Nejvíce citovaný článek - PubMed ID 34404804
Parallel adaptation in autopolyploid Arabidopsis arenosa is dominated by repeated recruitment of shared alleles
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.
- Klíčová slova
- Arabidopsis, evolution, genetic load, genomics, natural selection,
- MeSH
- akumulace mutací * MeSH
- Arabidopsis * genetika MeSH
- duplikace genu MeSH
- genetická zátěž * MeSH
- genom rostlinný * MeSH
- jednonukleotidový polymorfismus MeSH
- molekulární evoluce MeSH
- mutace INDEL MeSH
- selekce (genetika) MeSH
- strukturální variace genomu MeSH
- tetraploidie * MeSH
- Publikační typ
- časopisecké články 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.
- Klíčová slova
- Alpine habitat, Arabidopsis arenosa, adaptation, cuticle, cuticular wax composition, ecotype, parallel evolution,
- MeSH
- Arabidopsis * genetika fyziologie MeSH
- ekosystém * MeSH
- ekotyp MeSH
- epidermis rostlin * fyziologie genetika MeSH
- fenotyp MeSH
- kvantitativní znak dědičný * MeSH
- listy rostlin * fyziologie genetika anatomie a histologie MeSH
- regulace genové exprese u rostlin MeSH
- rostlinné geny MeSH
- vosky metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- vosky 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.
- Klíčová slova
- Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
- MeSH
- biologická evoluce MeSH
- genom rostlinný genetika MeSH
- ploidie MeSH
- polyploidie * MeSH
- rostliny genetika MeSH
- rozmnožování genetika MeSH
- tok genů * MeSH
- vznik druhů (genetika) MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy 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
