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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
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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.
125 186
lings’) [4], and improving control over the size of mature
126 187
apple trees [1]. Despite the immense diversity of cultivars The status and genetic integrity of cultivated and wild
127 188
available, apple production worldwide is now largely based apple taxa
128 189
on the cultivation of a few dozen ornamental and edible The apple belongs to the Rosaceae family, as do other major
129 190
cultivars, grafted onto less than a dozen different clonal temperate fruit tree species (e.g., pear, apricot, peach,
130 191
rootstocks, with high levels of chemical inputs. plum, cherry, almond). The genus Malus consists of about
131 192
Wild Malus taxa constitute a useful source of variation 30 species and several subspecies, but the taxonomy of this
132 193
for apple breeding. They are also of ecological importance genus is complex, unclear, and likely to be revised in the
133 194
as a source of food for wildlife or as components of hedges in future [5]. Species delimitation in apples is hampered by
134 195
agricultural landscapes and, as such, they make a signifi- the paucity of diagnostic morphological features [6], the
135 196
cant contribution to ecosystem services. The use of these fact that records are lacking concerning the geographic
136 197
natural resources in breeding and the development of range of some taxa, and the prevalence of hybridization
137 198
effective conservation programs require a good under- between species. Hybridization among apples is facilitated
138 199
standing of the genetic relationships within and between by a lack of interspecific reproductive barriers, self-
139 200
cultivated and related wild Malus taxa. More generally, incompatibility, and the cultivation of apple in areas in
140 201
the cultivated apple and its wild relatives constitute a which wild apple populations occur naturally [7–11].
141 202
suitable model system for studies of the domestication of The cultivated (or ‘sweet’) apple is usually designated
142 203
long-lived perennial crops, about which much less is known as M. pumila Mill. or M. domestica Borkh., but many other
143 204
than for seed-propagated annual crops. synonyms, now considered illegitimate, have been used.
144 205
Recent population studies have provided insight into The name M. pumila seems to be more legitimate in terms
145 206
the origins of the cultivated apple, its domestication his- of the rules of botanical nomenclature, but M. domestica is
146 207
tory, and its spread by human populations, the status and the name most widely used, and this name will be
147 208
genetic integrity of its wild relatives, and the response to used here. Malus domestica belongs to the section Malus,
148 209
selection of these long-lived perennials. We review here one of the five sections within the genus Malus, and is a
149 210
recent progress in studies of the origin and diversity of diverse crop species containing a large number wild-
150 211
cultivated apple and its wild relatives. We also explore introgressed individuals and feral populations [12]. The
151 212
future prospects for increasing our understanding of the cultivated apple was initially domesticated from the wild
152 213
nature and genetic architecture of the phenotypic changes apple Malus sieversii (Ldb.) Roem in the Tian Shan Moun-
153 214
associated with apple domestication across the wide range tains in Central Asia [11,13–15]. People then took the 154 215 155 216 156 (A) 217
157 218
158 0 200 400 km 219 159 220 160 221 161 2 1 222 162 Origin: an shan 223 Malus sylvestris Hybridiza on 163 along the Silk Routes Malus sieversii 224 164 225 165 Malus domes ca (B) 226 166 227 167 Malus orientalis 228 Gene c markers 168 229 SSR* and chloroplast genome 169 230 SSR 170 231 SSR, chloroplast, and nuclear sequences 171 *SSR: simple sequence repeats (microsatellites) 232 172 233 173 234 1 174 10 000–4000 ya 235 2 175 4500–1500 ya 236 2 176 Hybridiza on between wild and cul vated apples 1500 ya 237 177 Crop-to-wild hybridiza on 238
Bidirec onal hybridiza ons 100 ya 178 BACC SIEV DOM OR SYL 239
179 TRENDS in Genetics 240
180 241
181 Figure 1. Evolutionary history of the cultivated apple. (A) This history was revealed by recent population studies using different types of molecular markers for evolutionary 242
inferences. (1) Origin in the Tian Shan Mountains from M. sieversii, followed by (2) dispersal from Asia to Europe along the Silk Route, facilitating hybridization and
182 introgression from the Caucasian and European crabapples. Arrow thickness is proportional to the genetic contribution of various wild species to the genetic makeup of 243
183 Malus domestica. (B) Genealogical relationships between wild and cultivated apples. Approximate dates of the domestication and hybridization events between wild and 244
cultivated species are detailed in the legend. BACC, Malus baccata; DOM, Malus domestica; OR, Malus orientalis; SIEV, Malus sieversii; SYL, Malus sylvestris; ya, years ago.
2
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245 306
domesticated apples westwards along the great trade (except for M. sieversii) in a wide range of habitats and
246 307
routes known as the Silk Route (Figure 1), where they environmental conditions ( Box 1).
