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Selection and adaptive introgression guided the complex evolutionary history of the European common bean.

ABSTRACT: Domesticated crops have been disseminated by humans over vast geographic areas. Common bean (Phaseolus vulgaris L.) was introduced in Europe after 1492. Here, by combining whole-genome profiling, metabolic fingerprinting and phenotypic characterisation, we show that the first common bean cultigens successfully introduced into Europe were of Andean origin, after Francisco Pizarro's expedition to northern Peru in 1529. We reveal that hybridisation, selection and recombination have shaped the genomic diversity of the European common bean in parallel with political constraints. There is clear evidence of adaptive introgression into the Mesoamerican-derived European genotypes, with 44 Andean introgressed genomic segments shared by more than 90% of European accessions and distributed across all chromosomes except PvChr11. Genomic scans for signatures of selection highlight the role of genes relevant to flowering and environmental adaptation, suggesting that introgression has been crucial for the dissemination of this tropical crop to the temperate regions of Europe.

SUBMITTER: Bellucci E

PROVIDER: S-EPMC10076260 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Selection and adaptive introgression guided the complex evolutionary history of the European common bean.

Bellucci Elisa E Benazzo Andrea A Xu Chunming C Bitocchi Elena E Rodriguez Monica M Alseekh Saleh S Di Vittori Valerio V Gioia Tania T Neumann Kerstin K Cortinovis Gaia G Frascarelli Giulia G Murube Ester E Trucchi Emiliano E Nanni Laura L Ariani Andrea A Logozzo Giuseppina G Shin Jin Hee JH Liu Chaochih C Jiang Liang L Ferreira Juan José JJ Campa Ana A Attene Giovanna G Morrell Peter L PL Bertorelle Giorgio G Graner Andreas A Gepts Paul P Fernie Alisdair R AR Jackson Scott A SA Papa Roberto R

Nature communications 20230405 1

Domesticated crops have been disseminated by humans over vast geographic areas. Common bean (Phaseolus vulgaris L.) was introduced in Europe after 1492. Here, by combining whole-genome profiling, metabolic fingerprinting and phenotypic characterisation, we show that the first common bean cultigens successfully introduced into Europe were of Andean origin, after Francisco Pizarro's expedition to northern Peru in 1529. We reveal that hybridisation, selection and recombination have shaped the genom ...[more]

PMID: 37019898

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Project description:Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.

Project description:We have investigated the role of selection in the determination of the detected levels of introgression from modern maize hybrid varieties into maize landraces still cultivated in situ in Italy. We exploited the availability of a historical collection of landraces undertaken before the introduction and widespread use of modern maize, to analyse genomic changes that have occurred in these maize landraces over 50 years of co-existence with hybrid varieties. We have combined a previously published SSR dataset (n=21) with an AFLP loci dataset (n=168) to provide higher resolution power and to obtain a more detailed picture. We show that selection pressures for adaptation have favoured new alleles introduced by migration from hybrids. This shows the potential for analysis of historical introgression even over this short period of 50 years, for an understanding of the evolution of the genome and for the identification of its functionally important regions. Moreover, this demonstrates that landraces grown in situ represent almost unique populations for use for such studies when the focus is on the domesticated plant. This is due to their adaptation, which has arisen from their dynamic evolution under a continuously changing agro-ecological environment, and their capture of new alleles from hybridisation. We have also identified loci for which selection has inhibited introgression from modern germplasm and has enhanced the distinction between landraces and modern maize. These loci indicate that selection acted in the past, during the formation of the flint and dent gene pools. In particular, the locus showing the strongest signals of selection is a Misfit transposable element. Finally, molecular characterisation of the same samples with two different molecular markers has allowed us to compare their performances. Although the genetic-diversity and population-structure analyses provide the same global qualitative pattern, which thus provides the same inferences, there are differences related to their natures and characteristics.

Dataset Information

Selection and adaptive introgression guided the complex evolutionary history of the European common bean.

Publications

Selection and adaptive introgression guided the complex evolutionary history of the European common bean.

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