Skip to main content
Log in

Genetic structure and differentiation of Oryza sativa L. in China revealed by microsatellites

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

China is one of the largest centers of genetic diversity of Oryza sativa L. in the world. Using a genetically representative primary core collection of 3,024 rice landraces in China, we analyzed the genetic structure and intraspecific differentiation of O. sativa, and the directional evolution of SSR. The genetic structure was investigated by model-based structure analysis and construction of neighbor-joining phylogenetic tree. Comparison between genetic structure and predefined populations according to Ting’s taxonomic system revealed a hierarchical genetic structure: two distinct subspecies, each with three ecotypes and different numbers of geo-ecogroups within each ecotype. Two subspecies evidently resulted from adaptation to different environments. The different cropping systems imposed on the subspecies led to further differentiation, but the variation within each subspecies resulted from different causes. Indica, under tropical-like or lowland-like environments, exhibited clear differentiation among seasonal ecotypes, but not among soil-watery ecotypes; and japonica showed clear differences between soil water regime ecotypes, but not among seasonal ecotypes. Chinese cultivated rice took on evident directional evolution in microsatellite allele size at several aspects, such as subspecies and geographical populations. Japonica has smaller allele sizes than indica, and this may partly be the result of their different domestication times. Allele size was also negatively correlated with latitude and altitude, and this may be interpreted by different mutation rates, selection pressures, and population size effects under different environments and cropping systems.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • AGRTPR—a study group on the response to temperature and photoperiod of rice. (1978) Studies on the photoperiod and temperature ecology of rice cultivars in China. Science Press, Beijing, China, 154 pp (in Chinese)

  • Akagi H, Yokozeki Y, Nagaki A, Fujimura T (1997) Highly polymorphic microsatellites of rice consist of AT repeats and a classification of closely related cultivars with these microsatellite loci. Theor Appl Genet 94:61–67

    Article  PubMed  CAS  Google Scholar 

  • Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME (1993) Optimizing parental selection for genetic linkage maps. Genome 36:181–186

    Article  PubMed  CAS  Google Scholar 

  • Banchs L, Bosch A, Guimera J, Lázaro C, Puig A, Estivill X (1994) New alleles at microsatellite loci in CEPH families mainly arise from somatic mutations in the lymphoblastold cell lines. Hum Mutat 3:365–372

    Article  PubMed  CAS  Google Scholar 

  • Bleiweiss R (1998) Slow rate of molecular evolution in high-elevation humming birds. Proc Natl Acad Sci USA 95:612–616

    Article  PubMed  CAS  Google Scholar 

  • Cai HW, Morishima H (2000) Diversity of rice varieties and cropping system in Bangladesh deepwater areas. Jpn Agric Res Q 34:221–226

    Google Scholar 

  • Cheng KS, Lu YX, Luo J, Huang NW, Lin GR, Wang XK (1984a) Studies on indigenous rice in Yunnan and their utilization—the photo-thermo-response patterns of rices in Yunnan province and their relation to the classification of maturity roups. Acta Agron Sin 10(3):163–171

    Google Scholar 

  • Cheng KS, Zhou JW, Lu YX, Huang NW, Wang XK (1984b) Studies on the indigenous rices in Yunnan and their utilization II. Revised classification of Asian cultivated rice. Acta Agron Sin 10:271–280

    Google Scholar 

  • Cheng CY, Motohashi R, Tsuchimoto S, Fukuta Y, Ohtsubo H, Ohtsubo E (2003) Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol Biol Evol 20:67–75

    Article  PubMed  CAS  Google Scholar 

  • Cooper G, Burroughs NJ, Rand DA, Rubinsztein DC, Amos W (1999) Markov chain Monte Carlo analysis of human Y-chromosome microsatellites provides evidence of biased mutation. Proc Natl Acad Sci USA 96:11916–11921

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Genet 5:435–445

    CAS  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 

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Flessa KW, Jablonski D (1996) The geography of evolutionary turnover: a global analysis of extant bivalves. In: Jablonski D, Erwin DH, Lipps JH (eds) Evolutionary palaeobiology. University of Chicago Press, Chicago, pp 376–397

