Nejvíce citovaný článek - PubMed ID 32667955
A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata
Abundance of established polyploid lineages varies across lineages, evolutionary time, and geography, suggesting both genetics and environment play a role in polyploid persistence. We show Arabidopsis lyrata is the most polyploid-rich species complex in the Arabidopsis genus, with multiple origins of autotetraploidy. This is revealed by genomic data from over 400 A. lyrata samples across Eurasia. We found over 30 previously undescribed autotetraploid populations in Siberia with a minimum of two separate origins, independent of those previously reported in Central Europe. The establishment of Siberian tetraploids is mediated by meiotic adaptation at the same genes as in European tetraploid A. lyrata and Arabidopsis arenosa, despite their genomic divergence and geographical separation. Haplotype analysis based on synthetic long-read assemblies supports the long-range introgression of adaptive alleles from the tetraploid interspecific pool of European A. lyrata and A. arenosa to tetraploid Siberian A. lyrata. Once adaptations to polyploidy emerge, they promote the establishment of new polyploid lineages through adaptive inter- and intraspecific introgression.
- Klíčová slova
- Arabidopsis lyrata, adaptation, introgression, polyploid,
- Publikační typ
- časopisecké články MeSH
Polyploidy, the result of whole genome duplication (WGD), is widespread across the tree of life and is often associated with speciation and adaptability. It is thought that adaptation in autopolyploids (within-species polyploids) may be facilitated by increased access to genetic variation. This variation may be sourced from gene flow with sister diploids and new access to other tetraploid lineages, as well as from increased mutational targets provided by doubled DNA content. Here, we deconstruct in detail the origins of haplotypes displaying the strongest selection signals in established, successful autopolyploids, Arabidopsis lyrata and Arabidopsis arenosa. We see strong signatures of selection in 17 genes implied in meiosis, cell cycle, and transcription across all four autotetraploid lineages present in our expanded sampling of 983 sequenced genomes. Most prominent in our results is the finding that the tetraploid-characteristic haplotypes with the most robust signals of selection were completely absent in all diploid sisters. In contrast, the fine-scaled variant 'mosaics' in the tetraploids originated from highly diverse evolutionary sources. These include widespread novel reassortments of trans-specific polymorphism from diploids, new mutations, and tetraploid-specific inter-species hybridization-a pattern that is in line with the broad-scale acquisition and reshuffling of potentially adaptive variation in tetraploids.
Introgression allows polyploid species to acquire new genomic content from diploid progenitors or from other unrelated diploid or polyploid lineages, contributing to genetic diversity and facilitating adaptive allele discovery. In some cases, high levels of introgression elicit the replacement of large numbers of alleles inherited from the polyploid's ancestral species, profoundly reshaping the polyploid's genomic composition. In such complex polyploids, it is often difficult to determine which taxa were the progenitor species and which taxa provided additional introgressive blocks through subsequent hybridization. Here, we use population-level genomic data to reconstruct the phylogenetic history of Betula pubescens (downy birch), a tetraploid species often assumed to be of allopolyploid origin and which is known to hybridize with at least four other birch species. This was achieved by modeling polyploidization and introgression events under the multispecies coalescent and then using an approximate Bayesian computation rejection algorithm to evaluate and compare competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 178,000-188,000 generations ago. Extensive hybridization with B. pendula, B. nana, and B. humilis followed in the aftermath of autopolyploidization, with the relative contribution of each of these species to the B. pubescens genome varying markedly across the species' range. Functional analysis of B. pubescens loci containing alleles introgressed from B. nana identified multiple genes involved in climate adaptation, while loci containing alleles derived from B. humilis revealed several genes involved in the regulation of meiotic stability and pollen viability in plant species.
- Klíčová slova
- Allopolyploidy, Betula, autopolyploidy, gene flow, genomic polarization, homoeologs, interploidal, introgressive hybridization, polyploid phylogenetics, polyploidization simulation, reticulate evolution,
- MeSH
- alely * MeSH
- bříza * genetika klasifikace MeSH
- fylogeneze * MeSH
- genom rostlinný * MeSH
- genová introgrese MeSH
- hybridizace genetická MeSH
- polyploidie * MeSH
- Publikační typ
- časopisecké články MeSH
Polyploidization is a common phenomenon in the evolution of flowering plants. However, only a few genes controlling polyploid genome stability, fitness, and reproductive success are known. Here, we studied the effects of loss-of-function mutations in NSE2 and NSE4A subunits of the Structural Maintenance of Chromosomes 5/6 (SMC5/6) complex in autotetraploid Arabidopsis thaliana plants. The diploid nse2 and nse4a plants show partially reduced fertility and produce about 10% triploid offspring with two paternal and one maternal genome copies. In contrast, the autotetraploid nse2 and nse4a plants were almost sterile and produced hexaploid and aneuploid progeny with the extra genome copies or chromosomes coming from both parents. In addition, tetraploid mutants had more severe meiotic defects, possibly due to the presence of four homologous chromosomes instead of two. Overall, our study suggests that the SMC5/6 complex is an important player in the maintenance of tetraploid genome stability and that autotetraploid Arabidopsis plants have a generally higher frequency of but also higher tolerance for aneuploidy compared to diploids.
- Klíčová slova
- NSE2, SMC5/6 complex, genome stability, meiosis, polyploidy, seed development,
- Publikační typ
- časopisecké články MeSH
Whole genome duplication (WGD) can promote adaptation but is disruptive to conserved processes, especially meiosis. Studies in Arabidopsis arenosa revealed a coordinated evolutionary response to WGD involving interacting proteins controlling meiotic crossovers, which are minimized in an autotetraploid (within-species polyploid) to avoid missegregation. Here, we test whether this surprising flexibility of a conserved essential process, meiosis, is recapitulated in an independent WGD system, Cardamine amara, 17 My diverged from A. arenosa. We assess meiotic stability and perform population-based scans for positive selection, contrasting the genomic response to WGD in C. amara with that of A. arenosa. We found in C. amara the strongest selection signals at genes with predicted functions thought important to adaptation to WGD: meiosis, chromosome remodeling, cell cycle, and ion transport. However, genomic responses to WGD in the two species differ: minimal ortholog-level convergence emerged, with none of the meiosis genes found in A. arenosa exhibiting strong signal in C. amara. This is consistent with our observations of lower meiotic stability and occasional clonal spreading in diploid C. amara, suggesting that nascent C. amara autotetraploid lineages were preadapted by their diploid lifestyle to survive while enduring reduced meiotic fidelity. However, in contrast to a lack of ortholog convergence, we see process-level and network convergence in DNA management, chromosome organization, stress signaling, and ion homeostasis processes. This gives the first insight into the salient adaptations required to meet the challenges of a WGD state and shows that autopolyploids can utilize multiple evolutionary trajectories to adapt to WGD.
- Klíčová slova
- adaptation, convergence, genome duplication, polyploidy,
- MeSH
- Arabidopsis * genetika MeSH
- duplikace genu * MeSH
- genom rostlinný MeSH
- meióza genetika MeSH
- polyploidie MeSH
- segregace chromozomů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