247 308
came into contact with other wild apples, such as Several recent studies have used molecular markers to
248 309
M. baccata (L.) Borkh. in Siberia, M. orientalis Uglitz. investigate the diversity, structure, and dispersal capaci-
249 310
in the Caucasus, and M. sylvestris Mill. in Europe ( Box 1). ties of wild apple relatives (Box 2) other than M. baccata,
250 311
These three crabapple species and M. sieversii are consid- which has been little studied to date. They have provided
251 312
ered to be the closest relatives of M. domestica, with which highly relevant and timely information, helping to identify
252 313
they are fully interfertile [12]. The four wild apple rela- and protect germplasm sources for apple breeding for traits
253 314
tives are widely distributed across temperate areas in such as resistance to pathogens (e.g., Venturia inaequalis,
254 315
Eurasia where they often grow as low-density populations the fungus causing apple scab, [16]). Population genetic 255 316 256 317
257 318
258 Box 1. Ecology of wild relatives of the cultivated apple 319
259 320
Three decades of field sampling expeditions in Eurasia by different occur sporadically across an area comprising Turkmenistan, Uzbeki-
260 research groups have provided a clearer picture of the geographic stan, Tajikistan, and northeastern Afghanistan (Figure I). Malus 321
261 distributions and ecology of wild apple relatives (Figure I). The four sieversii populations experienced severe overharvesting during the 322
262 wild apple species, M. sylvestris, M. orientalis, M. sieversii, and Soviet era, and the remaining populations are further threatened by 323
M. baccata, are mostly pollinated by bees and flies [36,51]. Diverse forest destruction [18].
263 324
wild animals, including mammals and large birds, feed on the fruits, Malus sylvestris Mill. occurs across Western and Central Europe
264 325
but their respective efficiencies as seed-dispersal vectors are un- [52] (Figure I). The European crabapple has a high light requirement,
265 known [1,36]. The wild apple species bear plentiful fragrant white resulting in its occurrence mostly at forest edges, in farmland 326
266 flowers and red to yellow fruits of about 1–6 cm in diameter (Figure I) hedges , and on marginal sites. It grows on almost all soils but 327
267 that are variable in shape, color, and taste. The fruits of M. orientalis, prefers the wet edge of the forest (http://www.euforgen.org/). This 328
M. baccata (http://www.efloras.org/), and M. sylvestris are edible and species has suffered from the abandonment of coppicing, a
268 329
were probably already used before the spread of cultivated apple [1]. traditional forest management practice designed to rejuvenate old
269 Malus sieversii (Ldb.) Roem grows at intermediate elevations trees or shrubs by cutting them to ground level, thus promoting the 330
270 (typically 900–1600 m) in the mountainous regions of Central Asia, regeneration of new stems from the base. The European crab apple 331
271 and is extremely variable in growth habit, height, fruit quality, and is now considered endangered in Belgium, the Czech Republic, and 332
272 fruit size [1,10,35]. Trees growing in this area, on their own roots, can Germany [52]. 333
bear fruit approaching the size of commercial cultivars (i.e., >60 mm Malus orientalis Uglitzh occurs in the Caucasian region (Turkey,
273 334
diameter), with excellent characteristics that are highly appreciated Armenia, Georgia, and southwestern Russia) but little is known about
274 locally. Currently, M. sieversii remains in only a few small intact its ecology (Figure I). 335
275 forests of no more than several hundred hectares in extent in the Tian Malus baccata occurs across Siberia and South Asia (India, 336
276 Shan, at the border of Kazakhstan and China, in southern Kazakhstan, Pakistan, Nepal) and is probably relatively cold-tolerant, although 337
277 with further small stands in Kyrgyzstan (Figure I). It is also reported to little is known about its ecology (Figure I). 338 278 339 279 340 280 341 281 342 Malus sylvestris Malus baccata
282 343 Diameter: 1–3 cm Diameter: 1 cm 283 344 284 345 285 346
286 347
287 0 200 400 km 348 288 349 Ο >30 289 ο 10 350 290 ο 1 351 291 352 292 353 293 354 294 355 295 356 296 Malus orientalis Malus sieversii 357 297 Diameter: 2–4 cm Diameter: up to 6 cm 358 298 359 299 360 300 361 301 362 302 TRENDS in Genetics 363
303 364
Figure I. Distribution and key morphological features of wild apples. The distribution of species can be inferred from the geographic origin of accessions included in
304
published studies: Malus sylvestris (blue) [15,17,20,34,36,36], Malus orientalis (yellow) [15,17,20–22], Malus sieversii (red) [5,14,15,17–20,53], and Malus baccata (purple) 365
305 [15]. Disk areas are proportional to the number of accessions. Pictures of the fruit of the different wild apples are provided, as well as their respective diameters. 366
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367 428
368 Box 2. Phylogeography, population structure, and dispersal of wild apples 429
369 The population structure of the four wild apple species has recently [20]. Comparison of the population structure of M. sieversii with that 430
370 been investigated with microsatellites [17,19,34]. A weak spatial of one of its major fungal pathogens, Venturia inaequalis, revealed 431
371 genetic population structure was detected for each species, consistent similar patterns of genetic differentiation in the M. sieversii forests of 432
with the high level of interpopulation gene flow. Estimates of the eastern mountains of Kazakhstan [54]. This correspondence
372 433
historical gene flow have suggested that wild apple relatives have suggests possible co-structuring of the populations of the main apple
373 high dispersal capacities, but further investigations of contemporary progenitor, M. sieversii, and its chief pathogen. The use of another 434
374 and historical pollen and seed dispersal distances are required. dataset (949 individuals) [19] revealed stronger population differen- 435
375 The European crabapple, Malus sylvestris, is the wild apple relative tiation in Kazakhstan than previously reported [20], with two large 436
376 with the most thoroughly investigated biogeographic history. Malus populations and two others with narrow distributions. The difference 437
sylvestris experienced range contraction in glacial refugia in Southern in sampling density (101 versus 949 individuals, respectively) may
377 438
Europe during the last glacial maximum. At the beginning of the account for these apparent differences in population structure.
