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Detecting epistatic effects associated with cotton traits by a modified MDR approach

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Abstract

Genetic expression of a trait is complicated and it is usually associated with many genes including their interactions (epistasis) and genotype-by-environment interactions. Genetic mapping currently focuses primarily on additive models or marginal genetic effects due to the complexity of epistatic effects. Thus, there exists a need to appropriately identify favorable epistatic effects for important biological traits. Several multifactor dimensionality reduction (MDR) based methods are important resources to identify high-order gene–gene interactions. These methods are mainly focused on human genetic studies. Many traits in plant systems are not only quantitatively inherited but also are often measured in repeated field plots under multiple environments. In this study, we proposed a mixed model based MDR approach, which is suitable for inclusion of various fixed and random effects. This approach was used to analyze a cotton data set that included eight agronomic and fiber traits and 20 DNA markers. The results revealed high order epistatic effects were detected for most of these traits using this modified MDR approach.

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References

  • Broman KW (2001) Review of statistical methods for QTL mapping in experimental crosses. Lab Animal 30(7):44–52

    PubMed  CAS  Google Scholar 

  • Cao G, Zhu J, He C, Gao Y, Yan J, Wu P (2001) Impact of epistasis and QTL × environment interaction on the developmental behavior of plant height in rice (Oryza sativa L.). Theor Appl Genet 103:153–160

    Article  CAS  Google Scholar 

  • Culverhouse R, Klein T, Shannon W (2004) Detecting epistatic interactions contributing to quantitative traits. Genet Epidemiol 27:141–152

    Article  PubMed  Google Scholar 

  • Davison AC, Hinkley DV (1998) Bootstrap methods and their application. Cambridge University Press. New York, NY

  • Dudley JW (1993) Molecular markers in plant improvement: manipulation of genes affecting quantitative traits. Crop Sci 33:660–668

    Article  CAS  Google Scholar 

  • Foulkes AS (2009) Applied statistical genetics with R. Springer, New York, NY

  • Goldringer I, Brabant P, Gallais A (1997) Estimation of additive and epistatic genetic variances for agronomic traits in a population of doubled-haploid lines of wheat. Heredity 79:60–71

    Google Scholar 

  • Guo W, Zhang T, Shen X, Yu J, Kohel RJ (2003) Development of SCAR marker linked to a major QTL for high fiber strength and its usage in molecular-marker assisted selection in upland cotton. Crop Sci 43:2252–2256

    Article  CAS  Google Scholar 

  • Gutierrez OA, Basu S, Saha S, Jenkins JN, Shoemaker DB, Cheatham CL, McCarty JC (2002) Genetic distance among selected cotton genotypes and its relationship with F2 performance. Crop Sci 42:1841–1847

    Article  Google Scholar 

  • Hahn LW, Ritchie MD, Moore JH (2003) Multifactor dimensionality reduction software for detecting gene–gene and gene–environment interactions. Bioinformatics 19:376–382

    Article  PubMed  CAS  Google Scholar 

  • Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324

    Article  PubMed  CAS  Google Scholar 

  • Hartley HO, Rao JNK (1967) Maximum-likelihood estimation for the mixed analysis of variance model. Biometrika 54:93–108

    PubMed  CAS  Google Scholar 

  • He D, Lin Z, Zhang X, Nie Y, Guo X, Feng C, Stewart JM (2005) Mapping QTLs of traits contributing to yield and analysis of genetic effects in tetraploid cotton. Euphytica 144:141–149

    Article  CAS  Google Scholar 

  • Jansen RC (1992) A general mixture model for mapping quantitative trait loci by using molecular markers. Theor Appl Genet 85:252–260

    Article  CAS  Google Scholar 

  • Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135:205–211

    PubMed  CAS  Google Scholar 

  • Jiang C, Wright RJ, El-Zik KM, Paterson AH (1998) Polyploid formation created unique avenues for response to selection in Gossypium (cotton). Proc Natl Acad Sci USA 95:4419–4424

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Wright RJ, Woo SS, DelMonte TA, Paterson AH (2000) QTL analysis of leaf morphology in tetraploid Gossypium (cotton). Theor Appl Genet 100:409–418

    Article  CAS  Google Scholar 

  • Knapp SJ (1998) Marker-assisted selection as a strategy for increasing the probability of selecting superior genotypes. Crop Sci 38:1164–1174

    Article  Google Scholar 

  • Kohel RJ, Yu J, Park YH, Lazo GR (2001) Molecular mapping and characterization of traits controlling fiber quality in cotton. Euphytica 121:163–172

    Article  CAS  Google Scholar 

  • Lacape JM, Nguyen TB, Courtois B, Belot JL, Giband M, Gourlot JP, Gawryziak G, Roques S, Hau B (2005) QTL analysis of cotton fiber quality using multiple Gossypium hirsutum × Gossypium barbadense backcross generations. Crop Sci 45:123–140

