Skip to main content
SpringerLink
Log in

Genetic diversity and population structure in Malus sieversii, a wild progenitor species of domesticated apple

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Malus sieversii (Lebed.) M. Roem. is a wild progenitor species of the domesticated apple. It is found across a mountainous region of central Asia and has been the focus of several collection expeditions by the USDA-ARS-National Plant Germplasm System. This study used microsatellite variation at seven loci to estimate diversity and differentiation within M. sieversii using several complimentary approaches. Multilocus genotypes were amplified from 949 individuals representing seedling trees from 88 half-sib families from eight M. sieversii populations collected in Kazakhstan. Apportioning of genetic variation was estimated at both the family and site level. Analyses using a hierarchical model to estimate F st showed that differentiation among individual families is more than three times greater than differentiation among sites. In addition, average gene diversity and allelic richness varied significantly among sites. A rendering of a genetic network among all sites showed that differentiation is largely congruent with geographical location. In addition, nonhierarchical Bayesian assignment methods were used to infer genetic clusters across the collection area. We detected four genetic clusters in the data set. The quality of these assignments was evaluated over multiple Markov Chain Monte Carlo runs using both posterior likelihood and stability of the assignments. The spatial pattern of genetic assignments among the eight collection sites shows two broadly distributed and two narrowly distributed clusters. These data indicate that the southwestern collection sites are more admixed and more diverse than the northern sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bretting PK, Widrlechner MP (1995) Genetic markers and plant genetic resources. Plant Breed Rev 13:11–86

    Google Scholar 

  • Coart E, Vekemans Z, Smulders M, Wagner I, van Huylenbroeck J, van Bockstaele E, Roldan-Ruiz I (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

    Article  PubMed  CAS  Google Scholar 

  • Coart E, van Glabeke S, De Loose M, Larsen AS, Roldan-Ruiz I (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

    Article  PubMed  CAS  Google Scholar 

  • Dyer RJ, Nason JD (2004) Population graphs: the graph-theoretic shape of genetic structure. Mol Ecol 13:1713–1728

    Article  PubMed  Google Scholar 

  • Dzhangaliev AD (2003) The wild apple tree of Kazakhstan. Hort Rev 29:63–303

    Google Scholar 

  • El Mousadik A, Petit RH (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic of Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Forsline PL, Aldwinckle HS (2004) Evaluation of Malus sieversii seedling populations for disease resistance and horticultural traits. Acta Hort 663:529–534

    Google Scholar 

  • Forsline PL, Aldwinckle HS, Dickson EE, Hokanson SC (2003) Collection, maintenance, characterization, and utilization of wild apples from central Asia. Hort Rev 29:1–61

    Google Scholar 

  • Forte AV, Ignatov AN, Ponomarenko VV, Dorokhov DB, Savelyev NI (2002) Phylogeny of the Malus (apple tree) species, inferred from the morphological traits and molecular DNA analysis. Russian J Genet 38:1150–1160

    Article  CAS  Google Scholar 

  • Galli Z, Halasz G, Kiss E, Heszky L, Dobranszki J (2005) Molecular identification of commercial apple cultivars with microsatellite markers. HortScience 40:1974–1977

    CAS  Google Scholar 

  • Gaurino C, Santoro S, De Simone L, Lain O, Cipriani G, Testolin R (2006) Genetic diversity in a collection of ancient cultivars of apple (Malus X domestica Borkh.) as revealed by SSR-based fingerprinting. J Hort Sci Biotechnol 81:39–44

    Google Scholar 

  • Gianfranceschi L, Seghas N, Kellerhals M, Gessler C (1999) Molecular markers applied to apple breeding: Analysis of oligogenic and single gene resistances. Acta Hort 484:417–428

    Google Scholar 

  • Goudet J (1995) FSTAT, a program for IBM PC compatibles to calculate Weir and Cockerham’s (1984) estimators of F-statistics. J Hered 86:485–486

    Google Scholar 

  • Guilford P, Prakash S, Zhu JM, Rikkerink E, Gardiner S, Bassett H, Forster R (1997) Microsatellites in Malus X domestica (apple): abundance, polymorphism and cultivar identification. Theor Appl Genet 94:249–254

    Article  CAS  Google Scholar 

  • Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A (2004) Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor Appl Genet 109:1702–1709

    Article  PubMed  CAS  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Trans Royal Soc London Series B Biol Sci 351:1291–1298

    Article  Google Scholar 

  • Harris SA, Robinson JP, Juniper BE (2002) Genetic clues to the origin of the apple. TRENDS Genetics 18:426–430

    Article  CAS  Google Scholar 

  • Hemmat M, Weeden NF, Brown SK (2003) Mapping and evaluation of Malus x domestica microsatellites in apple and pear. J Amer Soc Hort Sci 128:515–520

    CAS  Google Scholar 

  • Hokanson SC, Lamboy WF, Szewc-McFadden AK, McFerson JR (2001) Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids. Euphytica 118:281–294

    Article  CAS  Google Scholar 

  • Hokanson SC, Szewc-McFadden AK, Lamboy WF, McFersen JR (1998) Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus x domestica borkh. core collection. Theor Appl Genet 97:671–683

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175:1787–1802

    Article  PubMed  CAS  Google Scholar 

  • Kitahara K, Matsumoto S, Yamamoto T, Soejima J, Kimura T, Komatsu H, Abe K (2005) Molecular characterization of apple cultivars in Japan by S-RNase analysis and SSR markers. J Amer Soc Hort Sci 130:885–892