378 Holocene, when the climate became warmer in Europe, it recolonized Malus orientalis displays a weak north–south spatial genetic 439
379 northern Europe. Three main populations have been identified – in structure, with three distinct populations: a large population corre- 440
380 Western Europe, around the Carpathian Mountains, and in the Balkan sponding to most of the Armenian samples and two more narrowly 441
Peninsula – with admixture in their suture zones [17]. Further distributed populations, one in the Southern Caucasus (Turkey and
381 442
investigation, including high-density sampling in France, has re- southern Armenia) and the other at more northerly latitudes (in Russia).
382 vealed an alternative structure, with five distinct clusters in Italy, The population structure of M. baccata has not yet been investi- 443
383 Western France/Great Britain/Belgium, Eastern France, Sweden/ gated, mainly due to the lack of samples across its distribution. 444
384 Denmark/Norway, and the Balkans (Cornille et al., unpublished). The four wild relatives may have geographic distributions contig- 445
385 Malus sieversii exists as a main population spread over Central Asia uous with those of other wild species [1], but detailed information 446
and a smaller population (101 individuals) in the Tian Shan Mountains about the distribution of these other wild populations is lacking. 386 447 387 448
388 449
analyses of large collections of wild apple relatives have through adaptive introgression, because S locus alleles that
389 450
uncovered signatures of postglacial recolonization from introgress from a closely related species, if rare in the
390 451
distinct glacial refugia in M. sylvestris [17], and high levels recipient species, can rapidly spread by positive selection
391 452
of diversity and complex population structures in M. sie- [24,25].
392 453
versii [10,18–20] and M. orientalis [20–23]. Genetic data Population genetic methods are increasingly used to
393 454
have also revealed weak isolation by distance (Box 2). resolve taxonomic uncertainties or to identify misclassified
394 455
Ubiquitous and high levels of introgression from domesti- germplasm in apple collections. Admixture analyses have
395 456
cated apple were found in three of the four wild apple revealed that M. kirghisorum, the wild apple from the
396 457
relatives ( Box 3), revealing a threat to their genetic forests of Kyrgyzstan, and M. asiatica, the apple formerly
397 458
integrity. Thus, wild apple relatives clearly have a high cultivated in China, are in fact indistinguishable from
398 459
dispersal capacity, and the widespread cultivation of do- M. sieversii [14]. Multilocus microsatellite typing of the
399 460
mesticated apples in temperate latitudes has promoted US Department of Agriculture (USDA)–Agricultural Re-
400 461
extensive crop-to-wild gene flow. The mating system of search Service (ARS)–NPGS (National Plant Germplan
401 462
apple species, characterized by a self-incompatibility System) collection (Geneva, USA) suggested that hybrids
402 463
mechanism that ensures outbreeding, may have played and misclassifications may also be common in germplasm
403 464
a crucial role in these introgressions. This mechanism is repositories [26,27]. Further surveys of the diversity and
404 465
controlled by a single locus, the S locus, with a large distribution of ‘wild’ apples should facilitate the conserva-
405 466
number of alleles, up to several hundred in some species. tion of wild genetic resources in situ (e.g., conservation of
406 467
In apples, individual trees can only mate with other indi- genetically differentiated populations) or ex situ (e.g., es-
407 468
viduals with different S alleles. The self-incompatibility of tablishment of core collections of pure wild individuals,
408 469
apples may thus have favored interspecific hybridization maximizing genetic diversity), ultimately enabling their
409 470
and introgression not only by forcing outcrossing, but also optimal use [27,28]. 410 471
411 472
412 Box 3. Crop-to-wild gene flow in apple 473
413 Self-incompatibility and large dispersal capacities make the genus and introgression from the cultivated apple to M. sylvestris. Recent 474
414 Malus an outstanding system for the study of crop-to-wild and studies have also investigated crop-to-wild gene flow from modern 475
415 interspecific gene flow. The differentiation between domesticated and commercial varieties imported from Western countries to M. sieversii 476
