomic studies of adaptation both to environmental as well as intracellular challenges.
Current Opinion in Plant Biology (30) 116-122
Publisher's version: 10.1016/j.pbi.2016.02.004
ID: 55769read more
All newly formed polyploids face a challenge in meiotic chromosome segregation due to the presence of an additional set of chromosomes. Nevertheless, naturally occurring auto and allopolyploids are common and generally show high fertility, showing that evolution can find solutions. Exactly how meiosis is adapted in these cases, however, remains a mystery. The rise of Arabidopsis as a model genus for polyploid and meiosis research has seen several new studies begin to shed light on this long standing question.
Plant Physiology (171) 437-451
Publisher's version: 10.1104/pp.15.01875
ID: 52765read more
Weediness in ephemeral plants is commonly characterized by rapid cycling, prolific "all in" flowering, and loss of perenniality. Many species made transitions to weediness of this sort, which can be advantageous in high-disturbance or human associated habitats. The molecular basis of this shift, however, remains mostly mysterious. Here we use transcriptome sequencing, genome resequencing scans for selection, and stress tolerance assays to study a weedy population of the otherwise non-weedy Arabidopsis arenosa, an obligately outbreeding relative of A. thaliana. Though weedy A. arenosa is widespread, a single genetic lineage colonized railways throughout central and northern Europe. We show that railway plants, in contrast to plants from sheltered outcrops in hill/mountain regions, are rapid cycling, have lost vernalization requirement, show prolific flowering, and do not return to vegetative growth. Comparing transcriptomes of railway and mountain plants across timecourses with and without vernalization, we found railway plants have sharply abrogated vernalization responsiveness, and high constitutive expression of heat and cold-responsive genes. Railway plants also have strong constitutive heat shock and freezing tolerance compared with mountain plants, where tolerance must be induced. We found 20 genes with good evidence of selection in the railway population. One of these, LATE ELONGATED HYPOCOTYL (LHY) is known in A. thaliana to regulate many stress response genes we found to be differentially regulated among the distinct habitats. Our data suggest that beyond life history regulation, other traits like basal stress tolerance are also associated with the evolution of weediness in A. arenosa.
The challenge of evolving stable polyploidy: could an increase in “crossover interference distance” play a central role?
Chromosoma (125) 287
Publisher's version: 10.1007/s00412-015-0571-4
ID: 52471read more
Whole genome duplication is a prominent feature of many highly evolved organisms, especially plants. When duplications occur within species, they yield genomes comprising multiple identical or very similar copies of each chromosome (“autopolyploids”). Such genomes face special challenges during meiosis, the specialized cellular program that underlies gamete formation for sexual reproduction. Comparisons between newly formed (neo)-autotetraploids and fully evolved autotetraploids suggest that these challenges are solved by specific restrictions on the positions of crossover recombination events and, thus, the positions of chiasmata, which govern the segregation of homologs at the first meiotic division. We propose that a critical feature in the evolution of these more effective chiasma patterns is an increase in the effective distance of meiotic crossover interference, which plays a central role in crossover positioning. We discuss the findings in several organisms, including the recent identification of relevant genes in Arabidopsis arenosa, that support this hypothesis.
Proceedings of the National Academy of Sciences of the United States of America (113) 8320-8325
Publisher's version: 10.1073/pnas.1600405113
ID: 53288read more
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 multi-challenge 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, multi-trait basis for serpentine adaptation. Comparing our results to a previous study of independent serpentine colonizations in the closely related diploid A. lyrata in the UK and US, 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 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 suggests that migrant alleles may have facilitated adaptation of A. arenosa to this multi-hazard environment.
Genome management and mismanagement-cell-level opportunities and challenges of whole-genome duplication.
Genes & Development (29) 2405-19
Publisher's version: 10.1101/gad.271072.115
ID: 52429read more
Whole-genome duplication (WGD) doubles the DNA content in the nucleus and leads to polyploidy. In whole-organism polyploids, WGD has been implicated in adaptability and the evolution of increased genome complexity, but polyploidy can also arise in somatic cells of otherwise diploid plants and animals, where it plays important roles in development and likely environmental responses. As with whole organisms, WGD can also promote adaptability and diversity in proliferating cell lineages, although whether WGD is beneficial is clearly context-dependent. WGD is also sometimes associated with aging and disease and may be a facilitator of dangerous genetic and karyotypic diversity in tumorigenesis. Scaling changes can affect cell physiology, but problems associated with WGD in large part seem to arise from problems with chromosome segregation in polyploid cells. Here we discuss both the adaptive potential and problems associated with WGD, focusing primarily on cellular effects. We see value in recognizing polyploidy as a key player in generating diversity in development and cell lineage evolution, with intriguing parallels across kingdoms.