Theoretical and Applied Genetics

, Volume 123, Issue 5, pp 693–704 | Cite as

Genetic diversity and population structure in cultivated sunflower and a comparison to its wild progenitor, Helianthus annuus L

  • J. R. Mandel
  • J. M. Dechaine
  • L. F. Marek
  • J. M. BurkeEmail author
Original Paper


Crop germplasm collections are valuable resources for ongoing plant breeding efforts. To fully utilize such collections, however, researchers need detailed information about the amount and distribution of genetic diversity present within collections. Here, we report the results of a population genetic analysis of the primary gene pool of sunflower (Helianthus annuus L.) based on a broad sampling of 433 cultivated accessions from North America and Europe, as well as a range-wide collection of 24 wild sunflower populations. Gene diversity across the cultivars was 0.47, as compared with 0.70 in the wilds, indicating that cultivated sunflower harbors roughly two-thirds of the total genetic diversity present in wild sunflower. Population structure analyses revealed that wild sunflower can be subdivided into four genetically distinct population clusters throughout its North American range, whereas the cultivated sunflower gene pool could be split into two main clusters separating restorer lines from the balance of the gene pool. Use of a maximum likelihood method to estimate the contribution of the wild gene pool to the cultivated sunflower germplasm revealed that the bulk of the cultivar diversity is derived from two wild sunflower population genetic clusters that are primarily composed of individuals from the east-central United States, the same general region in which sunflower domestication is believed to have occurred. We also identified a nested subset of accessions that capture as much of the allelic diversity present within the sampled cultivated sunflower germplasm collection as possible. At the high end, a core set of 288 captured nearly 90% of the alleles present in the full set of 433, whereas a core set of just 12 accessions was sufficient to capture nearly 50% of the total allelic diversity present within this sample of cultivated sunflower.


Association Mapping Allelic Richness Online Resource Table Helianthus Annuus Wild Progenitor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Patrick Vincourt from INRA as well as the staff of the USDA North Central Regional Plant Introduction Station for providing us with germplasm. Patrick Vincourt also provided valuable scientific input. We thank John Hvala, Jason Strever, Michael Payne, and the University of Georgia greenhouse staff for assistance with data collection and plant maintenance. We are grateful to members of the Burke lab for useful comments on an earlier version of this manuscript. Finally, we would like to thank Brent Hulke of the USDA for helpful discussions regarding this work. This work was funded by a grant from the USDA National Institute of Food and Agriculture to JMB (2008-35300-19263).

Supplementary material

122_2011_1619_MOESM1_ESM.pdf (526 kb)
Online Resource Tables (PDF 525 kb)
122_2011_1619_MOESM2_ESM.pdf (597 kb)
Online Resource Figure 1 (PDF 596 kb)
122_2011_1619_MOESM3_ESM.pdf (250 kb)
Online Resource Figure 2 (PDF 249 kb)
122_2011_1619_MOESM4_ESM.pdf (314 kb)
Online Resource Figure 3 (PDF 313 kb)
122_2011_1619_MOESM5_ESM.pdf (360 kb)
Online Resource Figure 4 (PDF 359 kb)