wild gene pools makes it possible to track cultivated varieties with and M. orientalis [15,20]. Introgression from the cultivated apple
416 477
genetic tools, facilitating inferences about population history such as into the wild progenitor M. sieversii, and to a lesser extent into
417 movement, population subdivision, hybridization, and introgression, M. orientalis, has also been detected. The high potential for crop-to- 478
418 for example. wild gene flow must be considered in the management of wild apple 479
419 Multilocus microsatellite typing and Bayesian clustering methods, resources. 480
420 making use of the differentiation between domesticated and wild Phenotypic data have been reported in parallel with genetic data 481
gene pools, recently revealed the existence of extensive crop-to-wild and have been compared between wild and cultivated apple species
421 482
gene flow in apples [20,27,34,36,41]. Most studies have focused on (Table 1). The results obtained for molecular markers matched, to
422 M. domestica to M. sylvestris gene flow (Table 1). Statistical models some extent, the morphological traits studied, but no clear-cut 483
423 investigating the factors (environmental and human) influencing the morphological criteria distinguishing clearly between cultivated apple 484
424 extent of crop-to-wild introgression in apple (gene flow from and the European crabapple were identified [34,36]. Comparisons of 485
425 M. domestica to the European crabapple) have revealed a significant phenotypic data showed that admixed M. sieversii individuals had, on 486
positive effect of the number of apple orchards on crop-to-wild average, larger fruits than ‘pure’ wild individuals [27]. However, it is
426 487
introgression rates in the European crabapple (Cornille et al., difficult to determine the extent to which these admixed individuals
427 unpublished). Thus, human activity influences rates of hybridization are actually feral trees. 488
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489 a 550
Table 1. Crop-to-wild gene flow in apple
490 551
Species N Geographic area DNA Percentage Phenotypic data Ref. 491 b 552
marker of hybrids
492 553
Malus sylvestris 44 Belgium, Germany SSR, AFLP 6.8 Hairiness of the underside of the leaf [34]
493 554
Malus sylvestris 178 Denmark SSR 11.2 Fruit diameter, fruit color, pubescence of [36]
494 terminal part of long shoots, pubescence of 555
495 abaxial surface of leaves from long shoots, 556
496 and pubescence of abaxial surface of leaves 557
497 from spur shoots 558
159 Netherlands, Belgium SSR 17 – [41]
498 Malus sylvestris 559
Malus sylvestris 61 Germany, Macedonia SSR 19.7 [27]
499 560
Malus orientalis 46 Russia, Turkey 13.0
500 561
Malus sieversii 118 Kazakhstan 14.4 Mean fruit weight, length, and width
501 562
Malus sylvestris 796 Austria, Belgium, SSR 36.7 – [20] 502 563 Bosnia Herzegovina,
503 Bulgaria, Denmark, 564
504 France, Germany, 565
505 Great Britain, Hungary, 566
Italy, Norway, Poland, 506 567
Romania, Ukraine
507 568
Malus orientalis 217 Turkey, Armenia, Russia 3.2 –
508 569
Malus sieversii 101 Kazakhstan, China, Kyrgyzstan, 14.8 –
509 Tajikistan and Uzbekistan 570
a
510 Material features of each study: sampling size (N), geographic area covered, wild species, molecular and phenotypic data used. 571
b
511 AFLP, amplified fragment length polymorphisms; SSR, simple sequence repeats. 572 512 573 513 574
514 575
The enduring riddle of the genetic makeup of cultivated improvement’, in which breeders intentionally carry out
515 576
apples crosses for the selection of new traits in crop varieties [32].
516 577
Do ‘domesticated’ apples actually exist? Furthermore, crop improvement traits are typically vari-
517 578
The debate concerning whether a crop or animal ‘species’ able among the cultivars of a crop [33]. The modern breed-
518 579
should be considered ‘domesticated’ is similar to that re- ing phase can thus complicate studies of the genetic basis
519 580
garding the species concept [29]. Definitions of the bound- of phenotypic changes occurring during the initial domes-
520 581
aries of domesticated taxa are essential in studies of tication phase. However, it is theoretically possible to
521 582
domestication because the classification of domestication- distinguish between the two phases of the evolution of
522 583
related traits and of the underlying genes can have a domesticated plants by inferring the age and origin of
523 584
major impact on evolutionary inferences. De Queiroz [6] alleles contributing to agronomically important traits.
