A novel allele of<i>ASY3</i>promotes meiotic stability in autotetraploid<i>Arabidopsis lyrata</i>

Seear, Paul J.; Gregory, Catherine L.; Heavens, Darren; Schmickl, Roswitha; Yant, Levi; Higgins, James D.

doi:10.1101/2019.12.25.888388

Cited by 3 publications

(6 citation statements)

References 55 publications

(55 reference statements)

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“…Further, we observed the footprint of WGD-associated selection in genome-wide shifts in the frequencies of many alleles, replicated in three independent WGDs. This work, along with others 13,[15][16][17] , shows that these processes exhibit genomic signatures of adaptive evolution consistent with observations of altered phenotype upon WGD consistently in independent adaptation events. A primary, well-established challenge occurs during meiotic chromosome segregation, and we here illustrated in Cochlearia other genomic and physiological changes.…”

Section: Resultssupporting

confidence: 89%

“…The importance of these genes was highlighted by the discovery that these same alleles were shared by both young autotetraploids. Specific signatures of gene flow at these same 8 alleles indicated that the two cases were not independent, and that these 8 alleles that cooperatively function had their origins in sperate diploid species, coming together across species barriers only when the two autotetraploids hybridised 15,16 . More recently, a pool-seq-based genome scan for divergence outliers following WGD in Cardamine amara, a Brassicaceae ~17 million years diverged from A. arenosa, was unable to detect excess convergence beyond that expected by chance among individual loci under selection at the gene orthologue level 17 .…”

Section: Introductionmentioning

confidence: 99%

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Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Bray

Wolf

Zhou

et al. 2020

Preprint

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Convergent evolution is observed broadly across the web of life, but the degree of evolutionary constraint during adaptation of core intracellular processes is not known. High constraint has been assumed for conserved processes, such as cell division and DNA repair, but reports of nimble evolutionary shifts in these processes have confounded this expectation. Whole genome duplication (WGD) necessitates the concerted adjustment of a wide range of fundamental intracellular functions but nevertheless has been repeatedly survived in all kingdoms. Given this repeated adaptation to WGD despite obvious intracellular challenges to core processes such as meiosis, we asked: how do lineages not only survive WGD, but sometimes ultimately thrive? Are the solutions employed constrained or diverse? Here we detect genes and processes under selection following WGD in the Cochlearia species complex by performing a scan for selective sweeps following WGD in a large-scale survey of 73 resequenced individuals from 23 populations across Europe. We then contrast our results from two independent WGDs in Arabidopsis arenosa and Cardamine amara. We find that while WGD does require the adaptation of particular functional processes in all three cases, the specific genes recruited to respond are highly flexible. We also observe evidence of varying degrees of convergence between different cases. Our results point to a polygenic basis for the distributed adaptive systems that control meiotic crossover number, ionomic rewiring, cell cycle control, and nuclear regulation. Given the sheer number of loci under selection post-WGD, we surmise that this polygenicity may explain the general lack of convergence between these species that are ~30 million years diverged. Based on our results, we speculate that adaptive processes themselves – such as the rate of generation of structural genomic variants—may be altered by WGD in nascent autopolyploids, contributing to the occasionally spectacular adaptability of autopolyploids observed across kingdoms.

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Section: Resultssupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Bray

Wolf

Zhou

et al. 2020

Preprint

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“…Moreover, from a joint population genomic analysis of both species across a hybrid zone, clear signals of bidirectional adaptive gene flow emerge exactly at these adaptive alleles between A. arenosa and A. lyrata. 9,15 A panel of segregating populations across the hybrid zone was carefully phenotyped cytologically for meiotic chromosome configurations and the presence of each of the selected alleles was surveyed 15 . Highly contrasting single gene associations were picked up between the stability of meiosis and the presence of each of these alleles, including a reduction in crossover number and a change in crossover distribution 15 .…”

