New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties

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 cult...

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Published inPLoS genetics Vol. 8; no. 5; p. e1002703
Main Authors Cornille, Amandine, Gladieux, Pierre, Smulders, Marinus J M, Roldán-Ruiz, Isabel, Laurens, François, Le Cam, Bruno, Nersesyan, Anush, Clavel, Joanne, Olonova, Marina, Feugey, Laurence, Gabrielyan, Ivan, Zhang, Xiu-Guo, Tenaillon, Maud I, Giraud, Tatiana
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2012
Public Library of Science (PLoS)
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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.
AbstractList 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.
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. 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.
  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.
Audience Academic
Author Giraud, Tatiana
Feugey, Laurence
Nersesyan, Anush
Zhang, Xiu-Guo
Cornille, Amandine
Gabrielyan, Ivan
Laurens, François
Clavel, Joanne
Le Cam, Bruno
Tenaillon, Maud I
Roldán-Ruiz, Isabel
Olonova, Marina
Gladieux, Pierre
Smulders, Marinus J M
AuthorAffiliation 1 CNRS, Laboratoire Ecologie Systématique et Evolution – UMR8079, Orsay, France
10 Biological Institution, Tomsk State University, Tomsk, Russia
9 Institute of Botany, Department of Plant Taxonomy, Armenian National Academy of Sciences, Yerevan, Armenia
12 CNRS, UMR de Génétique Végétale, INRA/CNRS/Univ Paris-Sud, Gif-sur-Yvette, France
6 INRA, IRHS, PRES UNAM, SFR QUASAV, Beaucouzé, France
5 Growth and Development Group, Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Melle, Belgium
3 AgroParisTech, Orsay, France
8 Agrocampus Ouest, IRHS, PRES UNAM, SFR QUASAV, Angers, France
4 Plant Research International, Wageningen UR Plant Breeding, Wageningen, The Netherlands
7 Université d'Angers, IRHS, PRES UNAM, SFR QUASAV, Angers, France
University of Georgia, United States of America
2 Université Paris Sud, Orsay, France
11 Department of Plant Pathology, Shandong Agricultural University, Taian, China
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– name: 9 Institute of Botany, Department of Plant Taxonomy, Armenian National Academy of Sciences, Yerevan, Armenia
– name: 12 CNRS, UMR de Génétique Végétale, INRA/CNRS/Univ Paris-Sud, Gif-sur-Yvette, France
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– name: 6 INRA, IRHS, PRES UNAM, SFR QUASAV, Beaucouzé, France
– name: 11 Department of Plant Pathology, Shandong Agricultural University, Taian, China
– name: 10 Biological Institution, Tomsk State University, Tomsk, Russia
– name: 4 Plant Research International, Wageningen UR Plant Breeding, Wageningen, The Netherlands
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  surname: Cornille
  fullname: Cornille, Amandine
  email: amandine.cornille@gmail.com
  organization: CNRS, Laboratoire Ecologie Systématique et Evolution - UMR8079, Orsay, France. amandine.cornille@gmail.com
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22589740$$D View this record in MEDLINE/PubMed
https://hal.science/hal-01209929$$DView record in HAL
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ContentType Journal Article
Copyright COPYRIGHT 2012 Public Library of Science
2012 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: Cornille A, Gladieux P, Smulders MJM, Roldán-Ruiz I, Laurens F, et al. (2012) New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties. PLoS Genet 8(5): e1002703. doi:10.1371/journal.pgen.1002703
Distributed under a Creative Commons Attribution 4.0 International License
Cornille et al. 2012
Wageningen University & Research
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– notice: 2012 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: Cornille A, Gladieux P, Smulders MJM, Roldán-Ruiz I, Laurens F, et al. (2012) New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties. PLoS Genet 8(5): e1002703. doi:10.1371/journal.pgen.1002703
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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.
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Snippet 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...
  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...
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StartPage e1002703
SubjectTerms Agriculture
allele frequency data
ancestors
appels
Appels, peren
Apple
apples
Apples, Pears
approximate bayesian computation
Asia
Biology
Breeding
China
Crops
domesticatie
Domesticatie van cultuurgewassen
Domestication
Europe
Evolution, Molecular
Forests
Fruit - genetics
fruit tree
Fruits
Gene Flow
Genetic aspects
Genetic diversity
Genetic Variation
genetische bronnen van plantensoorten
genetische diversiteit
Genome, Plant
Genomes
genus malus
Life Sciences
Malus - genetics
malus domestica
microsatellite markers
Microsatellite Repeats
molecular-genetics
multilocus genotype data
Phylogeography
Physiological aspects
Plant Domestication
plant genetic resources
population-structure
Spain
spondias-purpurea
Studies
sylvestris l. mill
voorouders
wild relatives
wilde verwanten
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Title 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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http://dx.doi.org/10.1371/journal.pgen.1002703
Volume 8
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