Most cited article - PubMed ID 30804518
Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa
Genetic variation underpins evolutionary change, but mutation accumulation increases genetic load. Various factors affect the extent of load, such as population size and breeding system, but other important determinants remain unexplored. In particular, whole-genome duplication (WGD)-a pervasive macromutation occurring broadly across Eukaryotes-remains poorly understood in terms of its impact on neutral and selective processes within populations. Using iterative forward simulations and empirical analysis of 632 short- and 16 long-read sequenced individuals of Arabidopsis arenosa (in 23 diploid and 42 natural autotetraploid populations), we measure the effects of WGD on genome-wide diversity and mutation load. Our simulations show how genetic variation gradually rises in autotetraploids due to increased mutational target size. Moreover, mutation load increases due to relaxed purifying selection as ploidies rise, when deleterious mutations are masked by additional chromosome copies. Empirical data confirm these patterns, showing significant increases in nucleotide diversity, ratios of nonsynonymous to synonymous SNPs, and numbers of indels and large structural variants in A. arenosa autotetraploids. However, a rather modest increase in load proxies together with a broad distribution and niche of autotetraploids suggests load accumulation has not yet limited their successful expansion. Overall, we demonstrate a complex interplay between neutral processes and purifying selection in shaping genetic variation following WGD and highlight ploidy as an important determinant of mutation load, genetic diversity, and therefore adaptive potential in natural populations.
- Keywords
- Arabidopsis, evolution, genetic load, genomics, natural selection,
- MeSH
- Mutation Accumulation * MeSH
- Arabidopsis * genetics MeSH
- Gene Duplication MeSH
- Genetic Load * MeSH
- Genome, Plant * MeSH
- Polymorphism, Single Nucleotide MeSH
- Evolution, Molecular MeSH
- INDEL Mutation MeSH
- Selection, Genetic MeSH
- Genomic Structural Variation MeSH
- Tetraploidy * MeSH
- Publication type
- Journal Article MeSH
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.
- Keywords
- Arabidopsis lyrata, adaptation, introgression, polyploid,
- Publication type
- Journal Article MeSH
Cuticle function can be pivotal to plant success in different environments. Yet, the occurrence of intraspecific adjustments in cuticle traits resulting from acclimation or adaptation to different habitats remains poorly understood. Here, we used genetically well-characterised populations of Arabidopsis arenosa to investigate whether cuticle traits were adjusted as part of the parallel evolution from a foothill to an alpine ecotype. Six alpine and six foothill populations, representing at least three independent evolutionary origins of an alpine ecotype, were used in reciprocal transplantation experiments, to investigate cuticle traits at the eco-physiological, biochemical and structural levels. The genetic basis behind these traits was assessed by combining selection scans and differential gene expression analysis. Overall, alpine populations showed reduced cuticular transpiration in conjunction with consistently altered cuticular wax composition, with higher accumulation of two fatty alcohols and two iso-alkanes. Genomic analysis unravelled nine genes associated with cuticular wax metabolism showing allelic differentiation in alpine compared to lowland populations. In silico gene expression analysis revealed differences between ecotypes for several genes related to cuticle metabolism. Repeated ecotypic differentiation in cuticle traits together with the genetic architecture of the alpine ecotype points at an adaptive value of cuticle adjustments for the colonisation of alpine habitats.
- Keywords
- Alpine habitat, Arabidopsis arenosa, adaptation, cuticle, cuticular wax composition, ecotype, parallel evolution,
- MeSH
- Arabidopsis * genetics physiology MeSH
- Ecosystem * MeSH
- Ecotype MeSH
- Plant Epidermis * physiology genetics MeSH
- Phenotype MeSH
- Quantitative Trait, Heritable * MeSH
- Plant Leaves * physiology genetics anatomy & histology MeSH
- Gene Expression Regulation, Plant MeSH
- Genes, Plant MeSH
- Waxes metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Waxes MeSH
Polyploidisation is a significant reproductive barrier, yet genetic evidence indicates that interploidy admixture is more common than previously thought. Theoretical models and controlled crosses support the 'triploid bridge' hypothesis, proposing that hybrids of intermediate ploidy facilitate gene flow. However, comprehensive evidence combining experimental and genetic data from natural mixed-ploidy species is missing. Here, we investigated the rates and directionality of gene flow within a diploid-autotetraploid contact zone of Cardamine amara, a species with abundant natural triploids. We cytotyped over 400 individuals in the field, conducted reciprocal interploidy crosses, and inferred gene flow based on genome-wide sequencing of 84 individuals. Triploids represent a conspicuous entity in mixed-ploidy populations (5%), yet only part of them arose through interploidy hybridisation. Despite being rarely formed, triploid hybrids can backcross with their parental cytotypes, producing viable offspring that are often euploid (in 42% of cases). In correspondence, D-statistics and coalescent simulations documented a significant genome-wide signal of bidirectional gene flow in sympatric but not allopatric populations. Triploids, though rare, thus seem to play a key role in overcoming polyploidy-related reproductive barriers in C. amara. In sum, we present integrative evidence for interploidy gene flow mediated by a triploid bridge in natural populations.
- Keywords
- introgression, polyploidy, population genomics, speciation, whole genome duplication,
- MeSH
- Cardamine * genetics MeSH
- Genetic Introgression * MeSH
- Hybridization, Genetic MeSH
- Ploidies * MeSH
- Polyploidy MeSH
- Genetics, Population MeSH
- Gene Flow * MeSH
- Triploidy * MeSH
- Publication type
- Journal Article 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.
