Skip to main content
SpringerLink
Log in

Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

A collection of 142 accessions of 23 Malus species, derived hybrids and cultivar accessions from the USDA-ARS Plant Genetic Resources Unit's core collection, which represents an extensive range of Malus species, was screened with a set of previously described SSR (simple sequence repeat) markers. The markers were used to determine genetic identities, estimate genetic diversity, identify genetic relationships among the accessions, and determine the utility of SSR primers developed from Malus ×domestica for making genetic assessments across the whole Malus genus. All eight primer pairs amplified multiple fragments when used in polymerase chain reactions with DNA from these accessions. High levels of variation were detected with a mean of 26.4 alleles per locus and a mean direct count heterozygosity across all eight loci equal to 0.623. The eight primer pairs used in this study unambiguously differentiated all but five pairs of accessions in this collection of 142 accessions of 23 Malus species, derived hybrids and cultivars. These SSR data were not useful in identifying genetic relationships among this diverse collection of accessions, with the majority of the accessions not clustering in ways concordant with taxonomic information and/or geographic origin. The resulting phenogram resolved only two meaningful clusters, for the taxonomically isolated Section Chloromeles and for M. fusca accessions, reflecting genetic relationships arising from geographic origin. The detection of identical accessions in the collection, which were previously considered to be unique, highlights the critical need to further bolster collections of certain Malus species.

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

Similar content being viewed by others

References

  • Aldwinckle, H.S., P.L. Forsline, H.L. Gustafson & S.C. Hokanson, 1997. Evaluation of apple scab resistance of Malus sieversii populations from Central Asia. HortScience 32: 440.

    Google Scholar 

  • Beckmann, J.S. & M. Soller, 1990. Toward a unified approach to genetic mapping eukaryotes based on sequence tagged microsatellite sites. Bio/Technology 8: 930–932.

    Article  PubMed  CAS  Google Scholar 

  • Briggs, J.B. & F.H. Alston, 1969. Sources of pest resistance in apple cultivars. Rep E Malling Res Stn For 1968: 159–162.

  • Brooks, H.J. & G. Vest, 1985. Public programs on genetics and breeding of horticultural crops in the United States. HortScience 20: 826–830.

    Google Scholar 

  • Brown, A.H.D., 1989a. The case for core collections. In: A.H.D. Brown, O.H. Frankel, D.R. Marshall & J.T. Williams (Eds.), The Use of Plant Genetic Resources, pp. 136–156. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Brown, A.H.D., 1995. The core collection at the crossroads. In: T. Hodgkin, A.H.D. Brown, T.J.L. Hintum & E.A.V. Morales (Eds.), Core Collections of Plant Genetic Resources, pp. 319. John Wiley and Sons, Chichester, UK.

    Google Scholar 

  • Brown, S.K., R.C. Lamb, J.N. Cummins & W.H. Reissig, 1988. Evaluation of Malus germplasm for sources of insect resistance, p. 10. In: International symposium on horticultural germplasm, cultivated and wild. (Abstracts). Chinese Soc Hort Sci Intern Acad Pub, Beijing.

    Google Scholar 

  • Cregan, P.B., T. Jarvik, A.L. Bush, R.C. Shoemaker, K.G. Lark, A.L. Kahler, N. Kaya, T.T. VanToai, D.G. Lohnes, J. Chung & J.E. Sprecht, 1999. An integrated genetic linkage map of the soybean genome. Crop Science 39: 1464–1490.

    Article  CAS  Google Scholar 

  • Cummins, J.N. & H.S. Aldwinckle, 1980. Breeding tree crops. In: M.K. Harris (Ed.), Biology and Breeding for Resistance to Arthropods and Pathogens in Horticultural Plants, pp. 528–545. Texas A and M Univ, College Station, TX.

    Google Scholar 

  • Cummins, J.N., 1983a. Rootstock breeding. In: J.N. Moore & J. Janick (Eds.), Methods in Fruit Breeding, pp. 294–327. Purdue Univ Press, W. Lafayette, IN.

    Google Scholar 

  • Cummins, J.N., 1983b. Breeding apple rootstocks. Plant Breeding Rev 1: 294–394.

    Google Scholar 

  • Dabrowski, Z.T. & A. Rejman, 1975. Some aspects of host plant relationships of the fruit tree red spider mite, Panonychus ulmi (Koch). Zeszyty Probl Post Nauk Roln 171: 73–79.

    Google Scholar 

  • Dayton, D.F. & E.B. Williams, 1968. Independent genes in Malus for resistance to Venturia inaequalis. Proc Am Soc Hort Sci 92: 89–94.

