Genetic Resources and Crop Evolution

, Volume 60, Issue 2, pp 763–776

Analysis of average standardized SSR allele size supports domestication of soybean along the Yellow River

  • Ying-hui Li
  • Chen Zhang
  • Marinus J. M. Smulders
  • Wei Li
  • Yan-song Ma
  • Qu Xu
  • Ru-zhen Chang
  • Li-juan Qiu
Research Article


Soybean (Glycine max) was domesticated in China from its wild progenitor G. soja. The geographic region of domestication is, however, not exactly known. Here we employed the directional evolution of SSR (microsatellite) repeats (which mutate preferentially into longer alleles) to analyze the domestication process and to infer the most ancestral soybean landraces. In this study, the average standardized SSR allele sizes across 42 SSR loci in 62 accessions of G. soja were determined, and compared with those in 1504 landraces of G. max, collected from all over China and representing the diversity in the gene bank. The standardized SSR allele size in the landraces (0.009) was significantly (P = 8.63 × 10−58) larger than those in G. soja (−0.406). Pairwise comparisons between inferred clusters and sub-clusters of Chinese landraces indicated that the average standardized SSR allele size also increased with the further differentiation of landraces populations. Spring-sowed types had the shortest size, followed by summer-sown types, while the sub-cluster of autumn-sown type had the largest length. The spring-sowed landraces located near the middle region along the Yellow River had the smallest allele sizes, indicating that this is the most ancestral population of cultivated soybean. We concluded that soybean was most likely domesticated in the middle region of the Yellow River in central China, initially as a spring-sown type.