BACKGROUND: Whole-genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species. SCOPE: Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented. CONCLUSIONS: The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed.
- Keywords
- Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
- MeSH
- Biological Evolution MeSH
- Genome, Plant genetics MeSH
- Ploidies MeSH
- Polyploidy * MeSH
- Plants genetics MeSH
- Reproduction genetics MeSH
- Gene Flow * MeSH
- Genetic Speciation MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Baobab (Adansonia digitata) is a long-lived tree endemic to Africa with economic, ecological, and cultural importance, yet its genomic features are underexplored. Here, we report a chromosome-level reference genome anchored to 42 chromosomes for A. digitata, alongside draft assemblies for a sibling tree, two trees from distinct locations in Africa, and A. za from Madagascar. The baobab genome is uniquely rich in DNA transposons, which make up 33%, while LTR retrotransposons account for 10%. A. digitata experienced whole genome multiplication (WGM) around 30 million years ago (MYA), followed by a second WGM event 3-11 MYA, likely linked to autotetraploidy. Resequencing of 25 trees identify three subpopulations, with gene flow across West Africa distinct from East Africa. Gene enrichment and fixation index (Fst) analyses show baobab retained multiple circadian, flowering, and light-responsive genes, which likely support longevity through the UV RESISTANCE LOCUS 8 (UVR8) pathway. In sum, we provide genomic resources and insights for baobab breeding and conservation.
- MeSH
- Chromosomes, Plant * genetics MeSH
- Phylogeny MeSH
- Adaptation, Physiological genetics MeSH
- Genome, Plant * MeSH
- Evolution, Molecular * MeSH
- Retroelements genetics MeSH
- Trees genetics MeSH
- Gene Flow MeSH
- DNA Transposable Elements genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Madagascar MeSH
- Names of Substances
- Retroelements MeSH
- DNA Transposable Elements MeSH
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.
- Keywords
- Allopolyploidy, Betula, autopolyploidy, gene flow, genomic polarization, homoeologs, interploidal, introgressive hybridization, polyploid phylogenetics, polyploidization simulation, reticulate evolution,
- MeSH
- Alleles * MeSH
- Betula * genetics classification MeSH
- Phylogeny * MeSH
- Genome, Plant * MeSH
- Genetic Introgression MeSH
- Hybridization, Genetic MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article MeSH
Polyploidy, the result of whole-genome duplication (WGD), is a major driver of eukaryote evolution. Yet WGDs are hugely disruptive mutations, and we still lack a clear understanding of their fitness consequences. Here, we study whether WGDs result in greater diversity of genomic structural variants (SVs) and how they influence evolutionary dynamics in a plant genus, Cochlearia (Brassicaceae). By using long-read sequencing and a graph-based pangenome, we find both negative and positive interactions between WGDs and SVs. Masking of recessive mutations due to WGDs leads to a progressive accumulation of deleterious SVs across four ploidal levels (from diploids to octoploids), likely reducing the adaptive potential of polyploid populations. However, we also discover putative benefits arising from SV accumulation, as more ploidy-specific SVs harbor signals of local adaptation in polyploids than in diploids. Together, our results suggest that SVs play diverse and contrasting roles in the evolutionary trajectories of young polyploids.
Success or failure of plants to cope with freezing temperatures can critically influence plant distribution and adaptation to new habitats. Especially in alpine environments, frost is a likely major selective force driving adaptation. In Arabidopsis arenosa (L.) Lawalrée, alpine populations have evolved independently in different mountain ranges, enabling studying mechanisms of acclimation and adaptation to alpine environments. We tested for heritable, parallel differentiation in freezing resistance, cold acclimation potential and ice management strategies using eight alpine and eight foothill populations. Plants from three European mountain ranges (Niedere Tauern, Făgăraș and Tatra Mountains) were grown from seeds of tetraploid populations in four common gardens, together with diploid populations from the Tatra Mountains. Freezing resistance was assessed using controlled freezing treatments and measuring effective quantum yield of photosystem II, and ice management strategies by infrared video thermography and cryomicroscopy. The alpine ecotype had a higher cold acclimation potential than the foothill ecotype, whereby this differentiation was more pronounced in tetraploid than diploid populations. However, no ecotypic differentiation was found in one region (Făgăraș), where the ancient lineage had a different evolutionary history. Upon freezing, an ice lens within a lacuna between the palisade and spongy parenchyma tissues was formed by separation of leaf tissues, a mechanism not previously reported for herbaceous species. The dynamic adjustment of freezing resistance to temperature conditions may be particularly important in alpine environments characterized by large temperature fluctuations. Furthermore, the formation of an extracellular ice lens may be a useful strategy to avoid tissue damage during freezing.
- Keywords
- Adaptation, cold acclimation, freezing resistance, ice nucleation, parallel evolution, polyploidization,
- MeSH
- Acclimatization MeSH
- Arabidopsis * genetics MeSH
- Ecosystem MeSH
- Photosystem II Protein Complex MeSH
- Ice MeSH
- Plants MeSH
- Tetraploidy MeSH
- Freezing MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Photosystem II Protein Complex MeSH
- Ice MeSH