524 585
argued that all modern biologists agree that species corre- Analyses of population structure based on comprehen-
525 586
spond to segments of evolutionary lineages evolving sive samples of cultivated and wild gene pools have
526 587
independently from each other. The seemingly endless dis- revealed that the cultivated apple forms a distinct, pan-
527 588
pute about species concepts stems from the confusion be- mictic group, well separated from its Central Asian pro-
528 589
tween species definition and species criteria, with different genitor, M. sieversii, with similar levels of genetic variation
529 590
recognition criteria corresponding to different events occur- in the two groups [15,27]. Divergent selection between wild
530 591
ring during lineage divergence, rather than to fundamental and cultivated gene pools, extensive selection on domes-
531 592
differences in what is considered to represent a species [6]. ticates by humans outside the center of origin of the crop,
532 593
Applying a similar reasoning to the domestication process, and vegetative propagation have all contributed to a
533 594
domesticated species can be defined as segments of evolu- reduction of gene flow between cultivated apples and
534 595
tionary lineages diverging from their wild progenitors in their progenitors, and the resulting pattern of clear popu-
535 596
response to artificial selection pressures and human con- lation differentiation provides definitive evidence for the
536 597
trol over reproduction. Domestication, similarly to speci- domesticated ‘nature’ of apples. Several studies have in-
537 598
ation, is often quantitative in nature, and different means vestigated phenotypic variation in close relatives of
538 599
of quantifying lineage independence can be used to mea- M. domestica[10,23,27,34–36] but, to the best of our knowl-
539 600
sure different arbitrary ‘stages’ along this continuum edge, no attempt has been made to quantify the morpho-
540 601
[29–31]. The later stages of divergence along the domesti- logical and physiological changes associated with apple
541 602
cation continuum are characterized by the fixation of domestication. These phenotypic changes are expected to
542 603
marked discontinuities between crops and their wild be weaker in apples and other long-lived perennial fruit
543 604
ancestors (i.e., ‘domestication syndrome’) which can be crops than in seed-propagated annuals because the lengthy
544 605
used to classify plants categorically as ‘domesticated’. juvenile phase and the use of grafting make domestication
545 606
Earlier stages of divergence are more readily detected more recent, at least in terms of the number of generations
546 607
with rapidly evolving genetic markers. [37]. Nevertheless, several traits clearly distinguish do-
547 608
The domestication process, which typically involved mesticated long-lived perennials from their wild ancestors
548 609
open pollination and unconscious selection over thousands (see below), and the phenotypic changes associated with
549 610
of years, has been followed by the recent process of ‘crop domestication may parallel those in annual crops [30].
5
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Review Trends in Genetics xxx xxxx, Vol. xxx, No. x
611 672
Archaeological evidence route of spread of apple cultivation) have been recon-
612 673
Several scholars have evaluated the archaeological and structed from panels of markers tracing back different
613 674
historical evidence relating to the origin and use of apples evolutionary timescales (i.e., chloroplast, nuclear, and mi-
614 675
[1–3,12]. Evidence for the collection of wild apples has been crosatellite markers). These genetic markers have
615 676
found at Neolithic and Bronze Age archaeological sites revealed original patterns of diversity and differentiation
616 677
across Europe. Similar evidence suggesting the early use within cultivated apple, and non-trivial relationships with
617 678
of apples in Western and Central Asia is lacking, but some its wild relatives. The various steps in the domestication of
618 679
‘anomalies’ in the distribution of M. domestica, such as apple unraveled by the analysis of genetic markers are
619 680
isolated patches of large sweet apples (i.e., different from outlined below.
620 681
native bitter crabapples) in the Caucasus Mountains, the (i) Origin in the Tian Shan Mountains of Central Asia:
621 682
Crimean Peninsula, parts of Afghanistan, Iran, Turkey, was Malus sieversii the progenitor?
622 683
and the Kursk region of European Russia, and the large, The morphological similarity between M. domestica
623 684
possibly 3000-year-old apple discovered at Navan Fort and M. sieversii, and the extraordinary diversity of
624 685
(Northern Ireland), might be hallmarks of early apple wild apples in Kazakhstan, were first reported by
625 686
seedling imports from Central Asia [1]. Advances in an- Vavilov [13] and then by Ponomarenko (1983, cited in
626 687
cient DNA technology should facilitate diachronic investi- [39]). These findings were recently confirmed by
627 688
gations of the domesticated status of apple seed remains in collaborative collection expeditions involving Ameri-
628 689
the Neolithic and Bronze Age archaeological record across can, European, and Central Asian scientists
629 690
Eurasia, providing information about the transition from [10,14,15,39]. The genetic data were found to be
630 691
gathering to cultivation. The recent amplification of ribo- consistent with these morphological observations.
631 692
somal DNA from apple remains – seed coat (testa) and Initial phylogenetic analyses of chloroplast and
632 693
pericarp – preserved in waterlogged layers from a Roman nuclear sequences confirmed a progenitor–descendant
633 694
site in Switzerland suggests that it may be feasible to relationship, with M. sieversii–M. domestica being the
634 695
identify wild and domesticated apple from the archaeolog- pair of species most closely related genetically, based
635 696
ical record [38]. Insight into the human behavior responsi- on sequences, and possibly not even distinguishable,
636 697
ble for the changes associated with domestication can also but conclusions about the origin of this crop were
637 698
be gained by studying current practices such as the exploi- hampered by the lack of strong statistical support
638 699
tation of wild apples in some areas of Western and Central and/or limited sample size [11,14]. Analyses of
639 700
Asia. microsatellite data [i.e., simple sequence repeat (SSR)
640 701
Grafting, as a handy way to propagate elite cultivars, markers] for a comprehensive collection of wild and
641 702
has probably played a key role in the spread of apple as a cultivated apples have provided new insight, revealing
642 703
major fruit crop worldwide [1,11]. Grafting is a practice that M. domestica forms a distinct, panmictic group,
643 704
that is thought to have begun about 3800 years ago based well separated from M. sieversii [15,40]. This may
644 705
on a cuneiform description of budwood importation for indicate that the populations of M. sieversii from which
645 706
grape in Mesopotamia. Indirect evidence has been the crop was domesticated have yet to be identified or
646 707
obtained for the cultivation of apples 3000 years ago in may no longer exist. Malus sieversii is unusual in that
647 708
Mesopotamia [12], but the most compelling evidence for it grows at high density over large areas, but these
648 709
horticulture and for apple cultivation dates from the Greek forests have been decimated since Vavilov reported
649 710
period (i.e., from about the 3rd century BC) [1]. The Ro- their existence. The substantial genetic differentiation
650 711
mans probably learned apple grafting, cultivation, har- between M. domestica and M. sieversii may also result
651 712
vesting, and storage from the Greeks, and brought the from a combination of genetic drift and introgressions
652 713
production chain technology to the rest of their empire. from other wild apple species, erasing the genetic
653 714
Dwarf apple trees were known 2300 years ago, and dwarf- footprints of the initial contribution of M. sieversii.