Directional evolution Domestication Glycine max Glycine soja Landrace SSR 



NorthEast region, Spring-sowing type, Model-based


North region, Spring-sowing type, Model-based


Huanghuai (Yellow river) region, Summer-sowing type, Model-based


South region, Spring-sowing type, Model-based


South region, Spring-sowing type, Southwest, Model-based


South region, Summer-sowing type, Model-based


South region, Summer-sowing type, Southwest, Model-based


  1. Amos W, Rubinsztein DC (1996) Microsatellites are subject to directional evolution. Nat Genet 12(1):13–14PubMedCrossRefGoogle Scholar
  2. Amos W, Hutter CM, Schug MD, Aquadro CF (2003) Directional evolution of size coupled with ascertainment bias for variation in drosophila microsatellites. Mol Biol Evol 20:660–662PubMedCrossRefGoogle Scholar
  3. Anthony F, Combes M, Astorga C, Bertrand B, Graziosi G, Lashermes P (2002) The origin of cultivated Coffea arabica L. varieties revealed by AFLP and SSR markers. Theor Appl Genet 104(5):894–900PubMedCrossRefGoogle Scholar
  4. Carter TE, Nelson RL, Sneller CH, Cui ZL (eds) (2004) Genetic diversity in soybean. Soybeans: improvement, production and uses. ASA, CSSA, SSSA, MadisonGoogle Scholar
  5. Chang RZ (1989) Studies on the origin of the cultivated soybean (Glycine max (L) Merr.) Chinese J Oil Crops Sci 1:1–6 (in Chinese with English abstract)Google Scholar
  6. Cornille A, Gladieux P, Smulders M, Roldán-Ruiz I, Laurens F, Cam B, Nersesyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang X, Tenaillon M, Giraud T (2012) 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):e1002703PubMedCrossRefGoogle Scholar
  7. Dong YS, Zhao LM, Liu B, Wang ZW, Jin ZQ, Sun H (2004) The genetic diversity of cultivated soybean grown in China. Theor Appl Genet 108(5):931–936PubMedCrossRefGoogle Scholar
  8. Ellegren H, Primmer CR, Sheldon BC (1995) Microsatellite ‘evolution’: directionality or bias? Nat Genet 11(4):360–362PubMedCrossRefGoogle Scholar
  9. Forbes SH (1995) Microsatellite evolution in congeneric mammals: domestic and bighorn sheep. Mol Biol Evol 12(6):1106–1113PubMedGoogle Scholar
  10. Fukuda Y (1933) Cyto-genetical studies on the wild and cultivated Manchurian soy beans (Glycine L.). Jpn J Bot 6:489–506Google Scholar
  11. Gai JY, Xu DH, Gao Z, Shimamoto Y, Abe J, Fukushi H, Kitajima S (2000) Studies on the evolutionary relationship among eco-types of G.max and G. soja in China. Acta Agri Sin 26(5):513–520 (in Chinese with English abstract)Google Scholar
  12. Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169(3):1631–1638PubMedCrossRefGoogle Scholar
  13. Grassi F, Labra M, Imazio S, Spada A, Sgorbati S, Scienza A, Sala F (2003) Evidence of a secondary grapevine domestication centre detected by SSR analysis. Theor Appl Genet 107(7):1315–1320PubMedCrossRefGoogle Scholar
  14. Guo J, Wang Y, Song C, Zhou J, Qiu L, Huang H (2010) A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences. Ann Bot 106(3):505–514PubMedCrossRefGoogle Scholar
  15. Harlan JR (1971) Agricultural origins: centers and noncenters. Science 174(4008):468PubMedCrossRefGoogle Scholar
  16. Hymowitz T, Newell CA (1981) Taxonomy of the genus Glycine, domestication and uses of soybeans. Econ Bot 35(3):272–288CrossRefGoogle Scholar
  17. Kim M, Lee S, Vana K, Kimb T, Jeong S, Choi I, Kim D, Lee Y, Park D, Ma J, Kim W, Kim B, Park S, Lee K, Kim D, Kim K, Shin J, Jang Y, Kim K, Liu W, Chaisan T, Kang Y, Lee Y, Kim K, Moon J, Schmutzh J, Jacksone S, Bhak J, Lee S (2010) Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci USA 107:22032–22037PubMedCrossRefGoogle Scholar
  18. Li FS (1994) A study on origin and evolution of soybean. Soybean Sci 13(1):61–66 (in Chinese with English abstract)Google Scholar
  19. Li YH, Guan RX, Liu ZH, Ma YS, Wang LX, Li LH, Lin FY, Luan WJ, Chen PY, Yan Z, Guan Y, Zhu L, Ning X, Smulders MJM, Li W, Piao R, Cui YH, Yu ZM, Guan M, Chang RZ, Hou AF, Shi AN, Zhang B, Zhu SL, Qiu LJ (2008) Genetic structure and diversity of cultivated soybean (Glycine max (L.) Merr.) landraces in China. Theor Appl Genet 117:857–871PubMedCrossRefGoogle Scholar
  20. Li YH, Li W, Zhang C, Yang L, Chang RZ, Gaut BS, Qiu LJ (2010a) Genetic diversity in domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence repeat and single nucleotide polymorphism loci. New Phytol 188:242–253PubMedCrossRefGoogle Scholar
  21. Li YH, Smulders MJM, Chang RZ, Qiu LJ (2010b) Analysis of SSRs uncovers hierarchical structure and genetic diversity in Chinese soybean landraces. Agric Sci China 9(12):1739–1748CrossRefGoogle Scholar
  22. Liu MS, Amirkhanian VD (2003) DNA fragment analysis by an affordable multiple-channel capillary electrophoresis system (Short communication). Electrophoresis-Weinheim 24(1/2):93–95CrossRefGoogle Scholar
  23. Liu K, Muse S (2005) Power marker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129PubMedCrossRefGoogle Scholar