    Google Scholar 

  • Gao LZ, Innan H (2008) Nonindependent domestication of the two rice subspecies, Oryza sativa ssp. indica and ssp. japonica, demonstrated by multilocus microsatellites. Genetics 179:965–976

    Article  PubMed  CAS  Google Scholar 

  • Gao H, Williamson S, Bustamante CD (2007) An MCMC approach for joint inference of population structure and inbreeding rates from multi-locus genotype data. Genetics 176:1635–1651

    Article  PubMed  Google Scholar 

  • Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638

    Article  PubMed  CAS  Google Scholar 

  • Gillooly JF, Allen AP, West GB, Brown JH (2005) The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc Natl Acad Sci USA 102:140–145

    Article  PubMed  CAS  Google Scholar 

  • Glaszmann JC (1987) Isozymes and classification of Asian rice varieties. Theor Appl Genet 74:21–30

    Article  CAS  Google Scholar 

  • Goldstein DB, Schlotterer C (1999) Microsatellites: evolution and applications. Oxford University Press, Oxford

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html

  • Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • ICGRCAAS (Institute of Crop Germplasm Resources of China Academy of Agricultural Science) (1996) Catalogue of rice germplasm resources in China (1988–1993). China Agricultural Press, Beijing

    Google Scholar 

  • Jablonski D (1993) The tropics as a source of evolutionary novelty through geological time. Nature 364:142–144

    Article  Google Scholar 

  • Kato S, Kosaka H, Hara S (1928) On the affinity of rice varieties as shown by the fertility of rice plants. Bull Sci Fac Agric Kyushu Univ 3:132–147

    Google Scholar 

  • Khush G (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  PubMed  CAS  Google Scholar 

  • Kochko AD (1987) Isozyme variability of traditional rice in Africa. Theor Appl Genet 73:675–682

    Article  Google Scholar 

  • Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312:1382–1396

    Article  CAS  Google Scholar 

  • Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587

    Article  PubMed  CAS  Google Scholar 

  • Li ZC, Zhang HL, Cao YS, Qiu ZE, Wei XH, Tang SX, Yu P, Wang XK (2003) Studies on the sampling strategy for the primary core collection of Chinese ingenious rice. Acta Agron Sin 29:20–24

    CAS  Google Scholar 

  • Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936–1939

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Muse S (2004) PowerMarker: new genetic data analysis software, version 2.7 (http://www.powermarker.net/)

  • Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA (2006) Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa L. Proc Natl Acad Sci USA 103:9578–9583

    Article  PubMed  CAS  Google Scholar 

  • Manly BFJ (1985) The statistics of natural selection. Chapman and Hall, London

    Google Scholar 

  • Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data

  • Nakagawa H, Yamagishi J, Miyamoto N, Motoyama M, Yano M, Nemoto K (2005) Flowering response of rice to photoperiod and temperature: a QTL analysis using a phenological model. Theor Appl Genet 110:778–786

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Oka HI (1988) Origin of cultivated rice. Japan Science Society Press, Tokyo

    Google Scholar 

  • Oka HI (1992) Ecology of wild rice planted in Taiwan III. Differences in regenerating strategies among genetic stocks. Bot Bull Acad Sin 33:133–140

    Google Scholar 

  • Panaud O, Chen X, McCouch SR (1996) Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Mol Gen Genet 252:597–607

    PubMed  CAS  Google Scholar 

  • Primmer CR, Ellegren H, Saino N, Moller AP (1996) Directional evolution in germline microsatellite mutations. Nat Genet 13:391–393

    Article  PubMed  CAS  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 

  • Rohlf F (1997) NTSYS-pc: numerical taxonomy and multivariate analysis system, version 2.00. Exeter Software, Setauket, New York

    Google Scholar 

  • Rosenberg NA (2002) Distruct: a program for the graphical display of structure results. (http://www.cmb.usc.edu/~noahr/distruct.html)

  • 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 10:337–343

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sano R, Morishima H (1992) Indica-japonica differentiation of rice cultivars viewed from the variation in key characters and isozymes with special reference to land races from the Himalayan hilly areas. Theor Appl Genet 84:266–274