654 715
ing rootstocks were probably brought to the West from the Genomic studies and further sampling of wild apple
655 716
Caucasus. In the 19th century, dwarfing clones known as and cultivar diversity should provide quantitative and
656 717
Paradise (or French Paradise) or Doucin (or English Para- qualitative insight into the origin of M. domestica, and
657 718
dise) were common in Europe, before the East Malling improve our understanding of the genetic architecture
658 719
Research Station in England created a standardized col- and basis of the phenotypic changes selected during
659 720
lection of 10 rootstocks with new names. Two of the original domestication and subsequent crop improvement.
660 721
East Malling selections, M9 (Paradis Jaune de Metz) and (ii) Diversification of the domesticated apple along the Silk
661 722
M7 (Doucin Reinette), are still widely used by horticultur- Route
662 723
ists worldwide. Several studies have highlighted the importance of the
663 724
European crabapple, M. sylvestris, in the evolution
664 725
Genetic evidence and diversification of the cultivated apple and, to a
665 726
Having originated from M. sieversii in Central Asia about lesser extent, that of the Caucasian crabapple M.
666 727
4000 to 10 000 years ago, the cultivated apple then under- orientalis, through the use of microsatellite markers
667 728
went hybridization with its wild relatives during its spread and nuclear or chloroplast sequences [15,36,41,42].
668 729
from the Tian Shan mountains westward along the Silk Malus sieversii was probably the initial progenitor, but
669 730
Route (Figure 1). The different timescales of the domesti- other wild apple species subsequently contributed to
670 731
cation process (ancient initial domestication in Central the genetic makeup of cultivated apple through
671 732
Asia followed by more recent hybridization during the introgressive hybridization, affecting both nuclear
6
TIGS 1094 1–9
Review Trends in Genetics xxx xxxx, Vol. xxx, No. x
733 794
and chloroplast DNA, during its dispersal westwards
These traditional methods may have contributed to a
734 795
along the Silk Route (Figure 1). These introgressions
high level of diversity in the cultivated gene pool, but
735 796
obscure the signal of any initial bottleneck occurring
current breeding practice methods, in which a small set
736 797
during the original domestication of M. domestica.
of cultivars is common to the pedigree of many new culti-
737 798
Introgression has been so extensive that M. domestica
vars, may be eroding the genetic diversity available in the
738 799
now appears to be more similar genetically to the
cultivated genepool. For instance, a genetic analysis of a
739 800
European crabapple M. sylvestris than to the Asian
comprehensive sample of commercial cultivars revealed
740 801
wild apple M. sieversii on the basis of microsatellite
extensive first-, second- and third-degree relationships
741 802
markers [15]. Most, but not all, apple cultivars now
between popular apple varieties [43], as previously
742 803
also appear to contain the chloroplast genome of
reported for grape [44]. This highlights the need to make
743 804
M. sylvestris [42]. Genetic evidence has also demon-
better use of the diversity in apple germplasm [28,45].
744 805
strated that current cider cultivars, which usually
Conversely, the current situation may also reflect the
745 806
produce smaller fruits that are more bitter than those
extensive use of genetic diversity by breeders, but with
746 807
of dessert cultivars, are not the cultivars genetically
the cultivars generated replacing each other in the produc-
747 808
closest to M. sylvestris [15], as initially hypothesized.
tion area rather than being grown alongside older varie-
748 809
This hypothesis was based on the known use of
ties. This is the situation that applies for many vegetable
749 810
crabapples for the preparation of apple beverages,
and arable crops in which genetic diversity remains at a
750 811
even before apple cultivation [1], and the astringent,
high level if considered over a longer period of time.
