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 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.
Vyšlo v časopise:
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): e32767. doi:10.1371/journal.pgen.1002703
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002703
Souhrn
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.
Zdroje
1. DiamondJ 1997 Guns, Germs, and Steel: The Fates of Human Societies Norton, W. W. & Company, Inc. Sales
2. ZederMAEmshwillerESmithBDBradleyDG 2006 Documenting domestication: the intersection of genetics and archaeology. Trends Genet 22 139 155
3. DiamondJ 2002 Evolution, consequences and future of plant and animal domestication. Nature 418 700 707
4. PuruggananMDFullerDQ 2009 The nature of selection during plant domestication. Nature 457 843 848
5. WrightSIGautBS 2005 Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22 506 519
6. TenaillonMIManicacciD 2011 Maize origins: an old question under the spotlights. PrioulJ-LThévenotCMolnarT Advances in Maize (Essential Reviews in Experimental Biology): The Society for Experimental Biology 89 110
7. AllabyRGFullerDQBrownTA 2008 The genetic expectations of a protracted model for the origins of domesticated crops. PNAS 105 13982 13986
8. CaicedoALWilliamsonSHHernandezRDBoykoAFledel-AlonA 2007 Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3 e163.
9. DoebleyJFGautBSSmithBD 2006 The molecular genetics of crop domestication. Cell 127 1309 1321
10. GrossBLOlsenKM 2009 Genetic perspectives on crop domestication. Trends Plant Sci 15 529 537
11. BrownTAJonesMKPowellWAllabyRG 2009 The complex origins of domesticated crops in the Fertile Crescent. Trends Ecol Evol 24 103 109
12. FeuilletCLangridgePWaughR 2008 Cereal breeding takes a walk on the wild side. Trends Genet 24 24 32
13. GléminSBataillonT 2009 A comparative view of the evolution of grasses under domestication. New Phytol 183 273 290
14. KilianBÖzkanHWaltherAKohlJDaganT 2007 Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture. Mol Biol Evol 24 2657 2668
15. KovachMJSweeneyMTMcCouchSR 2007 New insights into the history of rice domestication. Trends Genet 23 578 587
16. RussellJDawsonIKFlavellAJSteffensonBWeltzienE 2011 Analysis of >1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol 191 564 578
17. WangCChenJZhiHYangLLiW 2010 Population genetics of foxtail millet and its wild ancestor. BMC Genet 11 90
18. MatsuokaYVigourouxYGoodmanMMSanchezGJBucklerE 2002 A single domestication for maize shown by multilocus microsatellite genotyping. PNAS 99 6080 6084
19. OumarIMariacCPhamJ-LVigourouxY 2008 Phylogeny and origin of pearl millet (Pennisetum glaucum [L.] R. Br) as revealed by microsatellite loci. Theor Appl Genet 117 489 497
20. BlackmanBKScascitelliMKaneNCLutonHHRasmussenDA 2011 Sunflower domestication alleles support single domestication center in eastern North America. PNAS 108 14360 14365
21. HarterAVGardnerKAFalushDLentzDLByeRA 2004 Origin of extant domesticated sunflowers in eastern North America. Nature 430 201 205
22. TenaillonMIU'RenJTenaillonOGautBS 2004 Selection versus demography: A multilocus investigation of the domestication process in maize. Mol Biol Evol 21 1214 1225
23. TannoK-iWillcoxG 2006 How Fast Was Wild Wheat Domesticated? Science 311 1886
24. ChenHMorrellPLAshworthVETMde la CruzMCleggMT 2009 Tracing the geographic origins of major avocado cultivars. J Hered 100 56 65
25. MillerAGrossBL 2011 From forest to field: perennial fruit crops domestication. Am J Bot 98 1389 1414
26. MillerASchaalB 2005 Domestication of a Mesoamerican cultivated fruit tree, Spondias purpurea. PNAS 102 12801 12806
