Abstract
Cold tolerance at booting stage is one of the major determinants for a stable yield of rice (Oryza sativa L.) in many high elevation or high latitude regions. Understanding the genetic basis of cold tolerance is crucial for the improvement of cold tolerance through breeding. In this study, association mapping was performed in 347 rice accessions worldwide with different statistical models in order to identify the genetic marker loci/QTL associated with cold tolerance traits at the booting stage. The evaluation of cold tolerance for all the traits was conducted under natural low temperature in Yunnan and cold water irrigation in Jilin. The 148 SSRs were used for the genotyping. Population structure analysis identified three main subpopulations for the accessions that corresponded to major geographic origins. The relative kinship analysis revealed a weak or no relationship for most of the individual pairs. Model comparisons indicated that the Q+K model controlling both population structure (Q) and the relative kinship (K) was performed better than other models in association mapping. In total, 24 markers were identified that were significantly associated with cold tolerance, including five markers in Yunnan and 19 markers in Jilin. Moreover, RM282, RM252, RM335 and RM6824 were identified in multiple environments or years. Many of these identified markers were located either in or nearby the regions where the QTLs have been reported for cold tolerance at booting stage. These results highlighted the targeted regions for future studies and might be subsequently used in breeding programs to trace and select the useful alleles by MAS.
Similar content being viewed by others
References
Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356
Andaya VC, Mackill DJ (2003) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica×indica cross. Theor Appl Genet 106:1084–1090
Bradbury PJ, Zhang ZW, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Camus-Kulandaivelu L, Veyrieras JB, Madur D et al (2006) Maize adaptation to temperate climate: relationship with population structure and polymorphism in the Dwarf8 gene. Genetics 10:1534–1572
Dai LY, Lin XH, Ye CR et al (2004) Identification of quantitative trait loci controlling cold tolerance at the reproductive stage in Yunnan landrace of rice, Kunmingxiaobaigu. Breed Sci 54:253–258
Doyle JJ, Dickson EE (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36:715–722
Ehrenreich IM, Hanzawa Y, Chou L et al (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183:325–335
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
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolut Bioinform Online 1:47–50
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
Flint-Garcia SA, Thuillet AC, Yu JM et al (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064
Garris AJ, Tai TH, Coburn J et al (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638
Hagenblad J, Nordborg M (2002) Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics 161:289–298
Hall D, Tegstrom C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genom 9:157–165
Han LZ, Qiao YL, Zhang YY et al (2005) Identification of QTLs for cold tolerance at the booting stage in rice. Acta Agronomica Sinica 31(5):653–657
Hardy OJ, Vekemans X (2002) Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Huang XH, Wei XH, Sang T et al (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967
Huang XH, Yan Zhao, Wei XH et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 21:1801–1806
Jin L, Lu Y, Xiao P et al (2010) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121:475–487
Jun TH, Van K, Kim MY et al (2008) Association analysis using SSR markers to find QTL for seed protein content in soybean. Euphytica 162:179–191
Kraakman ATW, Niks RE, Van den Berg PMMM et al (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168(1):435–446
Kuroki M, Koji S, Matsuba S et al (2007) A quantitative trait locus for cold tolerance at the booting stage on rice chromosome 8. Theor Appl Genet 115:593–600
Lapitan VC, Brar DS, Abe T et al (2007) Assessment of genetic diversity of Philippine rice cultivars carrying good quality traits using SSR markers. Breed Sci 57:236–270
Li XB, Yan WG, Agrama HA et al (2012) Unraveling the complex trait of harvest index with association mapping in rice (Oryza sativa L.). PLoS ONE 7(1):e29350
Liu KJ, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129
Ma L, Yu XQ, Zhao FS (2010) SSR-based analysis on genetic diversity of rice landraces from Guizhou province. China. Chin J Rice Sci 24(3):237–243
Malysheva-Otto LV, Ganal MW, Röder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet 7:6
Mather KA, Caicedo AL, Polato NR et al (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232
Mori M, Onishi K, Tokizono Y et al (2011) Detection of a novel quantitative trait locus for cold tolerance at the booting stage derived from a tropical japonica rice variety Silewah. Breeding Sci 61:61–68
Myles S, Peiffer J, Brown PJ et al (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202
Nordborg M, Borevitz JO, Bergelson J et al (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193
