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      Evidence for Introduction Bottleneck and Extensive Inter-Gene Pool (Mesoamerica x Andes) Hybridization in the European Common Bean ( Phaseolus vulgaris L.) Germplasm

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          Abstract

          Common bean diversity within and between Mesoamerican and Andean gene pools was compared in 89 landraces from America and 256 landraces from Europe, to elucidate the effects of bottleneck of introduction and selection for adaptation during the expansion of common bean ( Phaseolus vulgaris L.) in Europe. Thirteen highly polymorphic nuclear microsatellite markers (nuSSRs) were used to complement chloroplast microsatellite (cpSSRs) and nuclear markers (phaseolin and Pv-shatterproof1) data from previous studies. To verify the extent of the introduction bottleneck, inter-gene pool hybrids were distinguished from “pure” accessions. Hybrids were identified on the basis of recombination of gene pool specific cpSSR, phaseolin and Pv-shatterproof1 markers with a Bayesian assignments based on nuSSRs, and with STRUCTURE admixture analysis. More hybrids were detected than previously, and their frequency was almost four times larger in Europe (40.2%) than in America (12.3%). The genetic bottleneck following the introduction into Europe was not evidenced in the analysis including all the accessions, but it was significant when estimated only with “pure” accessions, and five times larger for Mesoamerican than for Andean germplasm. The extensive inter-gene pool hybridization generated a large amount of genotypic diversity that mitigated the effects of the bottleneck that occurred when common bean was introduced in Europe. The implication for evolution and the advantages for common bean breeding are discussed.

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          Estimation of average heterozygosity and genetic distance from a small number of individuals.

          M Nei (1978)
          The magnitudes of the systematic biases involved in sample heterozygosity and sample genetic distances are evaluated, and formulae for obtaining unbiased estimates of average heterozygosity and genetic distance are developed. It is also shown that the number of individuals to be used for estimating average heterozygosity can be very small if a large number of loci are studied and the average heterozygosity is low. The number of individuals to be used for estimating genetic distance can also be very small if the genetic distance is large and the average heterozygosity of the two species compared is low.
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            Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations.

            Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (G(ST)) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on G(ST). Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (approximately 0.10). G(ST) at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas G(ST) at paternally and biparentally inherited markers also covary positively but more loosely and G(ST) at maternally inherited markers are largely independent of values based on nuclear markers. A model-based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen-to-seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (N(ST) or R(ST)) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.
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              Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae).

              Domesticated materials with well-known wild relatives provide an experimental system to reveal how human selection during cultivation affects genetic composition and adaptation to novel environments. In this paper, our goal was to elucidate how two geographically distinct domestication events modified the structure and level of genetic diversity in common bean. Specifically, we analyzed the genome-wide genetic composition at 26, mostly unlinked microsatellite loci in 349 accessions of wild and domesticated common bean from the Andean and Mesoamerican gene pools. Using a model-based approach, implemented in the software STRUCTURE, we identified nine wild or domesticated populations in common bean, including four of Andean and four of Mesoamerican origins. The ninth population was the putative wild ancestor of the species, which was classified as a Mesoamerican population. A neighbor-joining analysis and a principal coordinate analysis confirmed genetic relationships among accessions and populations observed with the STRUCTURE analysis. Geographic and genetic distances in wild populations were congruent with the exception of a few putative hybrids identified in this study, suggesting a predominant effect of isolation by distance. Domesticated common bean populations possessed lower genetic diversity, higher F(ST), and generally higher linkage disequilibrium (LD) than wild populations in both gene pools; their geographic distributions were less correlated with genetic distance, probably reflecting seed-based gene flow after domestication. The LD was reduced when analyzed in separate Andean and Mesoamerican germplasm samples. The Andean domesticated race Nueva Granada had the highest F(ST) value and widest geographic distribution compared to other domesticated races, suggesting a very recent origin or a selection event, presumably associated with a determinate growth habit, which predominates in this race.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                1 October 2013
                : 8
                : 10
                : e75974
                Affiliations
                [1 ]Scuola di Scienze Agrarie, Forestali, Alimentari ed Ambientali, Università degli Studi della Basilicata, Potenza, Italy
                [2 ]Dipartimento di Agraria, Sezione di Agronomia, Coltivazioni Erbacee e Genetica, Università degli Studi di Sassari, Sassari, Italy
                [3 ]Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università Politecnica delle Marche, Ancona, Italy
                [4 ]Dipartimento delle Scienze delle Produzioni Vegetali, del Suolo e dell'Ambiente Agroforestale, Università degli Studi di Firenze, Firenze, Italy
                [5 ]Dipartimento di Biologia Applicata, Università degli Studi di Perugia, Perugia, Italy
                [6 ]Consiglio per la Ricerca e la sperimentazione in Agricoltura, Cereal Research Centre (CRA-CER), Foggia, Italy
                Nanjing Forestry University, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GA VN SB RP PSZ. Performed the experiments: GL EB SB. Analyzed the data: TG GL PSZ. Contributed reagents/materials/analysis tools: GA VN SB RP PSZ. Wrote the manuscript: TG.

                Article
                PONE-D-13-21639
                10.1371/journal.pone.0075974
                3788063
                36339441-31b1-4731-8c70-828b180e7b37
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 May 2013
                : 19 August 2013
                Funding
                This study was supported by the Italian Government (MIUR) grant no. #2002075423, Project COFIN 2002: "Beans in Europe: structure of genetic diversity under the effect of colonization and breeding system". TG was supported by a student research fellowship from the Università degli Studi della Basilicata (Potenza, Italy). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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