Analysis of the genetic diversity and structure across a wide range of germplasm reveals prominent gene flow in apple at the European level

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  Urrestarazu, Jorge ^a,b,j   Denancé, Caroline ^a   Ravon, Elisa ^a   Guyader, Arnaud ^a   Guisnel, Rémi ^a   Feugey, Laurence ^a   Poncet, Charles ^c   Lateur, Marc ^d   Houben, Patrick ^d   Ordidge, Matthew ^e   Fernandez Fernandez, Felicidad ^f   Evans, Kate M ^g   Paprstein, Frantisek ^h   Sedlak, Jiri ^h   Nybom, Hilde ⁱ   Garkava Gustavsson, Larisa ⁱ   Miranda, Carlos ^j   Gassmann, Jennifer ^k   Kellerhals, Markus ^k   Suprun, Ivan ^l   Pikunova, Anna V ^m   Krasova, Nina G ^m   Torutaeva, Elnura ⁿ   Dondini, Luca ^b   Tartarini, Stefano ^b   Laurens, François ^a   Durel, Charles Eric ^a   more..

^a UNIVERSITÉ D'ANGERS   (France)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c Diversity and Ecophysiology of Cereals   (France)

^d WALLOON AGRICULTURAL RESEARCH CENTRE   (Belgium)

^e UNIVERSITY OF READING   (United Kingdom)

^f EAST MALLING RESEARCH   (United Kingdom)

^g WASHINGTON STATE UNIVERSITY   (United States)

^h RESEARCH AND BREEDING INSTITUTE OF POMOLOGY HOLOVOUSY LTD   (Czech Republic)

ⁱ SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^j PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^k AGROSCOPE   (Switzerland)

^l Federal Agency of Scientific Organizations   (Russian Federation)

^m Federal Agency of Scientific Organizations   (Russian Federation)

ⁿ Kyrgyz National Agrarian University named after KI Skryabin   (Kyrgyzstan)

more..

Author keywords

Differentiation; Genetic resources; Malus x domestica Borkh.; Parentage analysis; Population structure; SSR markers; Variability

Indexed keywords

GENETIC MARKER; MICROSATELLITE DNA;

CLASSIFICATION; EMBRYOLOGY; EUROPE; GENE FLOW; GENETIC MARKER; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; MALUS; METABOLISM; PHYLOGENY;

EUROPE; GENE FLOW; GENETIC MARKERS; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; MALUS; MICROSATELLITE REPEATS; PHYLOGENY;

EID: 84975705518     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-016-0818-0     Document Type: Article

References (78)