Olsen KM, Halldorsdottir SS, Stinchcombe JR et al (2004) Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics 167:1361–1369
Ordonez SA Jr, Silva J, Oard JH (2010) Association mapping of grain quality and flowering time in elite japonica rice germplasm. J Cereal Sci 51:337–343
Palaisa KA, Morgante M, Williams M et al (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806
Pritchard JK, Rosenberg NA (1999) Use of unlinked genetic markers to detect population stratification in association studies. Am J Hum Genetics 65:220–228
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rakshit S, Rakshit A, Matsumura H et al (2007) Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731–743
Remington DL, Thornsberry JM, Matsuoka Y et al (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Rohlf F (2000) FNTSYS-PC numerical taxonomy and multivariate analysis system ver 2.11L. Applied Biostatistics, Newyork
Saito K, Miura K, Nagano K et al (2001) Identification of two closely linked quantitative trait loci for cold tolerance on chromosome 4 of rice and their association with anther length. Theor Appl Genet 103:862–868
Saito K, Hayano-Saito Y, Maruyama-Funatsuki W et al (2004) Physical mapping and putative candidate gene identification of a quantitative trait locus Ctb1 for cold tolerance at the booting stage of rice. Theor Appl Genet 109:515–522
Saito K, Hayano-Saito Y, Kuroki M et al (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant Sci 179:97–102
Takeuchi Y, Hayasaka H, Chiba B et al (2001) Mapping quantitative trait loci controlling cool-temperature tolerance at the booting stage in temperate japonica rice. Breed Sci 51:191–197
Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tenaillon MI, Sawkins MC, Long AD et al (2001) Patterns of DNA sequence polymorphism along chromosome1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9916
Thomson MJ, Septiningsih EM, Suwardjo F et al (2007) Genetic diversity analysis of traditional and improved Indonesian rice (Oryza sativa L.) germplasm using microsatellite markers. Theor Appl Genet 114:559–568
Wang LQ, Liu WJ, Xu Y et al (2007) Genetic basis of 17 traits and viscosity parameters characterizing the eating and cooking quality of rice grain. Theor Appl Genet 115:463–476
Wen W, Mei H, Feng F et al (2009) Population structure and association mapping on chromosome 7 using a diverse panel of Chinese germplasm office(Oryza sativa L.). Theor Appl Genet 119:459–470
Whitt SR, Buckler ES (2003) Using natural allelic diversity to evaluate gene function. Methods Mol Biol 236:123–139
Wilson LM, Whitt SR, Ibanez AM et al (2004) Dissection of maize kernel composition and starch production by candidate gene associations. Plant Cell 16:2719–2733
Xu YB, Beachell H, McCouch SR (2005) A marker-based approach to broadening the genetic base of rice in the USA. Crop Sci 44:1947–1959
Xu L, Zhou L, Zeng Y et al (2008) Identification and mapping of quantitative trait loci for cold tolerance at the booting stage in a japonica rice near-isogenic line. Plant Sci 174:340–347
Yan JB, Shah T, Warburton M et al (2009a) Genetic characterization of a global maize collection using SNP markers. PLoS ONE 4:e8451
Yan WG, Li Y, Agrama HA et al (2009b) Association mapping of stigma and spikelet characteristics in rice (Oryza sativa L.). Mol Breed 24(3):277–292
Yan JB, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L) genetic improvement. Crop Sci 51:433–449
Yang XH, Yan JB, Shah T et al (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431
Yu JM, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:1–6
Yu JM, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhang HL, Sun JL, Wang MX et al (2006) Genetic structure and phylogeography of rice landraces in Yunnan, China, revealed by SSR. Genome 50:72–83
Zhang P, Li J, Li X et al (2011) Population structure and genetic diversity in a rice core collection (Oryza sativa L.) investigated with SSR markers. PLoS ONE 6(12):e27565
Zhang LN, Cao GL, Han LZ (2012) Analysis of genetic diversity of japonica rice landrace in China with microsatellite marker. Acta Agron Sinica 45(3):405–413
Zhou L, Zeng YW, Zheng WW et al (2010) Fine mapping a QTL qCTB7 for cold tolerance at the booting stage on rice chromosome 7 using a near-isogenic line. Theor Appl Genet 121:895–905
Zhu YL, Song QJ, Hyten DL et al (2003) Single-nucleotide polymorphisms in soybean. Genetics 63(3):1123–1134
Zhu C, Gore M, Buckler ES et al (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20
Zhu C, Yu J (2009) Nonmetric multidimensional scaling corrects for population structure in association mapping with different sample types. Genetics 182:875–888
Acknowledgments
This work was supported by project 973 (2010CB125904-5), the National Key Technology Research and Development Program of China (2013BAD01B02-2), the Protective Program of Crop Germpalsm of China (NB2012-2130135-25-01).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cui, D., Xu, Cy., Tang, Cf. et al. Genetic structure and association mapping of cold tolerance in improved japonica rice germplasm at the booting stage. Euphytica 193, 369–382 (2013). https://doi.org/10.1007/s10681-013-0935-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-013-0935-x