    CAS  Google Scholar 

  • Lamboy WF, Yu J, Forsline PL, Weeden NF (1996) Partitioning of allozyme diversity in wild populations of Malus sieversii L. and implications for germplasm collection. J Amer Soc Hort Sci 121:982–987

    Google Scholar 

  • Lewis PO, Zaykin D (2001) GDA User’s manual. Department of Ecology and Evolutionary Biology, University of Connecticut. 27 July 2004. <http://lewis.eeb.uconn.edu/lewishome>

  • Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterization of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol Breed 10:217–241

    Article  CAS  Google Scholar 

  • Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526

    Article  PubMed  CAS  Google Scholar 

  • Luby J, Forsline P, Aldwinckle H, Bus V, Giebel M (2001) Silk road apples—collection, evaluation, and utilization of Malus sieversii from Central Asia. HortScience 36:225–231

    Google Scholar 

  • Luby JJ, Alspach PA, Bus VGM, Oraguzie NC (2002) Field resistance to fire blight in a diverse apple (Malus sp.) germplasm collection. J Amer Soc Hort Sci 127:245–253

    Google Scholar 

  • Morgan J, Richards A (1993) The book of apples. Ebury Press, London

    Google Scholar 

  • Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Amer Soc Hort Sci 121:773–782

    Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biology 3:1289–1299

    Article  CAS  Google Scholar 

  • Oraguzie NC, Yamamoto T, Soejima J, Suzuki T, DeSilva HN (2005) DNA fingerprinting of apple (Malus spp.) rootstocks using simple sequence repeats. Plant Breed 124:197–202

    Article  CAS  Google Scholar 

  • Pereira-Lorenzo S, Ramos-Cabrer AMR, Ascasibar-Errasti J (2003) Analysis of apple germplasm in northwestern Spain. J Amer Soc Hort Sci 128:67–84

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Ramos-Cabrer AM, Diaz-Hernandez MB, Pereira-Lorenzo S (2007) Morphology and microsatellites in Spanish apple collections. J Hort Sci Biotechnol 82:257–265

    CAS  Google Scholar 

  • Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW (2002) Genetic structure of human populations. Science 298:2381–2385

    Article  PubMed  CAS  Google Scholar 

  • Van Treuren R, van Soest LJM, van Hintum ThJL (2001) Marker-assisted rationalization of genetic resource collections: a case study with flax using AFLPs. Theor Appl Genet 103:144–152

    Article  Google Scholar 

  • Vavilov NI (1992) Origin and geography of cultivated plants. D. Love (translator). Cambridge University Press, Cambridge, England

    Google Scholar 

  • Volk GM, Richards CM, Reilley AA, Henk AD, Forsline PL, Aldwinckle HS (2005) Ex situ conservation of vegetatively-propagated species: development of a seed-based core collection for Malus sieversii. J Am Soc Hort Sci 130:203–210

    Google Scholar 

  • Volk GM, Richards CM, Reilley AA, Henk AD, Forsline PL, Aldwinckle HS (2008) Genetic diversity and disease resistance of wild Malus orientalis from Turkey and southern Russia. J Am Soc Hort Sci 133:383–389

    Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  PubMed  CAS  Google Scholar 

  • Watkins R (1995) Apple and pear. In: Smartt and Simmonds (eds) Evolution of crop plants. Longman scientific and technical, Essex, England, pp 418–422

  • Yan G, Hong L, Song W, Chen R (2008) Genetic polymorphism of Malus sieversii populations in Xinjiang, China. Genet Res Crop Evol 55:171–181

    Article  CAS  Google Scholar 

  • Zhang C, Chen X, He T, Liu X, Feng T, Yuan Z (2007) Genetic structure of Malus sieversii population from Xinjiang, China, revealed by SSR markers. J Genet Genomics 34:947–955

    Article  PubMed  CAS  Google Scholar 

  • Zhou ZQ, Li YN (2000) The RAPD evidence for the phylogenetic relationship of the closely related species of cultivated apple. Genet Res Crop Evol 47:353–357

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Angela Baldo and Dr. Gennaro Fazio of the ARS Plant Genetic Resources Unit in Geneva, NY for helpful comments on earlier drafts of this work. This project was partially supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number #2005-00751. Dale Lockwood was supported by a USDA-ARS Specific Cooperative Agreement with Colorado State University’s Program for Interdisciplinary Mathematics, Ecology and Statistics. Any mention of trade names of commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Author information

Authors and Affiliations

  1. National Center for Genetic Resources Preservation, United States Department of Agriculture, Fort Collins, CO, 80521, USA

    Christopher M. Richards, Gayle M. Volk, Ann A. Reilley, Adam D. Henk & Patrick A. Reeves

  2. Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Dale R. Lockwood

  3. Plant Genetic Resources Unit, United States Department of Agriculture, Geneva, NY, 14456-0462, USA

    Philip L. Forsline

Authors
  1. Christopher M. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gayle M. Volk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ann A. Reilley
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adam D. Henk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dale R. Lockwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrick A. Reeves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Philip L. Forsline
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher M. Richards.

Additional information

Communicated By: A. Dandekar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richards, C.M., Volk, G.M., Reilley, A.A. et al. Genetic diversity and population structure in Malus sieversii, a wild progenitor species of domesticated apple. Tree Genetics & Genomes 5, 339–347 (2009). https://doi.org/10.1007/s11295-008-0190-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-008-0190-9

Keywords

Search

Navigation