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      New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties

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          Abstract

          The apple is the most common and culturally important fruit crop of temperate areas. The elucidation of its origin and domestication history is therefore of great interest. The wild Central Asian species Malus sieversii has previously been identified as the main contributor to the genome of the cultivated apple ( Malus domestica), on the basis of morphological, molecular, and historical evidence. The possible contribution of other wild species present along the Silk Route running from Asia to Western Europe remains a matter of debate, particularly with respect to the contribution of the European wild apple. We used microsatellite markers and an unprecedented large sampling of five Malus species throughout Eurasia (839 accessions from China to Spain) to show that multiple species have contributed to the genetic makeup of domesticated apples. The wild European crabapple M. sylvestris, in particular, was a major secondary contributor. Bidirectional gene flow between the domesticated apple and the European crabapple resulted in the current M. domestica being genetically more closely related to this species than to its Central Asian progenitor, M. sieversii. We found no evidence of a domestication bottleneck or clonal population structure in apples, despite the use of vegetative propagation by grafting. We show that the evolution of domesticated apples occurred over a long time period and involved more than one wild species. Our results support the view that self-incompatibility, a long lifespan, and cultural practices such as selection from open-pollinated seeds have facilitated introgression from wild relatives and the maintenance of genetic variation during domestication. This combination of processes may account for the diversification of several long-lived perennial crops, yielding domestication patterns different from those observed for annual species.

          Author Summary

          The apple, one of the most ubiquitous and culturally important temperate fruit crops, provides us with a unique opportunity to study the process of domestication in trees. The number and identity of the progenitors of the domesticated apple and the erosion of genetic diversity associated with the domestication process remain debated. The Central Asian wild apple has been identified as the main progenitor, but other closely related species along the Silk Route running from Asia to Western Europe may have contributed to the genome of the domesticated crop. Using rapidly evolving genetic markers to make inferences about the recent evolutionary history of the domesticated apple, we found that the European crabapple has made an unexpectedly large contribution to the genome of the domesticated apple. Bidirectional gene flow between the domesticated apple and the European crabapple resulted in the domesticated apple being currently more similar genetically to this secondary genepool than to the ancestral progenitor, the Central Asian wild apple. We found that domesticated apples have evolved over long time scales, with contributions from at least two wild species in different geographic areas, with no significant erosion of genetic diversity. This process of domestication and diversification may be common to other fruit trees and contrasts with the models documented for annual crops.

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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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            A single domestication for maize shown by multilocus microsatellite genotyping.

            There exists extraordinary morphological and genetic diversity among the maize landraces that have been developed by pre-Columbian cultivators. To explain this high level of diversity in maize, several authors have proposed that maize landraces were the products of multiple independent domestications from their wild relative (teosinte). We present phylogenetic analyses based on 264 individual plants, each genotyped at 99 microsatellites, that challenge the multiple-origins hypothesis. Instead, our results indicate that all maize arose from a single domestication in southern Mexico about 9,000 years ago. Our analyses also indicate that the oldest surviving maize types are those of the Mexican highlands with maize spreading from this region over the Americas along two major paths. Our phylogenetic work is consistent with a model based on the archaeological record suggesting that maize diversified in the highlands of Mexico before spreading to the lowlands. We also found only modest evidence for postdomestication gene flow from teosinte into maize.
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              The nature of selection during plant domestication.

              Plant domestication is an outstanding example of plant-animal co-evolution and is a far richer model for studying evolution than is generally appreciated. There have been numerous studies to identify genes associated with domestication, and archaeological work has provided a clear understanding of the dynamics of human cultivation practices during the Neolithic period. Together, these have provided a better understanding of the selective pressures that accompany crop domestication, and they demonstrate that a synthesis from the twin vantage points of genetics and archaeology can expand our understanding of the nature of evolutionary selection that accompanies domestication.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                May 2012
                May 2012
                10 May 2012
                : 8
                : 5
                : e1002703
                Affiliations
                [1 ]CNRS, Laboratoire Ecologie Systématique et Evolution – UMR8079, Orsay, France
                [2 ]Université Paris Sud, Orsay, France
                [3 ]AgroParisTech, Orsay, France
                [4 ]Plant Research International, Wageningen UR Plant Breeding, Wageningen, The Netherlands
                [5 ]Growth and Development Group, Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Melle, Belgium
                [6 ]INRA, IRHS, PRES UNAM, SFR QUASAV, Beaucouzé, France
                [7 ]Université d'Angers, IRHS, PRES UNAM, SFR QUASAV, Angers, France
                [8 ]Agrocampus Ouest, IRHS, PRES UNAM, SFR QUASAV, Angers, France
                [9 ]Institute of Botany, Department of Plant Taxonomy, Armenian National Academy of Sciences, Yerevan, Armenia
                [10 ]Biological Institution, Tomsk State University, Tomsk, Russia
                [11 ]Department of Plant Pathology, Shandong Agricultural University, Taian, China
                [12 ]CNRS, UMR de Génétique Végétale, INRA/CNRS/Univ Paris-Sud, Gif-sur-Yvette, France
                University of Georgia, United States of America
                Author notes

                Conceived and designed the experiments: TG PG. Performed the experiments: AC. Analyzed the data: AC PG. Contributed reagents/materials/analysis tools: AC PG MJMS IR-R FL BLC AN JC MO LF IG X-GZ TG. Wrote the paper: AC PG MJMS MIT TG. Searched for funding: TG PG AC MIT. Wrote grant proposals: TG PG AC MIT.

                Article
                PGENETICS-D-11-02365
                10.1371/journal.pgen.1002703
                3349737
                22589740
                51d026ad-68c3-4178-ba42-933376513cce
                Cornille et al. 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
                : 1 November 2011
                : 26 March 2012
                Page count
                Pages: 13
                Categories
                Research Article
                Agriculture
                Crops
                Forestry
                Biology
                Evolutionary Biology
                Evolutionary Genetics
                Population Genetics
                Genetics
                Molecular Genetics
                Plant Genetics
                Population Genetics
                Plant Science
                Plant Evolution
                Plant Genetics

                Genetics
                Genetics

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