  1. Acquaah G (2006) Principles of plant genetics and breeding. Blackwell, OxfordGoogle Scholar
  2. Asch DL (1993) Common sunflower (Helianthus annuus L.): the pathway toward domestication. In: Proceedings of the 58th Annual Meeting of the Society for American Archaeology. Society for American Archaeology, St. Louis, pp 1–15Google Scholar
  3. Beard B (1982) Registration of Helianthus germplasm pools III and IV. Crop Sci Crop Sci 22:1276–1277Google Scholar
  4. Bolker B, Okuyama T, Bjorndal K, Bolten A (2003) Sea turtle stock estimation using genetic markers: accounting for sampling error of rare genotypes. Ecol App 12:763–775CrossRefGoogle Scholar
  5. Brothers ME, JF Miller (1999) Core subset for the cultivated sunflower collection. In: Proceedings of 21st Sunflower Research Workshop. Fargo, ND, pp 124–127Google Scholar
  6. Brown C (2008) A lack of linguistic evidence for domesticated sunflower in pre-Columbian Mesoamerica. Proc Natl Acad Sci USA 105:E47PubMedCrossRefGoogle Scholar
  7. Buckler ES, Thornsberry J (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111PubMedCrossRefGoogle Scholar
  8. Burke JM, Knapp SJ, Rieseberg LH (2005) Genetic consequences of selection during the evolution of cultivated sunflower. Genet 171:1933–1940CrossRefGoogle Scholar
  9. Chapman MA, Pashley CH, Wenzler J, Hvala J, Tang S, Knapp SJ, Burke JM (2008) A genomic scan for selection reveals candidates for genes involved in the evolution of cultivated sunflower (Helianthus annuus L.). Plant Cell 20:2931–2945PubMedCrossRefGoogle Scholar
  10. Cheres MT, Knapp SJ (1998) Ancestral origins and genetic diversity of cultivated sunflower: coancestry analysis of public germplasm. Crop Sci 38:1476–1482CrossRefGoogle Scholar
  11. Crites GD (1993) Domesticated sunflower in fifth millennium B.P. Temporal context: new evidence from Middle Tennessee. Am Antiq 58:146–148CrossRefGoogle Scholar
  12. Cronn R, Brothers M, Klier K, Bretting PK, Wendel JF (1997) Allozyme variation in domesticated annual sunflower and its wild relatives. Theor Appl Genet 95:532–545CrossRefGoogle Scholar
  13. Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321PubMedCrossRefGoogle Scholar
  14. Dong GJ, Liu GS, Li KF (2007) Studying genetic diversity in the core germplasm of confectionary sunflower (Helianthus annuus L.) in China based on AFLP and morphological analysis. Russ Jour Genet 43:627–635CrossRefGoogle Scholar
  15. Doyle JL, Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem 19:11–15Google Scholar
  16. Evanno, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  17. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction sites. Genet 131:479–491Google Scholar
  18. Fehr WR (1987) Principles of cultivar development, vol 1, theory and technique. Macmillan, New YorkGoogle Scholar
  19. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  20. Fick GN, Miller JF (1997) Sunflower breeding. In: Scheiter AA (ed) Sunflower production and technology. Amer Society Agron, Madison, pp 395–440Google Scholar
  21. Fusari CM, Lia VV, Hopp HE, Heinz RA, Paniego NB (2008) Identification of single nucleotide polymorphisms and analysis of sinkage disequilibrium in sunflower elite inbred lines using the candidate gene approach. BMC Plant Bio 8:7CrossRefGoogle Scholar
  22. Halliburton R (2004) Introduction to population genetics. Pearson-Prentice Hall, New JerseyGoogle Scholar
  23. Harter AV, Gardner KA, Falush D, Lentz DL, Bye RA, Rieseberg LH (2004) Origin of extant domesticated sunflowers in eastern North America. Nat 430:201–205CrossRefGoogle Scholar
  24. Heiser CB (2008) How old is the sunflower in Mexico? Proc Natl Acad Sci USA 105:E48PubMedCrossRefGoogle Scholar
  25. Heiser CB, Smith DM, Clevenger S, Martin WC (1969) The North American sunflowers (Helianthus). Mem Torrey Bot Club 22:1–218Google Scholar
  26. Hongtrakul V, Huestis GM, Knapp SJ (1997) Amplified fragment length polymorphisms as a tool for DNA fingerprinting sunflower germplasms: genetic diversity among oilseed inbred lines. Theor Appl Genet 95:400–407CrossRefGoogle Scholar
  27. Hurlbert SH (1971) The non-concept of species diversity: a critique and alternative parameters. Ecol 52:577–586CrossRefGoogle Scholar
  28. Hyten DL, Song Q, Zhu Y, Choi I-Y, Nelson RL, Costa JM et al (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103:16666–16671PubMedCrossRefGoogle Scholar
  29. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543CrossRefGoogle Scholar
  30. Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  31. Kinman ML (1970) New developments in the USDA and state experiment station breeding programs. In: Proceedings of 4th International Sunflower Conference, Int Sunflower Assoc, Paris, pp 181–183Google Scholar
  32. Kolkman JM, Berry ST, Leon AJ, Slabaugh MB, Tang S, Gao W et al (2007) Single nucleotide polymorphisms and linkage disequilibrium in sunflower. Genet 177:457–468CrossRefGoogle Scholar
  33. Korell M, Mosges G, Friedt W (1992) Construction of a sunflower pedigree map. Helia 15:7–16Google Scholar
  34. Kuroda Y, Kaga A, Tomooka N, Vaughan D (2010) The origin and fate of morphological intermediates between wild and cultivated soybeans in their natural habitats in Japan. Mol Ecol 19:2346–2360PubMedCrossRefGoogle Scholar
  35. Leclercq P (1969) Une Sterilite male cytoplasmique chez le tournesol. Ann Amélior Plant 19:99–106Google Scholar