27. PetitRJHampeA 2006 Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37 187 214
28. SavolainenOPyhäjärviT 2007 Genomic diversity in forest trees. Curr Opin Plant Biol 10 162 167
29. AusterlitzFMarietteSMachonNGouyonPHGodelleB 2000 Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154 1309 1321
30. JanickJ 2005 The origins of fruits, fruit growing, and fruit breeding Plant Breeding Reviews: John Wiley & Sons, Inc 255 321
31. MillerAJSchaalBA 2006 Domestication and the distribution of genetic variation in wild and cultivated populations of the Mesoamerican fruit tree Spondias purpurea L. (Anacardiaceae). Mol Ecol 15 1467 1480
32. ZoharyDSpiegel-RoyP 1975 Beginnings of Fruit Growing in the Old World. Science 319 327
33. ZoharyD 2004 Unconscious selection and the evolution of domesticated plants. Econ Bot 58 5 10
34. PickersgillB 2007 Domestication of plants in the Americas: insights from mendelian and molecular genetics. Ann Bot 100 925 940
35. JuniperBEMabberleyDJ 2006 The story of the apple Imber Press, Inc 240
36. BesnardGRubio de CasasRVargasP 2007 Plastid and nuclear DNA polymorphism reveals historical processes of isolation and reticulation in the olive tree complex (Olea europaea). J Biogeogr 34 736 752
37. MylesSBoykoAROwensCLBrownPJGrassiF 2011 Genetic structure and domestication history of the grape. PNAS 108 3530 3535
38. DelplanckeMAlvarezNEspíndolaAJolyHBenoitL 2011 Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evolutionary Applications in press
39. ZoharyDHopfM 2000 Domestication of plants in the Old World New York Oxford University Press 316
40. CoartEVan GlabekeSDe LooseMLarsenASRoldán-RuizI 2006 Chloroplast diversity in the genus Malus: new insights into the relationship between the European wild apple (Malus sylvestris (L.) Mill.) and the domesticated apple (Malus domestica Borkh.). Mol Ecol 15 2171 2182
41. HarrisSARobinsonJPJuniperBE 2002 Genetic clues to the origin of the apple. Trends Genet 18 426 430
42. RobinsonJPHarrisSAJuniperBE 2001 Taxonomy of the genus Malus Mill. (Rosaceae) with emphasis on the cultivated apple, Malus domestica Borkh. Plant Syst Evol 226 35 58
43. VelascoRZharkikhAAffourtitJDhingraACestaroA 2010 The genome of the domesticated apple (Malus×domestica Borkh.). Nature Genetics 42 833 839
44. DzhangalievAD 2003 The wild apple tree of Kazakhstan Hortic Rev John Wiley & Sons, Inc 63 303
45. VavilovNI 1926 Studies on the origin of cultivated plants. Trudy Byuro Prikl Bot 16 139 245
46. ForslinePLAldwinckleHSDicksonEELubyJJHokansonSC 2002 Collection, maintenance, characterization and utilization of wild apples of central Asia Hortic Rev John Wiley & Sons, Inc 1 61
47. RehderA 1940 Manual of cultivated trees and shrubs Macmillan, New York
48. BoréJMFleckingerJ 1997 Pommiers à cidre: variétés de France: INRA éditions, Paris, FRANCE (1997) (Monographie) 771
49. LubyJJAlspachPABusVGMOraguzieNC 2001 Field resistance to fire blight in a diverse apple (Malus sp.) germplasm collection. J Am Soc Hortic Sci 127 245 253
50. HarrisonNHarrisonRJ 2011 On the evolutionary history of the domesticated apple. Nat Genet 43 1043 1044
51. MichelettiDTroggioMSalaminiFViolaRVelascoR 2011 On the evolutionary history of the domesticated apple. Nat Genet 43 1044 1045
52. Pereira-LorenzoSRamos-CabrerAMFischerM 2009 Breeding Apple (Malus×Domestica Borkh). Breeding Plantation Tree Crops: Temperate Species Springer New York 33 81
53. MeirmansPGVan TienderenPH 2004 Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4 792 794
54. KoopmanWJMLiYCoartEVan De WegWEVosmanB 2007 Linked vs. unlinked markers: multilocus microsatellite haplotype-sharing as a tool to estimate gene flow and introgression. Mol Ecol 16 243 256