    Article  Google Scholar 

  • Second G (1982) Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25–57

    Article  Google Scholar 

  • Sokal RR (1979) Testing statistical significance of geographic variation patterns. Syst Zool 28:227–232

    Article  Google Scholar 

  • Stehli FG, Douglas DG, Newell ND (1969) Generation and maintenance of gradients of taxonomic diversity. Science 164:947–949

    Article  PubMed  Google Scholar 

  • Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD et al (2007) Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3:1418–1424

    Article  CAS  Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399

    PubMed  CAS  Google Scholar 

  • Tam SM, Mhiri C, Vogelaar A, Kerkveld M, Pearce SR, Grandbastien M (2005) Comparative analyses of genetic diversities within tomato and pepper collections detected by retrotransposon-based SSAP, AFLP and SSR. Theor Appl Genet 110:819–831

    Article  PubMed  CAS  Google Scholar 

  • Ting Y (1957) The origin and evolution of cultivated rice in China. Acta Agron Sin 8:243–260

    Google Scholar 

  • Udupa SM, Baum M (2001) High mutation rate and mutational bias at (TAA)n microsatellite loci in chickpea (Cicer arietinum L.). Mol Gen Genet 265:1097–1103

    CAS  Google Scholar 

  • Vergara BS, Chang TT (1985) The flowering response of the rice plant to photoperiod, 4th edn. IRRI, Los Banos, Philippines, p 61

    Google Scholar 

  • Vigouroux Y, Matsuoka Y, Doebley J (2003) Directional evolution for microsatellite size in maize. Mol Biol Evol 20:1480–1483

    Article  PubMed  CAS  Google Scholar 

  • Wang MX, Zhang HL, Zhang DL, Qi YW, Fan ZL, Li DY, Pan DJ, Cao YS, Qiu ZE, Yu P, Yang QW, Wang XK, Li ZC (2008) Genetic structure of Oryza rufipogon Griff. in China. Heredity (http://www.nature.com/hdy/journal/vaop/ncurrent/full/hdy200861a.html)

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

  • Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417

    PubMed  Google Scholar 

  • Weber J, Wang C (1993) Mutation of short tandem repeats. Hum Mol Genet 8:1123–1128

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimation F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Xie ZW, Lu YQ, Ge S, Hong DY, Li FZ (2001) Clonality in wild rice (Oryza rufipogon, Poaceae) and its implications for conservation management. Am J Bot 88:1058–1064

    Article  Google Scholar 

  • Xu XH, Wang GC, Zheng XB, Wang HX (1974) A report on the vertical distribution of the rice varieties in Simao, Yunnan. Acta Bot Sin 16:208–222

    Google Scholar 

  • Yeh FC, Yang RC, Boyle T (1999) PopGene version 1.31, Microsoft Window-based freeware for population genetic analysis. http://www.ualberta.ca/~fyeh/

  • Zeven AC (1998) Landraces: a review of definitions and classifications. Euphytica 104:127–139

    Article  Google Scholar 

  • Zhang DL, Zhang HL, Wei XH, Qi YW, Wang MX, Sun JL, Ding L, Tang SX, Qiu ZE, Cao YS, Wang XK, Li ZC (2007a) Genetic structure and diversity of Oryza sativa L. in Guizhou, China. Chin Sci Bull 52:343–351

    Article  CAS  Google Scholar 

  • Zhang HL, Sun JL, Wang MX, Liao DQ, Zeng YW, Shen SQ, Yu P, Wang XK, Li ZC (2007b) Genetic structure and phylogeography of rice landraces in Yunnan, China revealed by SSR. Genome 50:72–83

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Professor Robert A McIntosh, University of Sydney, for suggested revisions to the manuscript. This research was supported by the National Basic Research Program of China (“973” Program, 2004CB117201), Program for Changjiang Scholars and Innovative Research Team in University, and Program of Introducing Talents of Discipline to Universities (111-2-03).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hongliang Zhang or Zichao Li.

Additional information

Communicated by J. Yu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 448 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, D., Zhang, H., Wang, M. et al. Genetic structure and differentiation of Oryza sativa L. in China revealed by microsatellites. Theor Appl Genet 119, 1105–1117 (2009). https://doi.org/10.1007/s00122-009-1112-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1112-4

Keywords

Navigation