Abstract
BackgroundElucidating the selective and neutral forces underlying molecular evolution is fundamental to understanding the genetic basis of adaptation. Plants have evolved a suite of adaptive responses to cope with variable environmental conditions, but relatively little is known about which genes are involved in such responses. Here we studied molecular evolution on a genome-wide scale in two species of Cardamine with distinct habitat preferences: C. resedifolia, found at high altitudes, and C. impatiens, found at low altitudes. Our analyses focussed on genes that are involved in stress responses to two factors that differentiate the high- and low-altitude habitats, namely temperature and irradiation.ResultsHigh-throughput sequencing was used to obtain gene sequences from C. resedifolia and C. impatiens. Using the available A. thaliana gene sequences and annotation, we identified nearly 3,000 triplets of putative orthologues, including genes involved in cold response, photosynthesis or in general stress responses. By comparing estimated rates of molecular substitution, codon usage, and gene expression in these species with those of Arabidopsis, we were able to evaluate the role of positive and relaxed selection in driving the evolution of Cardamine genes. Our analyses revealed a statistically significant higher rate of molecular substitution in C. resedifolia than in C. impatiens, compatible with more efficient positive selection in the former. Conversely, the genome-wide level of selective pressure is compatible with more relaxed selection in C. impatiens. Moreover, levels of selective pressure were heterogeneous between functional classes and between species, with cold responsive genes evolving particularly fast in C. resedifolia, but not in C. impatiens.ConclusionsOverall, our comparative genomic analyses revealed that differences in effective population size might contribute to the differences in the rate of protein evolution and in the levels of selective pressure between the C. impatiens and C. resedifolia lineages. The within-species analyses also revealed evolutionary patterns associated with habitat preference of two Cardamine species. We conclude that the selective pressures associated with the habitats typical of C. resedifolia may have caused the rapid evolution of genes involved in cold response.
Highlights
Elucidating the selective and neutral forces underlying molecular evolution is fundamental to understanding the genetic basis of adaptation
To minimize the chance of mistaking a paralogue for an orthologue, we considered as triplets of putative orthologues only those consisting of reciprocal best hits, i.e. those where the three sequences were consistently found as best hit matches of one another
In C. impatiens, the mean sequence length was 592.3 ± 5.8 bp, while in C. resedifolia the mean sequence length was 592.2 ± 5.8 bp. We partitioned these genes according to their putative function, and focused our analyses on those functional classes that are associated with the adaptive response to high altitude (Additional File 1)
Summary
Elucidating the selective and neutral forces underlying molecular evolution is fundamental to understanding the genetic basis of adaptation. The first is the candidate gene approach, whereby signatures of positive selection (e.g. the overrepresentation of specific polymorphisms) are identified using a population genetics framework in those genes previously known to be involved in the phenotypic trait of interest A useful compromise is to use the genome-wide approach in species closely related to well-studied model organisms, so that gene function can be inferred by comparative analyses. In this way it is possible to exploit what is known about the ecology and the life history of the species, and the approach is suited to identifying genes involved in species-specific and habitat-specific adaptations In this way it is possible to exploit what is known about the ecology and the life history of the species, and the approach is suited to identifying genes involved in species-specific and habitat-specific adaptations (e.g. [11,14])
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