Section: Introductionmentioning

confidence: 99%

“…9,15 A panel of segregating populations across the hybrid zone was carefully phenotyped cytologically for meiotic chromosome configurations and the presence of each of the selected alleles was surveyed 15 . Highly contrasting single gene associations were picked up between the stability of meiosis and the presence of each of these alleles, including a reduction in crossover number and a change in crossover distribution 15 . In seeking the origin of these adaptive alleles, both studies found that in A. arenosa and in A. lyrata there is clear signal that complementary, interacting subsets of the adaptive alleles originated in the opposite diploid species, indicating bidirectional adaptive gene flow between them.…”

Section: Introductionmentioning

confidence: 99%

“…In seeking the origin of these adaptive alleles, both studies found that in A. arenosa and in A. lyrata there is clear signal that complementary, interacting subsets of the adaptive alleles originated in the opposite diploid species, indicating bidirectional adaptive gene flow between them. This gene flow is potentiated by the WGD itself, and thus there is an interdependence in the stabilisation of each young WGD 9,15 . Therefore, A. lyrata and A. arenosa WGD stabilisation events are not independent.…”

Section: Introductionmentioning

confidence: 99%

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Genomic novelty and process-level convergence in adaptation to whole genome duplication

Bohutínská

Alston

Monnahan

et al. 2020

Preprint

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Whole genome duplication (WGD) occurs across kingdoms and can promote adaptation. However, the sudden increase in chromosome number, as well as immediate changes in cellular physiology, are traumatic to conserved cellular processes. Previous work in Arabidopsis arenosa revealed a clearly coordinated genomic response to WGD, involving a set of functionally and physically interacting proteins mediating crossover number and distribution during prophase I of meiosis. Here we ask: is this highly coordinated coevolutionary shift repeated in other species? We also test globally for convergence for all processes under selection in independent cases of adaptation to WGD, as other processes were under selection in A. arenosa and may be common to other independent adaptation events following WGD. Taking advantage of a well-characterised diploid/autopolyploid system, Cardamine amara, we test our hypothesis that convergence will be detected in the form of directional selection. We also investigate at what level convergence may be evident: identical genes, networks, or analogous processes. To do this we performed a genome scan between diploid and autotetraploid populations, while utilising a quartet-based sampling design to minimise false positives. Among the genes exhibiting the strongest signatures of selection in C. amara autotetraploids we detect an enrichment for DNA maintenance, chromosome organisation, and meiosis, as well as stress signalling. We find that gene-level convergence between the independent WGD adaptation events in C. amara and A. arenosa is negligible, with no more orthologous genes in common than would be expected by chance. In contrast to this, however, we observe very strong convergence at the level of functional processes and homologous (but not orthologous) genes. Taken together, our results indicate that these two autopolyploids survived the challenges attendant to WGD by modifying similar or identical processes through different molecular players and gives the first insight into the salient adaptations required to cope with a genome-doubled state.

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Adaptive introgression: how polyploidy reshapes gene flow landscapes

Schmickl

Yant

2021

New Phytologist

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Summary Rare yet accumulating evidence in both plants and animals shows that whole genome duplication (WGD, leading to polyploidy) can break down reproductive barriers, facilitating gene flow between otherwise isolated species. Recent population genomic studies in wild, outcrossing Arabidopsis arenosa and Arabidopsis lyrata indicate that this WGD‐potentiated gene flow can be adaptive and highly specific in response to particular environmental and intracellular challenges. The mechanistic basis of WGD‐mediated easing of species barrier strength seems to primarily lie in the relative dosage of each parental genome in the endosperm. While generalisations about polyploids can be fraught, this evidence indicates that the breakdown of these barriers, combined with diploid to polyploid gene flow and gene flow between polyploids, allows some polyploids to act as adaptable ‘allelic sponges’, enjoying increased potential to respond to challenging environments.

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A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Cited by 3 publications

References 55 publications

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Genomic novelty and process-level convergence in adaptation to whole genome duplication

Adaptive introgression: how polyploidy reshapes gene flow landscapes

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