1. Food and Agriculture Organization of the United Nations. FAO statistics database on the World Wide Web http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID0567#ancor. Accessed 27 July 2015.
2. Hokanson SC, Lamboy WF, Szewc-McFadden AK, McFerson JR. Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids. Euphytica. 2001;118:281-94.
3. Janick J, Moore JN. Fruit breeding. Volume I: tree and tropical fruits. New York: Wiley; 1996.
4. Laurens F, Durel CE, Patocchi A, Peil A, Salvi S, Tartarini S, Velasco R, van de Weg WE. Review on apple genetics and breeding programs and presentation of a new initiative of a news European initiative to increase fruit breeding efficiency. J Fruit Sci. 2010;27:102-7.
5. Noiton DAM, Alspach PA. Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci. 1996;121:773-82.
6. Brooks RM, Olmo HP. Register of new fruit and nut varieties list 35. HortScience. 1991;26:951-78.
7. Brooks RM, Olmo HP. Register of new fruit and nut varieties list 36. HortScience. 1994;29:942-69.
8. Brooks RM, Olmo HP. Register of fruit and nut varieties. Alexandria: ASHS; 1997.
9. de Vicente. The evolving role of genebanks in the fast-developing field of molecular genetics. Ed. Issues in genetic resources No XI, August 2004. Rome: International Plant Genetic Resources Institute-IPGRI; 2004.
10. Jing RC, Vershinin A, Grzebyta J, Shaw P, Smykal P, Marshall D, Ambrose MJ, Ellis THN, Flavell AJ. The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol. 2010;10:44.
11. van Treuren R, Kemp H, Ernsting G, Jongejans B, Houtman H, Visser L. Microsatellite genotyping of apple (Malus x domestica Borkh.) genetic resources in the Netherlands: application in collection management and variety identification. Genet Resour Crop Evol. 2010;57:853-65.
12. Nybom H, Weising K, Rotter B. DNA fingerprinting in botany: past, present, future. Investig Genet. 2014;5:1.
13. Bacilieri R, Lacombe T, Le Cunff L, Di Vecchi-Staraz M, Laucou V, Genna B, Péros JP, This P, Boursiquot JM. Genetic structure in cultivated grapevines is linked to geography and human selection. BMC Plant Biol. 2013;13:25.
14. Bühlmann A, Gassmann J, Ingenfeld A, Hunziker K, Kellerhals M, Frey JE. Molecular characterization of the Swiss fruit genetic resources. Erwerbs-Obstbau. 2015;57:29-34.
15. McCouch SR, McNally KL, Wang W, Sackville HR. Genomics of gene banks: a case study in rice. Am J Bot. 2012;99:407-23.
16. Wünsch A, Hormaza JI. Cultivar identification and genetic fingerprinting of temperate fruit tree species using DNA markers. Euphytica. 2002;125:59-67.
17. Ellegren H. Microsatellites: simple sequences with complex evolution. Nat Rev Genet. 2004;5:435-45.
18. Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ. Current trends in microsatellite genotyping. Mol Ecol Resour. 2011;11:591-611.
19. Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK. Microsatellite markers: an overview of the recent progress in plants. Euphytica. 2011;177:309-34.
20. Sunnucks P. Efficient genetic markers for population biology. Trends Ecol Evol. 2000;15:199-03.
21. Urrestarazu J, Royo JB, Santesteban LG, Miranda CM. Evaluating the influence of the microsatellite marker set on the genetic structure inferred in Pyrus communis L. PLoS One. 2015;10:e0138417.
22. Garkava-Gustavsson L, Kolodinska Brantestam A, Sehic J, Nybom H. Molecular characterisation of indigenous Swedish apple cultivars based on SSR and S-allele analysis. Hereditas. 2008;145:99-112.
23. Lassois L, Denancé C, Ravon E, Guyader A, Guisnel R, Hibrand-Saint-Oyant L, Poncet C, Lasserre-Zuber P, Feugey L, Durel CE. Genetic diversity, population structure, parentage analysis and construction of core collections in the French apple germplasm based on SSR markers. Plant Mol Biol Rep. 2015. doi: 10.1007/s11105-015-0966-7.
24. Liang W, Dondini L, De Franceschi P, Paris R, Sansavini S, Tartarini S. Genetic diversity, population structure and construction of a core collection of apple cultivars from Italian germplasm. Plant Mol Biol Rep. 2015;33:458-73.
25. Patzak J, Paprštein F, Henychová A, Sedlák J. Comparison of genetic diversity structure analyses of SSR molecular marker data within apple (Malus×domestica) genetic resources. Genome. 2012;55:647-65.
26. Urrestarazu J, Miranda C, Santesteban LG, Royo JB. Genetic diversity and structure of local apple cultivars from Northeastern Spain assessed by microsatellite markers. Tree Genet Genomes. 2012;8:1163-80.
27. Sehic J, Garkava-Gustavsson L, Nybom H. More harmonization needed for DNA-based identification of apple germplsm. Acta Hortic. 2013;976:277-83.