751 812
bitter properties of these small apples, ideal for cider-
Apple phenotypes selected by humans include (i) higher
752 813
making. Dessert apple cultivars were actually found to
productivity (e.g., number of fruits, fruit size, fruit weight);
753 814
be genetically closer to M. sylvestris than cider
(ii) fruit quality (e.g., color, shape), flavor (volatile com-
754 815
cultivars in studies using nuclear microsatellite
pounds), taste (e.g., fruit acidity, sugar content, polyphe-
755 816
markers [15]. Because cider is made and consumed
nolics), texture (fruit flesh firmness), and conservation
756 817
across Eurasia, cider apple cultivars may also have
(storage behavior); (iii) easier harvesting (e.g., growth
757 818
originated in Central Asia where wild apple popula-
habit, plant size); and (iv) greater phenological congruence
758 819
tions are highly diverse in terms of color, taste, and
with agricultural practices (e.g., shorter juvenile phases,
759 size. 820
synchronicity in blooming or fruit ripening). Crop improve-
760 821
ment and cultivar diversification have affected many char-
761 822
acteristics, including juvenile phase length, cold
762 823
Breeding methods for fruit tree crops and the requirement, cold tolerance, drought tolerance, fruit tenac-
763 824
phenotypic changes associated with apple ity, and disease resistance [3]. Rootstocks may also have
764 825
domestication been subject to selection for their effects on the productivity
765 826
The life-history traits of apples make it harder to fix the of aerial parts and their role in tolerance to edaphic,
766 827
desired agronomic traits quickly in this crop than in an- climatic, and biotic conditions. The domestication and
767 828
nual seed-propagated crops. In particular, apples have improvement of cultivated apples may have benefited from
768 829
long generation times and display obligate outcrossing the high heritability of quality traits [46].
769 830
due to their self-incompatibility system. The development Quantitative trait locus (QTL) mapping has been used
770 831
of appropriate breeding methods (i.e., open-pollination to dissect the genetic architecture of several desired traits
771 832
followed by the grafting of interesting phenotypes) resulted through crosses between cultivars [47]. However, QTL
772 833
in a model of domestication fundamentally different from mapping has not been used to investigate the genetic
773 834
that for annual seed-propagated crops. architecture of domestication traits through wild Â
774 835
Theoretically, the introduction of clonal propagation domesticated biparental crosses. Given the high costs of
775 836
may have rapidly decreased the genetic diversity of culti- developing and maintaining mapping populations in apple,
776 837
vated apples because grafting permitted the genetic fixa- alternatives, such as candidate gene and bottom-up
777 838
tion of a limited set of elite clones that could only diversify approaches, relying on population genetic analyses and
778 839
by accumulating somatic mutations. However, no evidence functional information to connect selected (candidate)
779 840
of a domestication bottleneck or clonal population struc- genes to phenotypes, are likely to be the best options for
780 841
ture has been found in apple in studies considering a single identifying the genomic regions that have undergone the
781 842
representative of each variety [15]. This raises questions greatest change during domestication [48,49]. The recently
782 843
about how high levels of diversity have been maintained, released ‘Golden Delicious’ genome sequence [14], and the
783 844
and about the lack of a clonal or relatedness structure availability of large-scale genotyping tools [50], have made
784 845
between cultivars. Long-prevailing apple breeding meth- it possible to generate population-scale data for both
785 846
ods may account for this apparent paradox. If many farm- domesticated and wild apples.
786 847
ers each independently selected trees producing good fruits
787 848
from progeny arising from natural pollination (‘chance Concluding remarks
788 849
seedlings’ [10]), the obligate outcrossing of the crop, the Recent studies of the evolutionary history of the domesti-
789 850
isolation of farms, and differences in taste preferences cated apple and its wild relatives have shown this to be an
790 851
across regions may have been powerful forces driving outstanding biological model for exploring the evolutionary
791 852
the maintenance of high levels of variation. The occasional process at work during domestication. Full-genome rese-
792 853
selection of plants resulting from hybridization with wild quencing and reference-assisted de novo assembly of do-
793 854
relatives would have further increased diversity. mesticated and wild apple genomes will undoubtedly
7
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855 916
5 Robinson, J.P. et al. (2001) Taxonomy of the genus Malus Mill.
provide further insight into the history of this remarkable
856 917
(Rosaceae) with emphasis on the cultivated apple, Malus domestica
crop, facilitating the genetic dissection of agronomically
857 Borkh. Plant Syst. Evol. 226, 35–58 918
and ecologically relevant traits. The main limiting factor
858 6 De Queiroz, K. (1999) The general lineage concept of species, species 919
may now be the availability of suitable accessions for
859 criteria, and the process of speciation. In Endless Forms: Species and 920
evolutionary inferences and plant breeding rather than Speciation (Howard, D.J. and Berlocher, S.H., eds), pp. 49–89, Oxford 860 921
University Press
the development of genomic tools, highlighting the need for Q4
861 7 Korban, S.S. (1986) Interspecific hybridization in Malus. HortScience Q5 922
further field collections. Future sampling campaigns
862 21, 41–48 923
