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Capturing pair-wise epistatic effects associated with three agronomic traits in barley

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Abstract

Genetic association mapping has been widely applied to determine genetic markers favorably associated with a trait of interest and provide information for marker-assisted selection. Many association mapping studies commonly focus on main effects due to intolerable computing intensity. This study aims to select several sets of DNA markers with potential epistasis to maximize genetic variations of some key agronomic traits in barley. By doing so, we integrated a MDR (multifactor dimensionality reduction) method with a forward variable selection approach. This integrated approach was used to determine single nucleotide polymorphism pairs with epistasis effects associated with three agronomic traits: heading date, plant height, and grain yield in barley from the barley Coordinated Agricultural Project. Our results showed that four, seven, and five SNP pairs accounted for 51.06, 45.66 and 40.42% for heading date, plant height, and grain yield, respectively with epistasis being considered, while corresponding contributions to these three traits were 45.32, 31.39, 31.31%, respectively without epistasis being included. The results suggested that epistasis model was more effective than non-epistasis model in this study and can be more preferred for other applications.

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References

  • Abeledo LG, Calderini DF, Slafer GA (2003) Genetic improvement of barley yield potential and its physiological determinants in Argentina (1944–1998). Euphytica 130:225–334

    Article  Google Scholar 

  • Akaike H (1969) Fitting autoregressive models for prediction. Ann Inst Stat Math 21:243–247

    Article  Google Scholar 

  • Alqudah AM et al (2014) Genetic dissection of photoperiod response based on GWAS of pre-anthesis phase duration in Spring Barley. Plos One 9(11):e113120

    Article  PubMed  PubMed Central  Google Scholar 

  • Breiman L (2001) Random Forests. Mach Learn 45(1):5–32

    Article  Google Scholar 

  • Bulman P, Mather DE, Smith DL (1993) Genetic improvement of spring barley cultivars grown in eastern Canada from 1910 to 1988. Euphytica 71:35–48

    Article  Google Scholar 

  • Casao MC et al (2011) Expression analysis of vernalization and day-length response genes in barley (Hordeum vulgare L.) indicates that VRNH2 is a repressor of PPDH2 (HvFT3) under long days. J Exp Bot 62(6):1939–1949

    Article  CAS  PubMed  Google Scholar 

  • Cockram J et al (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot 58(6):1231–1244

    Article  CAS  PubMed  Google Scholar 

  • Collins HM et al (2010) Variability in fine structures of noncellulosic cell wall polysaccharides from cereal grains: potential importance in human health and nutrition. Cereal Chem 87:272–282

    Article  CAS  Google Scholar 

  • Cuesta-Marcos A et al (2009) Yield QTL affected by heading date in Mediterranean grown barley. Plant Breed 128(1):46–53

    Article  CAS  Google Scholar 

  • Daoura BG et al (2014) Genetic effects of dwarfing gene Rht-5 on agronomic traits in common wheat (Triticum aestivum L.) and QTL analysis on its linked traits. Field Crops Res 156:22–29

    Article  Google Scholar 

  • Ellis RP et al (2000) Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 51(342):9–17

    Article  CAS  PubMed  Google Scholar 

  • Faure S et al (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176(1):599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein BA et al (2010) An application of Random Forests to a genome-wide association dataset: methodological considerations & new findings. BMC Genet 11:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Grausgruber H et al (2002) Genetic improvement of agronomic and qualitative traits of spring barley. Plant Breed 121:411–416

    Article  Google Scholar 

  • Hahn LW, Ritchie MD, Moore JH (2003) Multifactor dimensionality reduction software for detecting gene-gene and gene-environment interactions. Bioinformatics 19(3):376–382

    Article  CAS  PubMed  Google Scholar 

  • Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69(4):315–324

    Article  CAS  PubMed  Google Scholar 

  • Hastie T, Tibshirani R, Friedman JH (2001) The elements of statistical learning: data mining, inference, and prediction. Springer series in statistics. Springer, New York

    Book  Google Scholar 

  • Hemming MN et al (2008) Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147(1):355–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh YC et al (2012) Epistasis analysis for estrogen metabolic and signaling pathway genes on young ischemic stroke patients. PLoS One 7(10):e47773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006a) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88(3):360–371

    Article  CAS  PubMed  Google Scholar 

  • Jain M et al (2006b) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6(1):47–59

