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TIGS 1094r 1 1 19 2 Highlights 20 3 21 4 Trends in Genetics xxx (2013) xxx–xxx 22 5 The domestication and evolutionary ecology of apples 23 6 1,2 1,2 3 4 1,2 24 Amandine Cornille , Tatiana Giraud , Marinus J.M. Smulders , Isabel Rolda´ n-Ruiz , and Pierre Gladieux 7 25 1 8 Centre National de la Recherche Scientifique (CNRS), Unite´ Mixte de Recherche (UMR) 8079, Baˆ timent 360, 91405 Orsay, France 26 2 Universite´ Paris Sud, UMR 8079, Baˆ timent 360, 91405 Orsay, France 9 3 27 Plant Research International, Wageningen University and Research centre (UR) Plant Breeding, Wageningen, The Netherlands 10 4 28 Growth and Development Group, Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Melle, Belgium 11 29 12 Several wild crabapples have contributed to the genome of the domesticated apple. 30 13 The domesticated apple now constitutes a panmictic, well-separated species. 31 14 Apple breeding methods have played a major role in the history of the domesticated apple. 32 15 Crabapples are threatened by introgression from domesticated apples. 33 16 Apple is an ideal study system for unraveling adaptive diversification processes. 34 17 35 18 36 TIGS 1094 1–9 Review 1 62 2 63 3 64 4 The domestication and evolutionary 65 5 66 6 67 7 ecology of apples 68 8 69 1,2 1,2 3 9 70 Q1 Amandine Cornille , Tatiana Giraud , Marinus J.M. Smulders , 10 4 1,2 71 Isabel Rolda´ n-Ruiz , and Pierre Gladieux 11 72 1 12 Centre National de la Recherche Scientifique (CNRS), Unite´ Mixte de Recherche (UMR) 8079, Baˆ timent 360, 91405 Orsay, France 73 2 13 Universite´ Paris Sud, UMR 8079, Baˆ timent 360, 91405 Orsay, France 74 3 14 Plant Research International, Wageningen University and Research centre (UR) Plant Breeding, Wageningen, The Netherlands 75 4 15 Q2 Growth and Development Group, Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Melle, Belgium 76 16 77 17 78 18 The cultivated apple is a major fruit crop in temperate cultivars of largely unknown history and pedigree [2,3]. 79 19 zones. Its wild relatives, distributed across temperate Apples are self-incompatible, and it must soon have be- 80 20 Eurasia and growing in diverse habitats, represent po- come apparent that offspring grown from seed frequently 81 21 tentially useful sources of diversity for apple breeding. did not resemble the mother apple tree. This high degree of 82 22 We review here the most recent findings on the genetics variability of the progeny, combined with a long juvenile 83 23 and ecology of apple domestication and its impact on phase, probably complicated and slowed the artificial se- 84 24 wild apples. Genetic analyses have revealed a Central lection of interesting phenotypes by early farmers. The 85 25 Asian origin for cultivated apple, together with an un- introduction of vegetative propagation by grafting, and 86 26 expectedly large secondary contribution from the Euro- the selection of dwarfed apple trees for use as rootstocks, 87 27 pean crabapple. Wild apple species display strong were thus key events in the history of apples, facilitating 88 28 population structures and high levels of introgression 89 29 from domesticated apple, and this may threaten their Glossary 90 30 genetic integrity. Recent research has revealed a major 91 Crabapple: wild apple species, usually producing profuse blossom and small 31 role of hybridization in the domestication of the culti- 92 acidic fruits. The word crab comes from the Old English ‘crabbe’ meaning bitter vated apple and has highlighted the value of apple as an 32 or sharp tasting. Many crabapples are cultivated as ornamental trees and their 93 33 ideal model for unraveling adaptive diversification pro- apples are sometimes used for preserves. In Western Europe the term crabapple 94 is often used to refer to Malus sylvestris (the European crabapple), in the 34 cesses in perennial fruit crops. We discuss the implica- 95 Caucasus this term refers to M. orientalis (the Caucasian crabapple) and, in 35 tions of this knowledge for apple breeding and for the Siberia, to M. baccata (the Siberian crabapple). The native North American 96 36 conservation of wild apples. crabapples are M. fusca, M. coronaria, M. angustifolia, and M. ioensis. Malus 97 37 sieversii, the main progenitor of the cultivated apple, is usually not referred to as 98 a ‘crabapple’. The genus Malus as a model system for understanding 38 Diachronic: changing over time. 99 39 fruit tree evolution Germplasm: collection of genetic resources for a species. 100 Hybridization: the process of interbreeding between individuals from different 40 Apple (Malus domestica Borkh) is one of the most impor- 101 gene pools. 41 tant fruit crops in temperate regions worldwide in terms of Introgression: the transfer of genomic regions from one species into the gene 102 42 production levels (http://faostat.fao.org/), and it occupies a pool of another species through an initial hybridization event followed by 103 repeated backcrosses. 43 central position in folklore, culture, and art [1]. Dessert 104 Isolation by distance: pattern of correlation between genetic differentiation and 44 apples are popular because of their taste, nutritional prop- geographic distance, resulting from a balance between genetic drift and 105 45 erties, storability, and convenience of use. Apple-based dispersal. 106 Panmictic group: random mating population. 46 beverages such as ciders have been consumed for centuries 107 QTL mapping: identification of genomic regions governing a phenotypic trait 47 by the peoples of Eurasia, even before the advent of the by the statistical association of molecular markers with the phenotypic trait in a 108 population derived from a cross between two or more parental lines (a 48 cultivated apple. Humans have been exploiting, selecting, 109 ‘segregating population’) or in a population of unrelated individuals (an and transporting apples for centuries, and several thou- 49 ‘association mapping population’). 110 50 sand apple cultivars have been documented [2]. Much of Rootstocks: part of a plant (usually the underground part) onto which a graft is 111 fixed. In apples, the genotypes of the rootstocks used often result in dwarf 51 the diversity present in domesticated apples is currently 112 apple trees. maintained in germplasm (see Glossary) repositories 52 Self-incompatible: a plant incapable of self-fertilization because its own pollen 113 53 and amateur collections, including a broad spectrum of is prevented from germinating on the stigma or because the pollen tube is 114 54 blocked before it reaches the ovule. 115 Simple sequence repeats (SSR): in other words microsatellites, the repetition Corresponding author: Cornille, A. ([email protected]). 55 in tandem of di-, tri- or tetranucleotide motifs. 116 Keywords: QTL; archaeological record; crabapple; genome; microsatellites; Malus SSR marker (or microsatellite marker): a marker based on PCR amplification 56 domestica. 117 57 and separation of SSR alleles with differences in repeat length. 118 0168-9525/$ – see front matter Vegetative propagation: natural or assisted asexual reproduction in plants 58 ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tig.2013.10.002 through the regeneration of tissues or plant organs from one plant part or 119 59 tissue. Natural vegetative propagation methods include bulbs or corms, for 120 example. Horticultural vegetative propagation may involve stem or root 60 121 cuttings or grafting. Grafting is often used for the propagation and 61 maintenance of cultivars of interest in perennial fruit crops. 122 Trends in Genetics xx (2013) 1–9 1 TIGS 1094 1–9 Review Trends in Genetics xxx xxxx, Vol. xxx, No. x 123 184 the selection and propagation of superior genotypes de- of habitats and environmental conditions in which wild 124 185 rived from open-pollination progenies (i.e., ‘chance seed- apples grow.