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Epistasis and complementary gene action adequately account for the genetic bases of transgressive segregation of kilo-grain weight in rice

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Abstract

Transgressive segregation is a common phenomenon in plant species. In this study, transgressive segregation for kilo-grain weight (KGW) was observed in a recombinant inbred line (RIL) population derived from the cross between an indica variety, Teqing, and a wide compatible japonica variety, 02428, in three environments. A genetic linkage map with 154 single sequence repeat markers (SSR) was developed. Effects on KGW of quantitative trait loci (QTLs), digenetic epistasis, and their environmental interaction (QE) were determined using a mixed linear model approach. 13 QTLs with additive effects and 8 digenetic interactions involving 16 loci were identified. Eight QTLs were involved in interactions. Two QTLs and one epistasis showed QE. 30.0 and 14.0% of variation was explained by the additive effects and epistasis, respectively, which were much greater than the 4.4% of variation explained by QE. According to the model used, predicted KGW values of extreme phenotypes in the RIL population were very close to their observed values. This indicated that complementary action of additive QTLs and epistasis can adequately account for the important genetic bases of transgressive segregation for KGW in the rice RIL population.

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References

  • Albertson RC, Kocher TD (2005) Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution 59:686–690

    Article  PubMed  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Bell MA, Travis MP (2005) Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends Ecol Evol 20:358–361

    Article  PubMed  Google Scholar 

  • Bikard D, Patel D, Metté CL, Giorgi V, Camilleri C, Bennett MJ, Loudet O (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323:623–626

    Article  PubMed  CAS  Google Scholar 

  • Brem RB, Kruglyak L (2005) The landscape of genetic complexity across 5, 700 gene expression traits in yeast. Proc Natl Acad Sci USA 102:1572–1577

    Article  PubMed  CAS  Google Scholar 

  • Brondani C, Rangel PNN, Brondanil RPV, Ferreira ME (2002) QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice (Oryza sativa) using microsatellite markers. Theor Appl Genet 104:1192–1203

    Article  PubMed  CAS  Google Scholar 

  • Devicente MC, Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596

    PubMed  CAS  Google Scholar 

  • Engels WR (1983) The P family of transposable elements in Drosophila. Annu Rev Genet 17:315–344

    Article  PubMed  CAS  Google Scholar 

  • Ge XJ, Xing YZ, Xu CG, He YQ (2005) QTL analysis of cooked rice grain elongation, volume expansion, and water absorption using a recombinant inbred population. Plant Breeding 124:121–126

    Article  CAS  Google Scholar 

  • Grant V (1975) Genetics of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Hagiwara WE, Onishi K, Takamure I, Sano Y (2006) Transgressive segregation due to linked QTLs for grain characteristics of rice. Euphytica 150:27–35

    Article  CAS  Google Scholar 

  • Haq TU, Aakhtarl J, Gorham J, Steele KA, Khalid M (2008) Genetic mapping of QTLs, controlling shoot fresh and dry weight under salt stress in rice (Oryza sativa L.) cross between Co39 × Moroberekan. Pak J Bot 40:2369–2381

    CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Jiang WZ, Chu SH, Piao RH, Chin JH, Jin YM, Lee JH, Qiao YL, Han LZ, Piao ZZ, Koh HJ (2008) Fine mapping and candidate gene analysis of hwh1 and hwh2, a set of complementary genes controlling hybrid breakdown in rice. Theor Appl Genet 116:1117–1127

    Article  PubMed  CAS  Google Scholar 

  • Kim SC, Rieseberg LH (1999) Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153:965–977

    PubMed  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175

    Article  Google Scholar 

  • Lande R, Thompson R (1990) Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743–756

    PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Li ZK, Pinson SRM, Stansel JW, Park WD (1995) Identification of quantitative trait loci (QTLs) for heading date and plant height in cultivated rice (Oryza sativa L.). Theor Appl Genet 91:374–381

    CAS  Google Scholar 

  • Li ZK, Pinso SRM, Park WD, Paterson AH, Stansel JW (1997) Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145:453–465