    CAS  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, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lin Z, He D, Zhang X, Nie Y, Guo X, Feng C, Stewart JM (2005) Linkage map construction and mapping QTL for cotton fibre quality using SRAP, SSR and RAPD. Plant Breed 124:180–187

    Article  CAS  Google Scholar 

  • Liu P, Zhu J, Lou XY, Lu Y (2003) A method for marker-assisted selection based on QTLs with epistatic effects. Genetica 119:75–86

    Article  PubMed  CAS  Google Scholar 

  • Lou XY, Chen GB, Yan L, Ma JZ, Zhu J, Elston RC, Li MD (2007) A generalized combinatorial approach for detecting gene-by-gene and gene-by-environment interactions with application to nicotine dependence. Am J Human Genet 80:1125–1137

    Article  CAS  Google Scholar 

  • Lou XY, Chen GB, Yan L, Ma JZ, Mangold JE, Zhu J, Elston RC, Li MD (2008) A combinatorial approach to detecting gene–gene and gene–environment interactions in family studies. Am J Human Genet 83:457–467

    Article  CAS  Google Scholar 

  • Lü HY, Liu XF, Wei SP, Zhang YM (2011) Epistatic association mapping in homozygous crop cultivars. PLoS One 6(3):e17773

    Article  PubMed  Google Scholar 

  • Manly BFJ (2006) Randomization, bootstrap and Monte Carlo methods in biology, 3rd edn. Chapman and Hall/CRC, Boca Raton

    Google Scholar 

  • Martin ER, Ritchie MD, Hahn L, Kang S, Moore JH (2006) A novel method to identify gene-gene effects in nuclear families: the MDR-PDT. Genet Epidemiol 2:111–123

    Google Scholar 

  • Martin EZO, Curnow RN (1992) Estimation the locations and the sizes of the effects of quantitative trait loci using flanking markers. Theor Appl Genet 85:480–488

    Google Scholar 

  • McCarty JC, Jenkins JN, Parrott WL, Creech RG (1979) The conversion of photoperiodic primitive race stocks of cotton to day-neutral stocks. Miss Agric For Exp Stn Res Rep 4(19):4

    Google Scholar 

  • McCarty JC, Jenkins JN, Wu J (2004a) Primitive accession germplasm by cultivar crosses as sources for cotton improvement I: phenotypic values and variance components. Crop Sci 44:1226–1230

    Article  Google Scholar 

  • McCarty JC, Jenkins JN, Wu J (2004b) Primitive accession germplasm by cultivar crosses as sources for cotton improvement II: genetic effects and genotype values. Crop Sci 44:1231–1235

    Article  Google Scholar 

  • McCarty JC, Wu J, Jenkins JN (2008) Genetic associations of cotton yield with its component traits in derived primitive accessions crossed by elite upland cultivars using the conditional ADAA genetic model. Euphytica 161:337–352

    Article  CAS  Google Scholar 

  • Mei M, Syed NH, Gao W, Thaxton PM, Smith CW, Stelly DM, Chen Z (2004) Genetic mapping and QTL analysis of fiber-related traits in cotton (Gossypium). Theor Appl Genet 108:280–291

    Article  PubMed  CAS  Google Scholar 

  • Miller RG (1974) The jackknife: a review. Biometrika 61:1–15

    Google Scholar 

  • Moore JH, Gilbert JC, Tsai CT, Chiang FT, Holden T, Barney N, White BC (2006) A flexible computational framework for detecting, characterizing, and interpreting statistical patterns of epistasis in genetic studies of human disease susceptibility. J Theor Biol 241:252–261

    Article  PubMed  Google Scholar 

  • Nelson MR, Kardia SL, Ferrell RE, Sing CF (2001) A combinatorial partitioning method to identify multilocus genotypic partitions that predict quantitative trait variation. Genome Res 11:458–470

    Article  PubMed  CAS  Google Scholar 

  • Patterson HD, Thompson R (1971) Recovery of inter-block information when block size are unequal. Biometrika 58:545–554

    Article  Google Scholar 

  • Rao CR (1971) Estimation of variance and covariance components MINQUE theory. J Multivar Anal 1:257–275

    Article  Google Scholar 

  • Reinisch AJ, Dong J, Brubaker CL, Stelly DM, Wendel JF, Paterson AH (1994) A detailed RFLP map of cotton, Gossypium hirsutum × Gossypium barbadense: chromosome organization and evolution in a disomic polyploidy genome. Genetics 138:829–847

    PubMed  CAS  Google Scholar 

  • Ritchie MD, Hahn LW, Roodi N, Bailey LR, Dupont WD, Parl FF, Moore JH (2001) Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Human Genet 69:138–147