  24. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez G (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99(9):6080–6084PubMedCrossRefGoogle Scholar
  25. Maughan PJ, Saghi Maroof MA, Buss GR (1995) Microsatellite and amplified sequence length polymorphisms in cultivated and wild soybean. Genome 38(4):715–723PubMedCrossRefGoogle Scholar
  26. Neff BD, Gross MR (2001) Microsatellite evolution in vertebrates: inference from acdinucleotide repeats. Evolution 55(9):1717–1733PubMedGoogle Scholar
  27. Petit RJ, Deguilloux MF, Chat J, Grivet D, Garnier-Gere P, Vendramin GG (2005) Standardizing for microsatellite length in comparisons of genetic diversity. Mol Ecol 14(3):885–890PubMedCrossRefGoogle Scholar
  28. Qiu L, Cao Y, Chang R, Zhou X, Wang G, Sun J, Xie H, Zhang B, Li X, Xu Z, Liu L (2003) Establishment of Chinese soybean (G. max) core collection I. sampling strategy. Sci Agri Sin 36(12):1442–1449 (in Chinese with English abstract)Google Scholar
  29. Qiu L, Li Y, Guan R, Liu Z, Wang L, Chang R (2009) Establishment, representative testing and research progress of soybean core collection and mini core collection. Acta Agron Sin 35(4):571–579 (in Chinese with English abstract)CrossRefGoogle Scholar
  30. Ren TH, Chen F, Zou YT, Jia YH, Zhang HQ, Yan BJ, Ren ZL (2011) Evolutionary trends of microsatellites during the speciation process and phylogenetic relationships within the genus Secale. Genome 54:316–326PubMedCrossRefGoogle Scholar
  31. Rubinsztein DC, Amos W, Leggo J, Goodburn S, Jain S, Li SH, Margolis RL, Ross CA, Ferguson-Smith MA (1995) Microsatellite evolution: evidence for directionality and variation in rate between species. Nat Genet 10(3):337–343PubMedCrossRefGoogle Scholar
  32. Sun JX, Mullikin JC, Patterson N, Reich DE (2009) Microsatellites are molecular clocks that support accurate inferences about history. Mol Biol Evol 26(5):1017–1027PubMedCrossRefGoogle Scholar
  33. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24(21):2498PubMedCrossRefGoogle Scholar
  34. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  35. van Heerwaarden J, Doebley J, Briggs W, Glaubitz J, Goodman M, Gonzalez J, Ross-Ibarra J (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc Natl Acad Sci USA 108:1088–1092PubMedCrossRefGoogle Scholar
  36. Vavilov NI (1951) The origin, variation, immunity and breeding of cultivated plants. Translated from the Russian by K. Starrchester. Chron Bot 13:1–364Google Scholar
  37. Vigouroux Y, Matsuoka Y, Doebley J (2003) Directional evolution for microsatellite size in maize. Mol Biol Evol 20(9):1480–1483PubMedCrossRefGoogle Scholar
  38. Wang LX, Guan RX, Zhang XL, Chang RZ, Qiu LJ (2006) Genetic diversity of Chinese cultivated soybean revealed by SSR markers. Crop Sci 46(3):1032–1038CrossRefGoogle Scholar
  39. Wang LX, Guan RX, Li YH, Lin FY, Luan WJ, Li W, Ma YS, Liu ZX, Chang RZ, Qiu LJ (2008) Genetic diversity of Chinese spring soybean germplasm revealed by SSR markers. Plant Breed 127(1):56–61Google Scholar
  40. Xu B, Zhao SW, Zhou SH, Zheng HY, Hu ZA, Wang HX (1985) Seed protein electrophoresis profiles of wild soybean (G. soja) in China: the frequencies and geographical distribution of Tia and Sp1 alleles and the hypothesis on the original area of soybean. Soybean Sci 4:7–13 (in Chinese with English abstract)Google Scholar
  41. Xu B, Zheng HY, Lu QH, Zhao SW, Zhou SH, Hu ZA (1986) Three new evidences of the original area of soybean. Soybean Sci 5(2):123–130 (in Chinese with English abstract)Google Scholar
  42. Xu D, Abe J, Gai J, Shimamoto Y (2002) Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean. Theor Appl Genet 105(5):645–653PubMedCrossRefGoogle Scholar
  43. Zhao TJ, Gai JY (2004) The origin and evolution of cultivated soybean [Glycine max (L.) Merr.]. Sci Agri Sin 37 (7):954–962 (in Chinese with English abstract)Google Scholar
  44. Zhou XA, Peng YH, Wang GX, Chang RZ (1998) Preliminary studies on the centers of genetic diversity and origination of cultivated soybean in China. Sci Agri Sin 31(003):37–43 (in Chinese with English abstract)Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Ying-hui Li
    • 1
  • Chen Zhang
    • 1
  • Marinus J. M. Smulders
    • 2
  • Wei Li
    • 1
  • Yan-song Ma
    • 4
  • Qu Xu
    • 3
  • Ru-zhen Chang
    • 1
  • Li-juan Qiu
    • 1
  1. 1.The National Key Facility for Crop Gene Resources and Genetic Improvement (NFCRI), Institute of Crop ScienceChinese Academy of Agricultural SciencesBeijingPeople’s Republic of China
  2. 2.Plant Research International, Wageningen UR Plant BreedingWageningenThe Netherlands
  3. 3.High School Attached to Capital Normal UniversityBeijingPeople’s Republic of China
  4. 4.Soybean Research InstituteHeilongjiang Academy of Agricultural Sciences (HAAS)HarbinPeople’s Republic of China

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