  36. Lentz DL, Pohl MD, Alvarado JL, Tarighat S, Bye R (2008a) Sunflower (Helianthus annuus L.) as a pre-Columbian domesticate in Mexico. Proc Natl Acad Sci USA 105:6232–6237PubMedCrossRefGoogle Scholar
  37. Lentz DL, Pohl MD, Bye R (2008b) Reply to Rieseberg and Burke, Heiser, Brown, and Smith: Molecular, linguistic, and archaeological evidence for domesticated sunflower in pre-Columbian Mesoamerica. Proc Natl Acad Sci USA 105:E49–E50CrossRefGoogle Scholar
  38. Liu A, Burke JM (2006) Patterns of nucleotide diversity in wild and cultivated sunflower. Genet 173:321–330CrossRefGoogle Scholar
  39. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinforma 21:2128–2129CrossRefGoogle Scholar
  40. Matus IA, Hayes PM (2002) Genetic diversity in three groups of barley germplasm assessed by simple sequence repeats. Genome 45:1095–1106PubMedCrossRefGoogle Scholar
  41. Morariu VI, Srinivasan BV, Raykar VC, Duraiswami R, Davis LS (2008) Automatic online tuning for fast Gaussian summation. In: Koller D, Schuurmans D, Bengio Y, Bottou L (eds) Adv Neural Inf Process Sys (NIPS) 1113–1120Google Scholar
  42. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genet 89:583–590Google Scholar
  43. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  44. Pella JJ, Milner GB (1987) Use of genetic markers in stock composition analysis. In: Ryman N, Utter FW (eds) Population genetics and fisheries management. UW Press, Seattle, pp 247–276Google Scholar
  45. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  46. Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genet 155:945–956Google Scholar
  47. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genet 67:170–181PubMedCrossRefGoogle Scholar
  48. Purcell S, Cherny SS, Sham PC (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinforma 19:149–150CrossRefGoogle Scholar
  49. Pustovoit VS (1964) Conclusions of work on the selection and seed production of sunflowers (in Russian). Agrobio 5:662–697Google Scholar
  50. Putt ED (1997) Early history of sunflower. In: Scheiter AA (ed) Sunflower production and technology. Amer Society Agron, Madison, pp 1–19Google Scholar
  51. Rieseberg LH, Burke JM (2008) Molecular evidence and the origin of the domesticated sunflower. Proc Natl Acad Sci USA 105:E46PubMedCrossRefGoogle Scholar
  52. Rieseberg LH, Seiler GJ (1990) Molecular evidence and the origin and development of the domesticated sunflower (Helianthus annum Asteraceae). Econ Bot 44:79–91CrossRefGoogle Scholar
  53. Robertson JA, Burns EE (1975) Use of sunflower seed in food products. Crit Rev Food Sci 6:201–240CrossRefGoogle Scholar
  54. Robertson JA, Morrison WH (1977) Effect of heat and frying on sunflower oil stability. Symposium: Oilseeds-new foods for tomorrow. A Oil Chem Soc, New Orleans, LA pp 77A–81AGoogle Scholar
  55. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234PubMedCrossRefGoogle Scholar
  56. Smith BD (1989) Origins of agriculture in eastern North America. Science 246:1566–1571PubMedCrossRefGoogle Scholar
  57. Smith BD (2006) Eastern North America as an independent center of plant domestication. Proc Natl Acad Sci USA 103:2223–12228Google Scholar
  58. Smith BD (2008) Winnowing the archaeological evidence for domesticated sunflower in pre-Columbian Mesoamerica. Proc Natl Acad Sci USA 105:E45PubMedCrossRefGoogle Scholar
  59. Smouse PE, Waples RS, Tworek JA (1990) A genetic mixture analysis for use with incomplete source population data. Can J Fish Aquat Sci 47:620–634CrossRefGoogle Scholar
  60. Soleri D, Cleveland D (1993) Hopi crop diversity and change. J Ethnobiol 13:203–231Google Scholar
  61. Tanksley, Nelson JC (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 92:191–203CrossRefGoogle Scholar
  62. Vavilov NI (1940) The new systematics of cultivated plants. In: Huxley J (ed) The new systematics. Clarendon Press, Oxford, pp 549–566Google Scholar
  63. Vigouroux Y, Mitchell S, Matsuoka Y, Hamblin M, Kresovich S, Smith JSC, Jaqueth J, Smith OS, Doebley J (2005) An analysis of genetic diversity across the maize genome using microsatellites. Genet 169:1617–1630CrossRefGoogle Scholar
  64. Vigouroux Y, Glaubitz J, Matsuoka Y, Goodman MM, Sanchez GJ, Doebley J (2008) Population structure and genetic diversity of New World maize races assessed by DNA microsatellites. Am J Bot 95:1240–1253PubMedCrossRefGoogle Scholar
  65. Wahlund S (1928) Zusammensetzung von Population und Korrelationserscheinung vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106CrossRefGoogle Scholar
  66. Wills DM, Burke JM (2006) Chloroplast DNA variation confirms a single origin of domesticated sunflower (Helianthus annuus L.). J Hered 97:403–408PubMedCrossRefGoogle Scholar
  67. Wills DM, Hester ML, Liu A, Burke JM (2005) Chloroplast SSR polymorphisms in the Compositae and the mode of organellar inheritance in Helianthus annuus. Theor Appl Genet 110:941–947PubMedCrossRefGoogle Scholar
  68. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefGoogle Scholar
  69. Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar
  70. Yue B, Cai WX, Vick BA, Hu JG (2009) Genetic diversity and relationships among 177 public sunflower inbred lines assessed by TRAP markers. Crop Sci 49:1242–1249CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • J. R. Mandel
    • 1
  • J. M. Dechaine
    • 2
  • L. F. Marek
    • 3
  • J. M. Burke
    • 1
    Email author
  1. 1.Miller Plant SciencesUniversity of GeorgiaAthensUSA
  2. 2.University Way Central Washington UniversityEllensburgUSA
  3. 3.Iowa State UniversityAmesUSA

Personalised recommendations