28. Laurens F, Aranzana MJ, Arús P, Bassi D, Bonany J, Corelli L, Durel CE, Mes J, Pascal T, Patocchi A, Peil A, Quilot B, Salvi S, Tartarini S, Troggio M, Vecchietti A, Velasco R, van de Weg WE. Review of fruit genetics and breeding programmes and a new European initiative to increase fruit breeding efficiency. Acta Hortic. 2012;929:95-102.
29. Morin PA, Manaster C, Mesnick SL, Holland R. Normalization and binning of historical and multi-source microsatellite data: overcoming the problems of allele size shift with ALLELOGRAM. Mol Ecol Resour. 2009;9:1451-5.
30. Putman AI, Carbone I. Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecol Evol. 2014;4:4399-28.
31. Gasi F, Simon S, Pojskic N, Kurtovic M, Pejic I. Genetic assessment of apple germplasm in Bosnia and Herzegovina using microsatellite and morphologic markers. Sci Hortic. 2010;126:164-71.
32. Gharghani A, Zamani Z, Talaie A, Oraguzie NC, Fatahi R, Hajnajari H, Wiedow C, Gardiner SE. Genetic identity and relationships of Iranian apple (Malus x domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genet Resour Crop Evol. 2009;56:829-42.
33. Gao Y, Liu F, Wang K, Wang D, Gong X, Liu L, Richards CM, Henk AD, Volk GM. Genetic diversity of Malus cultivars and wild relatives in the Chinese National Repository of Apple Germplasm Resources. Tree Genet Genomes. 2015. doi: 10.1007/s11295-015-0913-7.
34. Gross BL, Volk GM, Richards CM, Forsline CL, Fazio G, Chao CT. Identification of "duplicate" accessions within the USDA-ARS National Plant Germplasm System Malus Collection. J Am Soc Hortic Sci. 2012;137:333-42.
35. Cornille A, Gladieux P, Smulders MJM, Roldán-Ruiz I, Laurens F, Le Cam B, Nerseyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang XG, Tenaillon MI, Giraud. New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet. 2012;8:e1002703.
36. Cornille A, Giraud T, Smulders MJM, Roldán-Ruiz I, Gladieux P. The domestication and evolutionary ecology of apples. Trends Genet. 2014;30:57-65.
37. Gross BL, Henk AD, Richards CM, Fazio G, Volk GM. Genetic diversity in Malus x domestica (Rosaceae) through time in response to domestication. Am J Bot. 2014;101:1770-9.
38. Hartmann HT, Kester DE, Davies FT, Geneve RL. Plant propagation: principles and practices. 7th ed. Upper Saddle River: Prentice Hall; 2002.
39. Zohary D, Hopf D. Domestication of plants in the Old World: the origin and spread of cultivated plants in West Asia, Europe and the Nile Valley. Oxford: Oxford University Press; 2000.
40. De Franceschi P, Dondini L, Sanzol J. Molecular bases and evolutionary dynamics of self-incompatibility in the Pyrinae (Rosaceae). J Exp Bot. 2012;63:4015-32.
41. Knutson L, Stoner AK. Biotic diversity and germplasm preservation: global imperative. Boston: Kluwer Academic Publishers; 1989.
42. McCouch S. Diversifying selection in plant breeding. PLoS Biol. 2004;2:e347.
43. World Apple and Pear Association. European apple and pear crop forecast. Brussels: World Apple and Pear Association; 2013.
44. Miller AJ, Gross BL. Forest to field: perennial fruit crop domestication. Am J Bot. 2011;98:1389-414.
45. Biswas S, Akey JM. Genomic insights into positive selection. Trends Genet. 2006;22:437-46.
46. Bourguiba H, Audergon JM, Krichen L, Trifi-Farah N, Mamouni A, Trabelsi S, D'Onofrio C, Asma BM, Santoni S, Khadari B. Loss of genetic diversity as a signature of apricot domestication and diffusion into the Mediterranean Basin. BMC Plant Biol. 2012;12:49.
47. Blanquart F, Gandon S, Nuismer SL. The effects of migration and drift on local adaptation to a heterogeneous environment. J Evol Biol. 2012;25:1351-63.
48. Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM, Grando MS. Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol. 2013;13:39.
49. Lia VV, Poggio L, Confalonieri VA. Microsatellite variation in maize landraces from Northwestern Argentina: genetic diversity, population structure and racial affiliations. Theor Appl Genet. 2009;119:1053-67.
50. Li XW, Meng XQ, Jia HJ, Yu ML, Ma RJ, Wang LR, Cao K, Shen ZJ, Niu L, Tian JB, Chen MJ, Xie M, Arus P, Gao ZS, Aranzana MJ. Peach genetic resources: diversity, population structure and linkage disequilibrium. BMC Genet. 2013;14:84.
51. Jacobs MMJ, Smulders MJM, van den Berg RG, Vosman B. What's in a name; genetic structure in Solanum section Petota studied using population-genetic tools. BMC Evol Biol. 2011;11:42.