should focus on: (i) worldwide rootstock accessions – the
863 8 Way, R.D. et al. (1991) Apples (Malus). Acta Hort. 290, 3–46 Q6 924
origin of rootstocks is unknown despite their key role in the
864 9 Watkins, R. (1995) Apple and pear. In Evolution of Crop Plants 925
tolerance of cultivars to abiotic conditions, (ii) local and (Smartt, J. and Simmonds, N.W., eds), pp. 418–422, Longman
865 926
10 Forsline, P.L. et al. (2003) Collection, maintenance, characterization
ancient cultivars from different parts of the world (Eastern
866 and utilization of wild apples of Central Asia. Hort. Rev. 29, 1–61 Q7 927
Europe, Mediterranean, and Asia), and (iii) wild
867 11 Harris, S.A. et al. (2002) Genetic clues to the origin of the apple. Trends 928
unsampled species and populations, from Central Asia
868 Genet. 18, 426–430 929
in particular. Domestication of Plants in the Old
869 12 Zohary, D. and Hopf, M. (2000) 930
Another unanswered question concerns the adaptive World. (3rd edn), Oxford University Press
870 931
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significance of the high levels of wild-to-crop gene flow:
871 Prikl. Bot. 16, 139–245 932
has human selection unwittingly favored gene flow from
872 14 Velasco, R. et al. (2010) The genome of the domesticated apple (Malus  933
wild species? Do introgressions localize in neutral
873 domestica Borkh.). Nat. Genet. 42, 833–839 934
regions of the crop genome or at regions of functional 15 Cornille, A. et al. (2012) New insight into the history of domesticated
874 935
apple: secondary contribution of the European wild apple to the
significance? Regarding crop-to-wild gene flow, has nat-
875
genome of cultivated varieties. PLoS Genet. 8, e1002703 936
ural selection retained M. domestica alleles introgressed
876 16 Leˆ Van, A. et al. (2013) Differential selection pressures exerted by host 937
into wild apples? Conversely, is introgression deleterious
877 resistance quantitativetrait loci on a pathogen population: a casestudy in 938
for crabapples, threatening wild populations, or will
878 an apple  Venturia inaequalis pathosystem. New Phytol. 197, 899–908 939
introgressions from the domesticated species be selected 17 Cornille, A. et al. (2013) Post-glacial recolonization history of the
879 940
against? European crabapple (Malus sylvestris Mill.), a wild contributor to
880 the domesticated apple. Mol. Ecol. 22, 2249–2263 941
The application of population and comparative geno-
881 18 Zhang, C. et al. (2007) Genetic structure of Malus sieversii population 942
mics to wild and cultivated apples provides new opportu-
882 from Xinjiang, China, revealed by SSR markers. J. Genet. Genomics 34, 943
nities to investigate the molecular basis and genetic
883 947–955 944
architecture of both (i) agronomic traits potentially select- 19 Richards, C. et al. (2009) Genetic diversity and population structure in
884 945
Malus sieversii, a wild progenitor species of domesticated apple. Tree
ed and introgressed during domestication (e.g., fruit size,
885 Genet. Genomes 5, 339–347 946
color, volatile content), and (ii) ecological traits contribut-
886 20 Cornille, A. et al. (2013) Crop-to-wild gene flow and spatial genetic 947
ing to the adaptation of wild apple populations to environ-
887 structure in the closest wild relatives of the cultivated apple. Evol. 948
mental and biotic factors (e.g., temperature, drought,
888 Appl. 6, 737–748 949
pathogens). Population and comparative genomics may 21 Volk, G.M. et al. (2008) Genetic diversity and disease resistance of wild
889 950
Malus orientalis from Turkey and Southern Russia. J. Am. Soc. Hortic.
also reveal which traits were selected during the early
890 Sci. 133, 383–389 951
steps of domestication and which were selected during the
891 22 Volk, G.M. et al. (2009) Capturing the diversity of wild Malus orientalis 952
modern breeding phase. Breeding programs will probably
892 from Georgia, Armenia, Russia, and Turkey. J. Am. Soc. Hortic. Sci. 953
benefit from the incorporation of candidate alleles identi- 134, 453–459
893 954
23 Ho¨fer, M. et al. (2013) Assessment of phenotypic variation of Malus
fied by evolutionary analyses, and there may be an in-
894
orientalis in the North Caucasus region. Genet. Resour. Crop Evol. 60, 955
crease in diversity from exotic germplasm in key genomic
895 1463–1477 956
regions (such as apparently less diverse candidate
896 24 Castric, V. et al. (2008) Repeated adaptive introgression at a gene 957
regions). The ecological genomics of apples sensu lato will,
897 under multiallelic balancing selection. PLoS Genet. 4, e1000168 958
therefore, not only advance our understanding of the his- 25 Joly, S. and Schoen, D.J. (2011) Migration rates, frequency-dependent
898 959
selection and self-incompatibility locus in Leavenworthia
tory of this fascinating system but will also guide and
899 (Brassicaceae). Evolution 65, 2357–2369 960
accelerate the development of new breeding strategies
900 26 Van Treuren, R. et al. (2010) Microsatellite genotyping of apple Malus 961
for increasing the volume and quality of apple production
901 domestica Borkh.) genetic resources in the Netherlands: application in 962
in the face of dynamic abiotic and biotic threats.
902 collection management and variety identification. Genet. Resour. Crop 963
Evol. 57, 853–865
903 964
Acknowledgments 27 Gross, B.L. et al. (2012) Identification of interspecific hybrids among
904 domesticated apple and its wild relatives. Tree Genet. Genomes 8, 965
905 We thank the editor and two referees for comments on a previous version 1223–1235 966
of this manuscript. We thank Ilya Zacharov for photographs of Malus
906 28 Myles, S. (2013) Improving fruit and wine: what does genomics have to 967
baccata and Pascal Heitlzer for photographs of Malus sieversii.
907 offer? Trends Genet. 29, 190–196 968
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9