    Article  CAS  PubMed  Google Scholar 

  • Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135(1):205–211

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Jia QJ et al (2009) GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Funct Integr Genomics 9(2):255–262

    Article  CAS  PubMed  Google Scholar 

  • Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152(3):1203–1216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karsai I et al (2005) The Vrn-H2 locus is a major determinant of flowering time in a facultative x winter growth habit barley (Hordeum vulgare L.) mapping population. Theor Appl Genet 110(8):1458–1466

    Article  CAS  PubMed  Google Scholar 

  • Kawahara Y et al (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (N Y):6(1):4. http://rice.plantbiology.msu.edu/downloads_gad.shtml

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121(1):185–199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lark KG et al (1995) Interactions between quantitative trait loci in soybean in which trait variation at one locus is conditional upon a specific allele at another. Proc Natl Acad Sci USA 92(10):4656–4660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z et al (1997) Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145(2):453–465

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li JZ et al (2006) Analysis of QTLs for yield components, agronomic traits, and disease resistance in an advanced backcross population of spring barley. Genome 49(5):454–466

    Article  CAS  PubMed  Google Scholar 

  • Liang M et al (2012) Expression and functional analysis of NUCLEAR FACTOR-Y, subunit B genes in barley. Planta 235(4):779–791

    Article  CAS  PubMed  Google Scholar 

  • Lorenz AJ, Hamblin MT, Jannink JL (2010) Performance of single nucleotide polymorphisms versus haplotypes for genome-wide association analysis in Barley. Plos One:5(11):e140795

    Article  Google Scholar 

  • Lou XY et al (2007) A generalized combinatorial approach for detecting gene-by-gene and gene-by-environment interactions with application to nicotine dependence. Am J Hum Genet 80(6):1125–1137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lou XY et al (2008) A combinatorial approach to detecting gene-gene and gene-environment interactions in family studies. Am J Hum Genet 83(4):457–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu HY et al (2011) Epistatic association mapping in homozygous crop cultivars. PLoS One 6(3):e17773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malmberg RL et al (2005) Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171(4):2013–2027

    Article  CAS  PubMed  PubMed Central  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 

  • Martinez JHE, Foster AE (1998) Genetic analysis of heading date and other agronomic characters in barley (Hordeum vulgare L.). Euphytica 99(3):145–153

    Article  Google Scholar 

  • Maurer A et al (2015) Modelling the genetic architecture of flowering time control in barley through nested association mapping. Bmc Genomics 16:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer KF et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491(7426):711–716

    CAS  PubMed  Google Scholar 

  • McGee H (2004) On food and cooking: the science and lore of the kitchen. Scribner, New York

    Google Scholar 

  • Miller AJ (1984) Selection of subsets of regression variables. J R Stat Soc Ser A 147:389–425

    Article  Google Scholar 

  • Miller AJ (2002) Subset selection in regression. In: Isham V et al (ed) Monographs on statistics and applied probability, 2nd edn. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  • Monna L et al (2002) Positional cloning of rice semidwarfing gene, sd-1: Rice “Green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9(1):11–17

    Article  CAS  PubMed  Google Scholar 

  • Nelson MR et al (2001) A combinatorial partitioning method to identify multilocus genotypic partitions that predict quantitative trait variation. Genome Res 11(3):458–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasam RK et al (2012) Genome-wide association studies for agronomical traits in a world wide spring barley collection. Bmc Plant Biol 12:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng J et al (2002) Molecular and physiological characterization of arabidopsis GAI alleles obtained in targeted Ds-tagging experiments. Planta 214(4):591–596

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2010) A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Vienna. http://www.r-project.org (ISBN 3–900051-07-0)

  • Reif JC et al (2011) Association mapping for quality traits in soft winter wheat. Theor Appl Genet 122(5):961–970

    Article  PubMed  Google Scholar 

  • Ren XF et al (2016) SNP-based high density genetic map and mapping of btwd1 dwarfing gene in barley. Sci Rep 6:31741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie MD et al (2001) Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Hum Genet 69(1):138–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie MD, Hahn LW, Moore JH (2003) Power of multifactor dimensionality reduction for detecting gene-gene interactions in the presence of genotyping error, missing data, phenocopy, and genetic heterogeneity. Genet Epidemiol 24(2):150–157

    Article  PubMed  Google Scholar 

  • Sasaki A et al (2002) Green revolution: A mutant gibberellin-synthesis gene in rice - New insight into the rice variant that helped to avert famine over thirty years ago. Nature 416(6882):701–702