    Google Scholar 

  • Dayton, D.F. & E.B. Williams, 1970. Additional allelic genes in Malus for scab resistance of two reaction types. J Am Soc Hort Sci 95: 735–736.

    Google Scholar 

  • Dunemann, F., R. Kahnau & H. Schmidt, 1994. Genetic relationships in Malus evaluated by RAPD ‘fingerprinting’ of cultivars and wild species. Plant Breeding 113: 150–159.

    Article  Google Scholar 

  • Ellegren, H., C.R. Primmer & B.C. Sheldon, 1995. Microsatellite evolution: Directionality or bias? Nature Genet 11: 36–362.

    Article  Google Scholar 

  • Food and Agriculture Organization, 1997. FAOSTAT database collections. Rome, Italy. http://apps.fao.org/cgi-bin/aphdb. pl?subset=agriculture.

  • Forsline, P.L., 2000. Procedures for collection, conservation, evaluation and documentation of germplasm using Malus as an example. Acta Hort 522: 223–234.

    Google Scholar 

  • Forsline, P.L., 1992. Core subsets in the USDA/NPGS with apple as an example. In: C.G. Davidson & J. Warner (Eds.), Proceedings of the 2nd Workshop on Clonal Genetic Resources: Emerging Issues and New Directions, pp. 172–175. Canadian Agriculture Research Council, Ottawa, Canada.

    Google Scholar 

  • Forsline, P.L. & R.D. Way, 1993. Apple accessions of low priority targeted for removal from the National Plant Germplasm System. Fruit Var Jour 47: 204–214.

    Google Scholar 

  • Frankel, O.H., 1984. Genetic perspectives of germplasm conservation. In: W. Arber, K. Llimensee, W.J. Peacock & P. Starlinger (Eds.), Genetic Manipulation: Impact on Man and Society. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Frey, K.J., 1996. National plant breeding study-I. Human and financial resources devoted to plant breeding research and development in the United States in 1994. Special Report 98. Iowa Agriculture and Home Economics Experiment Station. Ames, IA.

    Google Scholar 

  • Gardner, R., J.N. Cummins & H.S. Aldwinckle, 1980. Inheritance of fire blight resistance in Malus in relation to rootstock breeding. J Amer Soc HortSci 105: 912–916.

    Google Scholar 

  • Garza, J.C., M. Slatkin & N.B. Freimer, 1995. Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol Biol Evol 12: 594–603.

    PubMed  CAS  Google Scholar 

  • Gianfranceschi, L., N. Seglias, R. Tarchini, M. Komjanc & C. Gessler, 1998. Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96: 1069–1076.

    Article  CAS  Google Scholar 

  • Goldstein, D.B. & D.D. Pollock, 1997. Launching microsatellites: A review of mutation processes and methods of phylogenetic inference. J Hered 88: 335–342.

    PubMed  CAS  Google Scholar 

  • Goonewardene, H.F., 1987. E11–24, E14–32 and E36–7 apple germplasm with multiple pest resistance. HortScience 22: 1346–1348.

    Google Scholar 

  • Goonewardene, H.F. & P.H. Howard, 1989. E7–47, E7–54, E29–56, and E31–10 apple germplasm with multiple pest resistance. HortScience 24: 167–169.

    Google Scholar 

  • Hemmat, M., N.F. Weeden, A.K. Szewc-McFadden & S.C. Hokanson, 1998. Mapping of Malus domestica microsatellites in apple and pear. (Abstr.), pp. 148. Proceedings Plant and Animal Genome V, January 12–16, 1997, San Diego, CA.

  • Hokanson, S.C., A.K. Szewc-McFadden, W.F. Lamboy & J.R. McFerson, 1998. Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus × domestica Borkh. core subset collection. Theor Appl Genet 97: 671–683.

    Article  CAS  Google Scholar 

  • Hokanson, S.C., J.R. McFerson, P.L. Forsline, W.F. Lamboy, J.J. Luby, H.S. Aldwinckle & A.D. Djangaliev, 1997. Collecting and managing wild Malus germplasm in its center of diversity. HortScience 32: 173–176.

    Google Scholar 

  • Hough, L.F., J.R. Shay & D.F. Dayton, 1953. Apple scab resistance from Malus floribunda Sieb. Proc Am Soc Hort Sci 62: 341–347.

    Google Scholar 

  • Huckins, C.A., 1972. A revision of the sections of the genus Malus Miller. Ph.D. Thesis, Cornell University, Ithaca, NY.

    Google Scholar 

  • Janick, J., 1974. The apple in Java. HortScience 9: 13–15.

    Google Scholar 

  • Janick, J., J.N. Cummins, S.K. Brown & M. Hemmat, 1996. Apples. In: J. Janick & J.N. Moore (Eds.), Fruit breeding. vol. II. Tree and Tropical Fruits, pp. 1–76. Wiley, New York.