    PubMed  CAS  Google Scholar 

  • Li ZK, Yu SB, Lafitte HR, Huang N, Courtois B, Hittalmani S, Vijayakumar CHMl, Liu GF, Wang GC, Shashidhar HE, Zhuang JY, Zheng KL, Singh VP, Sidhu JS, Srivantaneeyakul S, Khush GS (2003) QTL × environment interactions in rice. I. Heading date and plant height. Theor Appl Genet 108:141–153

    Article  PubMed  CAS  Google Scholar 

  • Liu GF, Zhang ZM, Zhu HT, Zhao FM, Ding XH, Zeng RZ, Li WT, Zhang GQ (2008) Detection of QTLs with additive effects and additive-by-environment interaction effects on panicle number in rice (Oryza Sativa L.) with single-segment substitution lines. Theor Appl Genet 116:923–931

    Article  PubMed  CAS  Google Scholar 

  • Loudet FO, Chaillou S, Camilleri C, Bouchez D, Daniel-Vedele F (2002) Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor Appl Genet 104:1173–1184

    Article  PubMed  CAS  Google Scholar 

  • Lu CF, Shen LH, Tan ZB, Xu YB, He P, Chen Y, Zhu LH (1997) Comparative mapping of QTLs for agronomic traits of rice across environments by using a doubled-haploid population. Theor Appl Genet 94:145–150

    Article  PubMed  CAS  Google Scholar 

  • Matsubara K, Kono I, Hori K, Nonoue Y, Ono N, Shomura A, Mizubayashi T, Yamamoto S, Yamanouchi U, Shirasawa K, Nishio T, Yano M (2008) Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars. Theor Appl Genet 117:935–945

    Article  PubMed  CAS  Google Scholar 

  • McCouch SR, Teytelman L, Xu YB, Lobos KB, Clare K, Walto MN, Fu BY, Maghirang R, Li ZK, Xing YZ, Zhang QF, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207

    Article  PubMed  CAS  Google Scholar 

  • Monforte AJ, Asins MJ, Carbonell EA (1997) Salt tolerance in Lycopersicon species V. Does genetic variability at quantitative trait loci affect their analysis? Theor Appl Genet 95:284–293

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  PubMed  CAS  Google Scholar 

  • Ni JJ, Wu P, Senadhira D, Huang N (1998) Mapping QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:1361–1369

    Article  CAS  Google Scholar 

  • Rabiei BM, Valizadeh M, Ghareyazie B, Moghaddam M (2004) Evaluation of selection indices for improving rice grain shape. Field Crops Res 8:359–367

    Article  Google Scholar 

  • Redona ED, Mackill DJ (1996a) Molecular mapping of quantitative trait loci in japonica rice. Genome 39:395–403

    Article  PubMed  CAS  Google Scholar 

  • Redona ED, Mackill DJ (1996b) Mapping quantitative trait loci for seedling vigor in rice using RFLPs. Theor Appl Genet 92:395–402

    Article  CAS  Google Scholar 

  • Ribaut JM, Hoisington D (1998) Marker-assisted selection: new tools and strategies. Trends Plant Sci 3:236–239

    Article  Google Scholar 

  • Rick CM, Smith PG (1953) Novel variation in tomato species hybrids. Am Nat 87:359–375

    Article  Google Scholar 

  • Rieseberg LH, Ellstrand NC (1993) What can morphological and molecular markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241

    CAS  Google Scholar 

  • Rieseberg LH, Arche MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372

    Article  PubMed  Google Scholar 

  • Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy J, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1121–1126

    Article  Google Scholar 

  • Shomura A, Izawa T, Ebana K, Ebitani T, Kanegae H, Konishi S, Yano M (2008) Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 40:1023–1028

    Article  PubMed  CAS  Google Scholar 

  • Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630

    Article  PubMed  CAS  Google Scholar 

  • Temnykh S, Park WD, Ayres N, Cartinhour S, Hauck N, Lipovich L, Cho YG, Ishii T, McCouch SR (2000) Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor Appl Genet 100:697–712

    Article  CAS  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch SR (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    Article  PubMed  CAS  Google Scholar 

  • Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493

    Article  PubMed  CAS  Google Scholar 

  • Wan XY, Weng JF, Zhai HQ, Wang JK, Lei CL, Liu XL, Guo T, Jiang L, Su N, Wan JM (2008) Quantitative trait loci (QTL) analysis for rice grain width and fine mapping of an identified QTL allele gw-5 in a recombination hotspot region on chromosome 5. Genetics 179:2239–2252

    Article  PubMed  CAS  Google Scholar 

  • Wang DL, Zhu J, Li ZK, Paterson AH (1999) User manual for QTLMapper version 1.0—a computer software for mapping quantitative trait loci (QTLs) with main effects, epistatic effects and QTL × environment interactions. http://ibi.zju.edu.cn/software/qtlmapper/QTLMaperManual.PDF

  • Wang CL, Ulloa M, Roberts PA (2008) A transgressive segregation factor (RKN2) in Gossypium barbadense for nematode resistance clusters with gene rkn1 in G. hirsutum. Mol Genet Genomics 279:41–52

    Article  PubMed  CAS  Google Scholar 

  • Weng JF, Gu SH, Wan XY, Gao H, Guo T, Su N, Lei CL, Zhang X, Cheng ZJ, Guo XP, Wang JL, Jiang L, Zhai HQ, Wan JM (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209

    Article  PubMed  CAS  Google Scholar 

  • Winn JA, Mason RE, Robbins AL, Rooney WL, Hay DB (2009) QTL mapping of a high protein digestibility trait in Sorghum bicolor. Int J Plant Genomics 2009, 471853:6. doi:10.1155/2009/47185

  • Wu KS, Tanksley SD (1993) Abundance, polymorphism and genetic mapping of microsatellites in rice. Mol Gen Genet 241:225–235

    Article  PubMed  CAS  Google Scholar 

  • Xiao JH, Li JM, Yuan LP, Tanksley SD (1996) Identification of QTLs affecting traits of agronomic importance in a recombinant inbred population derived from a subspecific rice cross. Theor Appl Genet 92:230–244

    Article  CAS  Google Scholar 

  • Xiao JH, Li JM, Grandillo S, Ahn SN, Yuan LP, Tanksley SD, McCoucha SR (1998) Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. Genetics 150:899–909

    PubMed  CAS  Google Scholar 

  • Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG, Zhang QF (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice. Theor Appl Genet 105:248–257

    Article  PubMed  CAS  Google Scholar 

  • Xu YB, Crouch JH (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48:391–407

    Article  Google Scholar 

  • Xu YB, McCouch SR, Shen ZT (1998) Transgressive segregation of tiller angle in rice caused by complementary gene action. Crop Sci 38:12–19

    Article  Google Scholar 

  • Xue Y, Jiang L, Su N, Wang JK, Deng P, Ma JF, Zhai HQ, Wan JM (1997) The genetic basic and Wne-mapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta 227:255–262

    Article  Google Scholar 

  • Yamamoto E, Takashi T, Morinaka Y, Lin SY, Kitano H, Matsuoka M, Ashikari M (2007) Interaction of two recessive genes, hbd2 and hbd3, induces hybrid breakdown in rice. Theor Appl Genet 115:187–194

    Article  PubMed  CAS  Google Scholar 

  • Young ND (1996) QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopath 34:479–501

    Article  CAS  Google Scholar 

  • Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang QF, Saghai Maroof MA (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported in part by Grants from the National Program on the Development of Basic Research (2007CB109001) and the National Natural Science Foundation of China (30971749, 30830064).

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  1. National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, 430070, China

    Donghai Mao, Touming Liu, Caiguo Xu, Xianghua Li & Yongzhong Xing

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  1. Donghai Mao
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  2. Touming Liu
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Correspondence to Yongzhong Xing.

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Mao, D., Liu, T., Xu, C. et al. Epistasis and complementary gene action adequately account for the genetic bases of transgressive segregation of kilo-grain weight in rice. Euphytica 180, 261–271 (2011). https://doi.org/10.1007/s10681-011-0395-0

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