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Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification.

ABSTRACT: Reproductive genes and traits evolve rapidly in many organisms, including mollusks, algae, and primates. Previously we demonstrated that a family of glycine-rich pollen surface proteins (GRPs) from Arabidopsis thaliana and Brassica oleracea had diverged substantially, making identification of homologous genes impossible despite a separation of only 20 million years. Here we address the molecular genetic mechanisms behind these changes, sequencing the eight members of the GRP cluster, along with 11 neighboring genes in four related species, Arabidopsis arenosa, Olimarabidopsis pumila, Capsella rubella, and Sisymbrium irio. We found that GRP genes change more rapidly than their neighbors; they are more repetitive and have undergone substantially more insertion/deletion events while preserving repeat amino acid composition. Genes flanking the GRP cluster had an average K(a)/K(s) approximately 0.2, indicating strong purifying selection. This ratio rose to approximately 0.5 in the first GRP exon, indicating relaxed selective constraints. The repetitive nature of the second GRP exon makes alignment difficult; even so, K(a)/K(s) within the Arabidopsis genus demonstrated an increase that correlated with exon length. We conclude that rapid GRP evolution is primarily due to duplication, deletion, and divergence of repetitive sequences. GRPs may mediate pollen recognition and hydration by female cells, and divergence of these genes could correlate with or even promote speciation. We tested cross-species interactions, showing that the ability of A. arenosa stigmas to hydrate pollen correlated with GRP divergence and identifying A. arenosa as a model for future studies of pollen recognition.

SUBMITTER: Fiebig A

PROVIDER: S-EPMC365782 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

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Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification.

Fiebig Aretha A Kimport Rebecca R Preuss Daphne D

Proceedings of the National Academy of Sciences of the United States of America 20040217 9

Reproductive genes and traits evolve rapidly in many organisms, including mollusks, algae, and primates. Previously we demonstrated that a family of glycine-rich pollen surface proteins (GRPs) from Arabidopsis thaliana and Brassica oleracea had diverged substantially, making identification of homologous genes impossible despite a separation of only 20 million years. Here we address the molecular genetic mechanisms behind these changes, sequencing the eight members of the GRP cluster, along with ...[more]

PMID: 14970339

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Project description:Oceanic archipelagos provide striking examples of lineages that have radiated over pronounced ecological gradients. Accompanying this diversification, lineages have evolved adaptations allowing survival in extreme environments. Here, we investigate the genomic basis of ecological adaptation in Canary Island Descurainia (Brassicaceae), an island relative of Arabidopsis. The seven endemic species have diversified in situ along an elevational and ecological gradient, from low-elevation scrub to high-elevation sub-alpine desert. We first generated a reference genome for Descurainia millefolia, phylogenetic analysis of which placed it as sister to D. sophioides. Ninety-six gene families were found to be specific to D. millefolia and a further 1087 and 1469 gene families have expanded or contracted in size, respectively, along the D. millefolia branch. We then employed genome re-sequencing to sample 14 genomes across the seven species of Canary Island Descurainia and an outgroup. Phylogenomic analyses were consistent with previous reconstructions of Canary Island Descurainia in resolving low- and high-elevation clades. Using the branch-site dN/dS method, we detected positive selection for 275 genes on the branch separating the low- and high-elevation species and these positively selected genes (PSGs) were significantly enriched for functions related to reproduction and stress tolerance. Comparing PSGs to those in analyses of adaptation to elevation and/or latitude in other Brassicaceae, we found little evidence of widespread convergence and gene reuse, except for two examples, one of which was a significant overlap between Descurainia and Draba nivalis, a species restricted to high latitudes. The study of Canary Island Descurainia suggests that the transition to high-elevation environments such as that found in the high mountains of the Canary Islands involves selection on genes related to reproduction and stress tolerance but that repeated evolution across different lineages that have evolved into similar habitats is limited, indicating substantially different molecular trajectories to adaptation.

Dataset Information

Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification.

Publications

Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification.

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