    Google Scholar 

  • Jones, D.A., 1972. Blood samples: Probability of discrimination. J Forens Sci Soc 12: 355–359.

    Article  CAS  Google Scholar 

  • King, G.J., 1996. Progress of apple genetic mapping in Europe. HortScience 31: 1108–1111.

    CAS  Google Scholar 

  • Kloosterman, A.D., B. Budowle & P. Daselaar, 1993. PCRamplification and detection of the human D1S80 VNTR locus. Int J Leg Med 105: 257–264.

    Article  CAS  Google Scholar 

  • Knight, R.L. & F.H. Alston, 1968. Sources of field immunity to mildew (Podosphaera leucotricha). Can J Gen Cytol 10: 294–298.

    Google Scholar 

  • Korban, S.S., 1986. Interspecific hybridization in Malus. HortScience 21: 41–48.

    Google Scholar 

  • Kresovich, S., W.F. Lamboy, J.R. McFerson & P.L. Forsline, 1995. Integrating different types of information to develop core collections, with particular reference to Brassica oleracea and Malus x domestica. In: T. Hodgkin, A.H.D. Brown, T.J.L. Hintum & E.A.V. Morales (Eds.), Core Collections of Plant Genetic Resources, pp. 147–154. John Wiley and Sons, Chichester, UK.

    Google Scholar 

  • Lamboy, W.F. & C.G. Alpha, 1998. Using simple sequence repeats (SSRs) for DNA fingerprinting germplasm accessions of grape (Vitis L.) species. J Am Soc Hortic Sci 123: 182–188.

    CAS  Google Scholar 

  • Langenfeld, W.T., 1991. Apple trees. Morphological evolution, phylogeny, geography and systematics. Riga (Zinatne) 232. (In Russian).

  • Lapkins, K.O., 1969. Segregation of compact growth types in certain apple seedling progenies. Can J Pl Sci 49: 765–768.

    Article  Google Scholar 

  • Lapkins, K.O., 1976. Inheritance of compact growth type in apple. J Am Soc Hort Sci 101: 133–135.

    Google Scholar 

  • Li, Y., 1996. A critical review of the species and the classification of the genus Malus Mill. in the world. Journal of Fruit Science, Vol. 10 (Suppl.) Zhengzhou Fruit Research Institute, pp. 63–81. (In Chinese).

    Google Scholar 

  • Maliepaard, C., F.H. Alston, G. van Arkel, L.M. Brown, E. Chevreau, F. Dunemann, K.M. Evans, S. Gardiner, P. Guilford, A.W. van Heusden, J. Janse, F. Laurens, J.R. Lynn, A.G. Manganaris, A.P.M. den Nijs, N. Periam, E. Rikkerink, P. Roche, C. Ryder, S. Sansavini, H. Schmidt, S. Tartarini, J.J. Verhaegh, M. Vrielinkvan Ginkel & G.J. King, 1998. Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97: 60–73.

    Article  CAS  Google Scholar 

  • Marshall, D.R., 1990. Crop genetic resources: Current and emerging issues. In: A.H.D. Brown, M.H. Clegg, A.L. Kahler & B.S. Weir (Eds.), Plant Population Genetics, Breeding, and Genetic Resources, pp. 367–388. John Wiley and Sons, Chichester, UK.

    Google Scholar 

  • Meulenbroek, B., J. Verhaegh & J. Janse, 1999. Inheritance studies with columnar type trees. Acta Hort 484: 255–259.

    Google Scholar 

  • Momol, M.T., P.L. Forsline, W.F. Lamboy & H.S. Aldwinckle, 1999. Fire blight resistance and horticultural evaluation of wild Malus populations from Central Asia. Acta Hort 489: 229–234.

    Google Scholar 

  • Nei, M., 1972. Genetic distance between populations. Am Nat 106: 283–292.

    Article  Google Scholar 

  • Noiton, D.A.M. & P.A. Alspach, 1996. Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci 121: 773–782.

    Google Scholar 

  • Ragan, W.H., 1926. Nomenclature of the apple: a catalogue index of the known varieties referred to in American publications from 1804 to 1904. USDA Bur Plant Ind Bul 56.

  • Rehder, A., 1940. Manual of cultivated trees and shrubs. Ed. 2. Macmillan, New York.

    Google Scholar 

  • Röder, M.S., J. Plaschke, S.U. König, A. Börner, M.E. Sorrells, S.D. Tanksley & M.W. Ganal, 1995. Abundance, variability and chromosomal location of microsatellites in wheat. Mol Gen Genet 246: 327–333.

