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.
Angiosperms have become the dominant terrestrial plant group by diversifying for ~145 million years into a broad range of environments. During the course of evolution, numerous morphological innovations arose, often preceded by whole genome duplications (WGD). The mustard family (Brassicaceae), a successful angiosperm clade with ~4000 species, has been diversifying into many evolutionary lineages for more than 30 million years. Here we develop a species inventory, analyze morphological variation, and present a maternal, plastome-based genus-level phylogeny. We show that increased morphological disparity, despite an apparent absence of clade-specific morphological innovations, is found in tribes with WGDs or diversification rate shifts. Both are important processes in Brassicaceae, resulting in an overall high net diversification rate. Character states show frequent and independent gain and loss, and form varying combinations. Therefore, Brassicaceae pave the way to concepts of phylogenetic genome-wide association studies to analyze the evolution of morphological form and function.
Centromere position may change despite conserved chromosomal collinearity. Centromere repositioning and evolutionary new centromeres (ENCs) were frequently encountered during vertebrate genome evolution but only rarely observed in plants. The largest crucifer tribe, Arabideae (∼550 species; Brassicaceae, the mustard family), diversified into several well-defined subclades in the virtual absence of chromosome number variation. Bacterial artificial chromosome-based comparative chromosome painting uncovered a constancy of genome structures among 10 analyzed genomes representing seven Arabideae subclades classified as four genera: Arabis, Aubrieta, Draba, and Pseudoturritis Interestingly, the intra-tribal diversification was marked by a high frequency of ENCs on five of the eight homoeologous chromosomes in the crown-group genera, but not in the most ancestral Pseudoturritis genome. From the 32 documented ENCs, at least 26 originated independently, including 4 ENCs recurrently formed at the same position in not closely related species. While chromosomal localization of ENCs does not reflect the phylogenetic position of the Arabideae subclades, centromere seeding was usually confined to long chromosome arms, transforming acrocentric chromosomes to (sub)metacentric chromosomes. Centromere repositioning is proposed as the key mechanism differentiating overall conserved homoeologous chromosomes across the crown-group Arabideae subclades. The evolutionary significance of centromere repositioning is discussed in the context of possible adaptive effects on recombination and epigenetic regulation of gene expression.
The notion of species as reproductively isolated units related through a bifurcating tree implies that gene trees should generally agree with the species tree and that sister taxa should not share polymorphisms unless they diverged recently and should be equally closely related to outgroups. It is now possible to evaluate this model systematically. We sequenced multiple individuals from 27 described taxa representing the entire Arabidopsis genus. Cluster analysis identified seven groups, corresponding to described species that capture the structure of the genus. However, at the level of gene trees, only the separation of Arabidopsis thaliana from the remaining species was universally supported, and, overall, the amount of shared polymorphism demonstrated that reproductive isolation was considerably more recent than the estimated divergence times. We uncovered multiple cases of past gene flow that contradict a bifurcating species tree. Finally, we showed that the pattern of divergence differs between gene ontologies, suggesting a role for selection.
The Brassicaceae include several major crop plants and numerous important model species in comparative evolutionary research such as Arabidopsis, Brassica, Boechera, Thellungiella, and Arabis species. As any evolutionary hypothesis needs to be placed in a temporal context, reliably dated major splits within the evolution of Brassicaceae are essential. We present a comprehensive time-calibrated framework with important divergence time estimates based on whole-chloroplast sequence data for 29 Brassicaceae species. Diversification of the Brassicaceae crown group started at the Eocene-to-Oligocene transition. Subsequent major evolutionary splits are dated to ∼20 million years ago, coinciding with the Oligocene-to-Miocene transition, with increasing drought and aridity and transient glaciation events. The age of the Arabidopsis thaliana crown group is 6 million years ago, at the Miocene and Pliocene border. The overall species richness of the family is well explained by high levels of neopolyploidy (43% in total), but this trend is neither directly associated with an increase in genome size nor is there a general lineage-specific constraint. Our results highlight polyploidization as an important source for generating new evolutionary lineages adapted to changing environments. We conclude that species radiation, paralleled by high levels of neopolyploidization, follows genome size decrease, stabilization, and genetic diploidization.
- MeSH
- Arabidopsis genetika fyziologie MeSH
- Brassica genetika fyziologie MeSH
- Brassicaceae genetika fyziologie MeSH
- fylogeneze MeSH
- genom chloroplastový genetika MeSH
- genom rostlinný genetika MeSH
- molekulární evoluce * MeSH
- polyploidie MeSH
- sekvenční analýza DNA MeSH
- vznik druhů (genetika) MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: Wild relatives in the genus Arabidopsis are recognized as useful model systems to study traits and evolutionary processes in outcrossing species, which are often difficult or even impossible to investigate in the selfing and annual Arabidopsis thaliana. However, Arabidopsis as a genus is littered with sub-species and ecotypes which make realizing the potential of these non-model Arabidopsis lineages problematic. There are relatively few evolutionary studies which comprehensively characterize the gene pools across all of the Arabidopsis supra-groups and hypothesized evolutionary lineages and none include sampling at a world-wide scale. Here we explore the gene pools of these various taxa using various molecular markers and cytological analyses. RESULTS: Based on ITS, microsatellite, chloroplast and nuclear DNA content data we demonstrate the presence of three major evolutionary groups broadly characterized as A. lyrata group, A. halleri group and A. arenosa group. All are composed of further species and sub-species forming larger aggregates. Depending on the resolution of the marker, a few closely related taxa such as A. pedemontana, A. cebennensis and A. croatica are also clearly distinct evolutionary lineages. ITS sequences and a population-based screen based on microsatellites were highly concordant. The major gene pools identified by ITS sequences were also significantly differentiated by their homoploid nuclear DNA content estimated by flow cytometry. The chloroplast genome provided less resolution than the nuclear data, and it remains unclear whether the extensive haplotype sharing apparent between taxa results from gene flow or incomplete lineage sorting in this relatively young group of species with Pleistocene origins. CONCLUSIONS: Our study provides a comprehensive overview of the genetic variation within and among the various taxa of the genus Arabidopsis. The resolved gene pools and evolutionary lineages will set the framework for future comparative studies on genetic diversity. Extensive population-based phylogeographic studies will also be required, however, in particular for A. arenosa and their affiliated taxa and cytotypes.
- MeSH
- Arabidopsis klasifikace cytologie genetika MeSH
- biologická evoluce MeSH
- chloroplasty genetika MeSH
- ekotyp MeSH
- fylogeografie MeSH
- genetická variace MeSH
- genom chloroplastový MeSH
- genový pool MeSH
- mikrosatelitní repetice MeSH
- tok genů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