55. PritchardJKStephensMDonnellyP 2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959
56. EvannoGRegnautSGoudetJ 2005 Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14 2611 2620
57. VerckenEFontaineMCGladieuxPHoodMEJonotO 2010 Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathog 6 e1001229.
58. CornuetJMLuikartG 1996 Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144 2001 2014
59. MabberleyDJJarvisCEJuniperBE 2001 The name of the apple. Telopea 9 2001
60. DiegoMMichelaTFrancescoSRobertoVRiccardoV 2011 On the evolutionary history of the domesticated apple. Nat Genet 43 1044 1045
61. AndersonECThompsonEA 2002 A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160 1217 1229
62. ExcoffierLEstoupACornuetJ-M 2005 Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169 1727 1738
63. Ross-IbarraJTenaillonMGautBS 2009 Historical divergence and gene flow in the Genus Zea. Genetics 181 1399 1413
64. CornuetJ-MSantosFBeaumontMARobertCPMarinJ-M 2008 Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24 2713 2719
65. WagnerIWeedenNF 2000 Isozyme in Malus sylvestris, Malus×domestica and in related Malus species. Acta Horticulturae 538 51 56
66. GardinerSEBusVGMRusholmeRLChagnéDRikkerinkEHA 2007 Fruits and Nuts: Apple KoleC Springer Berlin Heidelberg 1 62
67. CoartEVekemansXSmuldersMJMWagnerIVan HuylenbroeckJ 2003 Genetic variation in the endangered wild apple (Malus sylvestris (L.) Mill.) in Belgium as revealed by amplified fragment length polymorphism and microsatellite markers. Mol Ecol 12 845 857
68. GharghaniAZamaniZTalaieAOraguzieNFatahiR 2009 Genetic identity and relationships of Iranian apple (Malus domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genet Resour Crop Ev 56 829 842
69. PonomarenkoV 1991 On a little known species Malus×asiatica (Rosaceae). Bot Zhurn 76 715 720
70. OlsenKMGrossBL 2008 Detecting multiple origins of domesticated crops. PNAS 105 13701 13702
71. van HeerwaardenJDoebleyJBriggsWHGlaubitzJCGoodmanMM 2011 Genetic signals of origin, spread, and introgression in a large sample of maize landraces. PNAS 108 1088 1092
72. OrtonV 1973 The American cider Book The story of America's natural beverage North Point Press
73. LeaAGHPiggottJR 2003 Fermented Beverage Production; 2, editor Kluwer Academic/Plenum
74. HajjarRHodgkinT 2007 The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156 1 13
75. PatocchiAFernàndez-FernàndezFEvansKGobbinDRezzonicoF 2009 Development and test of 21 multiplex PCRs composed of SSRs spanning most of the apple genome. Tree Genet Genomes 5 211 223
76. ExcoffierLLischerHEL 2010 Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10 564 567
77. RaymondMRoussetF 1995 GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86 248 249
78. RoussetF 2008 Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8 103 106
79. SchusterMBüttnerR 1995 Chromosome numbers in the Malus wild species collection of the genebank Dresden-Pillnitz. Genet Resour Crop Ev 42 353 361
80. Van OosterhoutCHutchinsonWFWillsDPMShipleyP 2004 Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4 535 538
81. SzpiechZAJakobssonMRosenbergNA 2008 ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24 2498 2504
82. LynchMRitlandK 1999 Estimation of pairwise relatedness with molecular markers. Genetics 152 1753 1766
83. SchwackeLSchwackeJRoselP 2005 RE-RAT: relatedness estimation and rarefaction analysis tool. http://people.musc.edu/~schwaclh/
84. PirySLuikartGCornuetJM 1999 Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity 90 502 503
85. FalushDStephensMPritchardJK 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 1567 1587
86. HubiszMJFalushDStephensMPritchardJK 2009 Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9 1322 1332
87. JakobssonMRosenbergNA 2007 CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23 1801 1806
88. CornuetJ-MRavigneVEstoupA 2010 Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11 401
89. LiebhardRGianfranceschiLKollerBRyderCDTarchiniR 2002 Development and characterisation of 140 new microsatellites in apple (Malus×domestica Borkh.). Mol Breeding 10 217 241
90. Silfverberg-DilworthEMatasciCVan de WegWVan KaauwenMWalserM 2006 Microsatellite markers spanning the apple (Malus×domestica Borkh.) genome. Tree Genet Genomes 2 202 224
91. GianfranceschiLSegliasNTarchiniRKomjancMGesslerC 1998 Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96 1069 1076
92. NeiM 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 583 590
93. WeirBSCockerhamCC 1984 Estimating F-Statistics for the analysis of population structure. Evolution 38 1358 1370
94. GoldsteinDBRuiz LinaresACavalli-SforzaLLFeldmanMW 1995 Genetic absolute dating based on microsatellites and the origin of modern humans. PNAS 92 6723 6727
95. FagundesNJRRayNBeaumontMNeuenschwanderSSalzanoFM 2007 Statistical evaluation of alternative models of human evolution. PNAS 104 17614 17619
96. BeaumontMAZhangWBaldingDJ 2002 Approximate Bayesian Computation in population genetics. Genetics 162 2025 2035
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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