    Article  CAS  PubMed  Google Scholar 

  • Schulte D et al (2009) The international barley sequencing consortium–at the threshold of efficient access to the barley genome. Plant Physiol 149(1):142–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Shahinnia F et al (2006) QTL mapping of heading date and plant height in Barley cross “Azumamugi” × “Kanto Nakate Gold”. Iran J Biotechnol 4(2):88–94

    Google Scholar 

  • Shen X et al (2006) Mapping fiber and yield QTLs with main, epistatic, and QTL × environment interaction effects in recombinant inbred lines of upland cotton. Crop Sci 46(1):61–66

    Article  CAS  Google Scholar 

  • Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99(13):9043–9048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szucs P et al (2006) Positional relationships between photoperiod response QTL and photoreceptor and vernalization genes in barley. Theor Appl Genet 112(7):1277–1285

    Article  CAS  PubMed  Google Scholar 

  • Tavakol E et al (2016) Genetic dissection of heading date and yield under Mediterranean dry climate in barley (Hordeum vulgare L.). Euphytica 212(2):343–353

    Article  Google Scholar 

  • Tibshirani R (1996) Regression shrinkage and selection via the Lasso. J R Stat Soc Ser B Methodol 58(1):267–288

    Google Scholar 

  • Turner A et al (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310(5750):1031–1034

    Article  CAS  PubMed  Google Scholar 

  • von Korff M, Leon J, Pillen K (2010) Detection of epistatic interactions between exotic alleles introgressed from wild barley (H. vulgare ssp. spontaneum). Theor Appl Genet 121(8):1455–1464

    Article  Google Scholar 

  • Wang DL et al (1999) Mapping QTLs with epistatic effects and QTL × environment interactions by mixed linear model approaches. Theor Appl Genet 99:1255–1264

    Article  Google Scholar 

  • Wang JM et al (2014) A new QTL for plant height in Barley (Hordeum vulgare L.) showing no negative effects on grain yield. Plos One 9(2):e90144

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang JB et al (2016) QTL underlying some agronomic traits in barley detected by SNP markers. BMC Genetics 17:103

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber K et al (2001) An analysis of polygenes affecting wing shape on chromosome 2 in Drosophila melanogaster. Genetics 159(3):1045–1057

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J et al (2012) Detecting epistatic effects associated with cotton traits by a modified MDR approach. Euphytica 187:289–301

    Article  Google Scholar 

  • Xu S (2007) An empirical Bayes method for estimating epistatic effects of quantitative trait loci. Biometrics 63(2):513–521

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Jia Z (2007) Genomewide analysis of epistatic effects for quantitative traits in barley. Genetics 175(4):1955–1963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Wu J (2014a) linkim: Linkage information based genotype imputation method. https://cran.r-project.org/web/packages/linkim/index.html

  • Xu Y, Wu J (2014b) CateSelection: categorical variable selection methods: A multi-factor dimensionality reduction based forward selection method for genetic association mapping. https://cran.r-project.org/web/packages/CateSelection/index.html

  • Xu Y et al (2015) A linkage based imputation method for missing SNP markers in association mapping. J Appl Bioinform Comput Biol 4(1)

  • Yang J et al (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42(7):565–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J et al (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178(1):539–551

    Article  PubMed  PubMed Central  Google Scholar 

  • Zanke CD et al (2014) Whole genome association mapping of plant height in winter wheat (Triticum aestivum L.). PLoS One 9(11):e113287

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136(4):1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng ZB, Kao CH, Basten CJ (1999) Estimating the genetic architecture of quantitative traits. Genet Res 74(3):279–289

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Bonney G (2000) Use of classification trees for association studies. Genet Epidemiol 19(4):323–332

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author of this research paper wants to express our gratitude to those scientists who helped phenotype and genotypes these barley cultivars and prepare the data for public use. This study was partially supported by USDA-NIFA Hatch Project (1005459), South Dakota State University Research Scholarship Support Fund, and the Agricultural Experiment Station at South Dakota State University.

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Correspondence to Jixiang Wu.

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Xu, Y., Wu, Y. & Wu, J. Capturing pair-wise epistatic effects associated with three agronomic traits in barley. Genetica 146, 161–170 (2018). https://doi.org/10.1007/s10709-018-0008-0

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