    Article  PubMed  Google Scholar 

  • Rohlf, F.J., 1998. NTSYS-pc, numerical taxonomy and multivariate analysis system, version 2.01. Exeter Publishing, Ltd., Setauket, New York.

    Google Scholar 

  • Sax, K., 1959. The cytogenetics of facultative apomixis in Malus species. Journal of the Arnold Arboretum 40: 289–297.

    Google Scholar 

  • Sneath, P.H.A. & R.R. Sokal, 1973. Numerical Taxonomy. W.H. Freeman and Co., San Francisco, CA.

    Google Scholar 

  • Stepanov, S.N., 1974. Species and forms of fruit trees and bushes of the USSR and their utilization in plant breeding. Proc. 19th Intl. Hort. Congr., Warsaw 2: 1–12.

    Google Scholar 

  • Strang, J.G. & C. Stushnoff, 1975. A classification of hardy North American apple cultivars based on hardiness zones. Fruit Var J 29: 78–108.

    Google Scholar 

  • Szewc-McFadden, A.K., S. Bleik, C.G. Alpha, W.F. Lamboy & J.R. McFerson, 1995. Identification of simple sequence repeats in Malus (Apple). HortScience 30: 855.

    Google Scholar 

  • Szewc-McFadden, A.K., W.F. Lamboy, S.C. Hokanson & J.R. McFerson, 1996. Utilization of identified simple sequence repeats (SSRs) in Malus x domestica (Apple) for germplasm characterization. HortScience 31: 619.

    Google Scholar 

  • Tanksley, S.D. & J.C. Nelson, 1996. Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet 92: 191–203.

    Article  Google Scholar 

  • van der Zwet, T. & H.L. Keil, 1979. Fireblight. USDA Hdbk. No. 510. U.S. Govt. Printing Office, Washington, D.C.

    Google Scholar 

  • Walter, K.S. & H.J. Gillett, 1998. 1997 IUCN Red List of Threatened Plants. Compiled by the World Conservation Monitoring Centre. IUCN - The World Conservation Union, Gland, Switzerland and Cambridge, UK.

    Google Scholar 

  • Watkins, R., 1973. Fruit Breeding. Annu. Rpt. E. Malling Res. Sta. 1972. pp. 134–136.

  • Watkins, R., 1981. The main species of Malus. In: B. Hora (Ed.), The Oxford Encyclopedia of Trees of the World, pp. 188–192. Oxford Univ. Press, Oxford.

    Google Scholar 

  • Way, R.D., H.S. Aldwinckle, R.C. Lamb, A. Rejman, S. Sansavini, T. Shen, R. Watkins, M.N. Westwood & Y. Yoshida, 1991. Apples (Malus). In: J.N. Moore & J.R. Ballington (Eds.), Genetic Resources of Temperate Fruit and Nut Crops 1, pp. 3–62. Intl Soc Hort Sci, Wageningen, Netherlands.

    Google Scholar 

  • Weber, J.L., 1990. Human DNA polymorphisms and methods of analysis. Curr Opin Biotechnol 1: 166–171.

    Article  PubMed  CAS  Google Scholar 

  • Weir, B.S., 1989. Sampling properties of gene diversity. In: A.H.D. Brown M.T. Clegg, H.L. Kahler & B.S. Weir (Eds.), Plant Population Genetics, Breeding and Genetic Resources. Sinauer Associates, Sunderland, Mass, pp. 23–42.

    Google Scholar 

  • Williams, E.B. & J. Kuc, 1969. Resistance in Malus to Venturia inaequalis. Ann Rev Phytopath 7: 223–246.

    Article  CAS  Google Scholar 

  • Xiao, J., S. Grandillo, S.N. Ahn, S.R. McCouch & S.D. Tanksley, 1996. Genes from wild rice improve yield. Nature 384: 223–224.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. USDA-ARS Fruit Lab, Building 010A, Rm. 210, BARC-W, 10300 Baltimore Ave., Beltsville, MD, 20705-2350, U.S.A.

    S.C. Hokanson

  2. USDA-ARS Plant Genetic Resources Unit, Cornell University, Geneva, NY, 14456-0462, U.S.A.

    W.F. Lamboy & A.K. Szewc-McFadden

  3. Washington Tree Fruit Research Commission, 1719 Springwater Ave., Wenatchee, WA, 98801, U.S.A.

    J.R. McFerson

Authors
  1. S.C. Hokanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W.F. Lamboy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A.K. Szewc-McFadden
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J.R. McFerson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hokanson, S., Lamboy, W., Szewc-McFadden, A. et al. Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids. Euphytica 118, 281–294 (2001). https://doi.org/10.1023/A:1017591202215

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1017591202215

Search

Navigation