    Article  CAS  Google Scholar 

  • Saha S, Wu J, Jenkins JN, McCarty JC, Hayes RW, Stelly DM (2010) Genetic dissection of chromosome substitution lines of cotton to discover novel Gossypium barbadense L. alleles for improvement of agronomic traits. Theor Appl Genet 120:1193–1205

    Article  PubMed  Google Scholar 

  • Searle SR, Casella G, McCulloch CE (1992) Variance components. Wiley, New York

    Book  Google Scholar 

  • Shen S, Zhang T, Guo W, Zhu X, Zhang X (2006) Mapping fiber and yield QTLs with main, epistatic, and QTL × environment Interaction effects in recombinant inbred lines of upland cotton. Crop Sci 46:61–66

    Article  CAS  Google Scholar 

  • Stich B, Möhring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754

    Article  PubMed  Google Scholar 

  • Stromberg LD, Dudley JW, Rufener GK (1994) Comparing conventional early generation selection with molecular marker assisted selection in maize. Crop Sci 34:1221–1225

    Article  Google Scholar 

  • Swindle MG (1993) Performance of F2 hybrids in cotton from crosses of exotic germplasm and cultivars. M.S. thesis, Mississippi State University, Mississippi State, MS

  • Tang B, Jenkins JN, Watson CE, McCarty JC, G. Creech RG (1996) Evaluation of genetic variances, heritabilities, and correlations for yield and fiber traits among cotton F2 hybrid populations. Euphytica 91:315–322

  • Ulloa M, Saha S, Jenkins JN, Meredith WR, McCarty JC, Stelly DM (2005) Chromosomal assignment of RFLP linkage groups harboring important QTLs on an intraspecific cotton (Gossypium hirsutum L.) join map. J Hered 96:132–144

    Article  PubMed  CAS  Google Scholar 

  • Wang DL, Zhu J, Li ZK, Paterson AH (1999) Mapping QTLs with epistatic effects and QTL × environment interactions by mixed linear model approaches. Theor Appl Genet 99:1255–1264

    Article  Google Scholar 

  • Wu J, Jenkins JN, McCarty JC (2011) A Generalized approach and computer tool for quantitative genetics study. Proceedings of Applied Statistics in Agriculture April 25–27, 2010, Manhattan, KS, USA, pp 85–106

  • Wu J, Jenkins JC, McCarty JC, Wu D (2006) Variance component estimation using the ADAA model when genotypes vary across environments. Crop Sci 46:174–179

    Article  Google Scholar 

  • Wu J, Jenkins JN, McCarty JC, Zhong M, Swindle M (2007) AFLP marker associations with agronomic and fiber traits in cotton. Euphytica 153:153–163

    Article  CAS  Google Scholar 

  • Wu J, Jenkins JN, McCarty JC (2008) Testing variance components by two jackknife techniques. In: Proceedings of applied statistics in agriculture, Manhattan, pp 1–17

  • Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG, Zhang Q (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 ZC, Zhu J (1999) A new approach for predicting heterosis based on an additive, dominance and additive × additive model with environment interaction. J Hered 82:510–517

    Google Scholar 

  • Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536

    Article  PubMed  CAS  Google Scholar 

  • Yu J, 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. Nature Genetics 38:203–208

    Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

  • Zhang T, Yuan Y, Yu J, Guo W, Kohel RJ (2003) Molecular tagging of major QTL for fiber strength in Upland cotton and its marker-assisted selection. Theor Appl Genet 106:262–268

    PubMed  CAS  Google Scholar 

  • Zhang K, Tian J, Zhao L, Wang S (2008) Mapping QTLs with epistatic effects and QTL × environment interactions for plant height using a doubled haploid population in cultivated wheat. J Genetics Genomics 35:119–127

    Article  CAS  Google Scholar 

  • Zhong M (2001) Comparative analyses of backcrossed derived lines from exotic germplasm for day-neutral genes using AFLP markers. M.S. thesis, Mississippi State University, Mississippi State, MS

  • Zhong M, McCarty JC, Jenkins JN, Saha S (2002) Assessment of day-neutral backcross populations of cotton using AFLP markers. J Cotton Sci 6:97–103

    Google Scholar 

  • Zhu J (1989) Estimation of genetic variance components in the general mixed model. Ph.D. dissertation, North Carolina State University, Raleigh, NC

  • Zhu J (1993) Methods of predicting genotype value and heterosis for offspring of hybrids. J Biomath 8:32–44

    Google Scholar 

  • Zhu J, Weir BS (1994) Analysis of cytoplasmic and maternal effects: I. A genetic model for diploid plant seeds and animals. Theor Appl Genet 89:153–159

    Google Scholar 

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Wu, J., Jenkins, J.N., McCarty, J.C. et al. Detecting epistatic effects associated with cotton traits by a modified MDR approach. Euphytica 187, 289–301 (2012). https://doi.org/10.1007/s10681-012-0770-5

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  • DOI: https://doi.org/10.1007/s10681-012-0770-5

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