52. Jing R, Ambrose MA, Knox MR, Smykal P, Hybl M, Ramos A, Caminero C, Burstin J, Duc G, van Soest LJM, Swiecicki WK, Pereira MG, Vishnyakova M, Davenport GF, Flavell AJ, Ellis THN. Genetic diversity in European Pisum germplasm collections. Theor Appl Genet. 2012;125:365-80.
53. Kalinowski ST, Taper ML, Marshall TC. Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol. 2007;16:1099-2006.
54. Salvi S, Micheletti D, Magnago P, Fontanari M, Viola R, Pindo M, Velasco R. One-step reconstruction of multi-generation pedigree networks in apple (Malus×domestica Borkh.) and the parentage of Golden Delicious. Mol Breed. 2014;34:511-24.
55. Bianco L, Cestaro A, Sargent DJ, Banchi E, Derdak S, Di Guardo M, Salvi S, Jansen J, Viola R, Gut I, et al. Development and validation of a 20K single nucleotide polymorphism (SNP) whole genome genotyping array for apple (Malus x domestica Borkh). PloS ONE. 2014;9:e110377.
56. Bianco L, Cestaro A, Linsmith G, Muranty H, Denancé C, Théron A, Poncet C, Micheletti D, Kersshbamer E, Di Pierro EA, Larger S, Pindo M, van de Weg WE, Davassi A, Laurens F, Velasco R, Durel CE, Troggio M. Development and validation of the Axiom®Apple480K SNP genotyping array. Plant J. 2016;86:62-74.
57. Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B, Lawley C, Vanderzande S, Hellens RP, Kumar S, Cestaro A et al. Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PloS ONE. 2012;7:e31745.
58. Morgan J, Richards A, Dowle E. The new book of Apples: the definitive guide to apples, including over 2000 varieties. London: Ebury Press; 2002.
59. Hokanson SC, Szewc-McFadden AK, Lamboy WF, McFerson JR. Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus x domestica Borkh. core subset collection. Theor Appl Genet. 1998;97:671-83.
60. Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, van de Weg E, Gessler C. Development and characterisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol Breed. 2002;10:217-41.
61. Silfverberg-Dilworth E, Matasci CL, van de Weg WE, van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A. Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet Genomes. 2006;2:202-24.
62. Vinatzer BA, Patocchi A, Tartarini S, Gianfranceschi L, Sansavini S, Gessler C. Isolation of two microsatellite markers from BAC clones of the Vf scab resistance region and molecular characterization of scab-resistant accessions in Malus germplasm. Plant Breed. 2004;123:321-6.
63. Evans KM, Fernández F, Govan C. Harmonising fingerprinting protocols to allow comparisons between germplasm collections - Pyrus. Acta Hortic. 2009;814:103-6.
64. Fernández-Fernández F. Fingerprinting the National apple and pear collections. Final report of DEFRA research project GC0140. 2010. p. 1-18. http://randd.defra.gov.uk/Document.aspx?Document=GC0140SID5FingerprintingFernandez.pdf.
65. Hardy OJ, Vekemans X. SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes. 2002;2:618-20.
66. Waits LP, Luikart G, Taberlet P. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol. 2001;10:249-56.
67. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945-59.
68. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611-20.
69. Earl DA, von Holdt BM. Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Genet Resour. 2012;4:359-61.
70. Breton C, Pinatel C, Médail F, Bonhomme F, Bervillé A. Comparison between classical and Bayesian methods to investigate the history of olive cultivars using SSR-polymorphisms. Plant Sci. 2008;175:524-32.
71. Miranda C, Urrestarazu J, Santesteban LG, Royo JB, Urbina V. Genetic diversity and structure in a collection of ancient Spanish pear cultivars assessed by microsatellite markers. J Am Soc Hortic Sci. 2010;135:428-37.
72. Marra FP, Caruso T, Costa F, Di Vaio C, Mafrica R, Marchese A. Genetic relationships, structure and parentage simulation among the olive tree (Olea europaea L. subsp. europaea) cultivated in Southern Italy revealed by SSR markers. Tree Genet Genomes. 2013;9:961-73.
73. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:801-6.
74. Rosenberg NA. Distruct: a program for the graphical display of population structure. Mol Ecol Notes. 2004;4:137-8.
75. Perrier X, Jacquemoud-Collet JP. DARwin Software. 2006. http://darwin.cirad.fr/darwin.
76. Meirmans PG, van Tienderen PH. Genotype and Genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes. 2004;4:792-4.
77. Goudet J. FSTAT 2.9.3.2. 2002. http://www2.unil.ch/popgen/softwares/fstat.htm.
78. Lacombe T, Boursiquot JM, Laucou V, Di Vecchi-Staraz M, Péros JP. This P. Large-scale parentage analysis in an extended set of grapevine cultivars (Vitis vinifera L.). Theor Appl Genet. 2013;126:401-14.