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High congruency of QTL positions for heterosis of grain yield in three crosses of maize

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Abstract

The genetic basis of heterosis in maize has been investigated in a number of studies but results have not been conclusive. Here, we compare quantitative trait loci (QTL) mapping results for grain yield, grain moisture, and plant height from three populations derived from crosses of the heterotic pattern Iowa Stiff Stalk Synthetic × Lancaster Sure Crop, investigated with the Design III, and analyzed with advanced statistical methods specifically developed to examine the genetic basis of mid-parent heterosis (MPH). In two populations, QTL analyses were conducted with a joint fit of linear transformations Z 1 (trait mean across pairs of backcross progenies) and Z 2 (half the trait difference between pairs of backcross progenies) to estimate augmented additive and augmented dominance effects of each QTL, as well as their ratio. QTL results for the third population were obtained from the literature. For Z 2 of grain yield, congruency of QTL positions was high across populations, and a large proportion of the genetic variance (~70%) was accounted for by QTL. This was not the case for Z 1 or the other two traits. Further, almost all congruent grain yield QTL were located in the same or an adjacent bin encompassing the centromere. We conclude that different alleles have been fixed in each heterotic pool, which in combination with allele(s) from the opposite heterotic pool lead to high MPH for grain yield. Their positive interactions very likely form the base line for the superior performance of the heterotic pattern under study.

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References

  • Abler BSB, Edwards MD, Stuber CW (1991) Isoenzymatic identification of quantitative trait loci in crosses of elite maize hybrids. Crop Sci 31:267–274

    Article  CAS  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723

    Article  Google Scholar 

  • Austin DF, Lee M, Veldboom LR, Hallauer AR (2000) Genetic mapping in maize with hybrid progeny across testers and generations: grain yield and grain moisture. Crop Sci 40:30–39

    Google Scholar 

  • Baierl A, Bogdan M, Frommlet F, Futschik A (2006) On locating multiple interacting quantitative trait loci in intercross designs. Genetics 173:1693–1703

    Article  CAS  PubMed  Google Scholar 

  • Beavis WD, Smith OS, Grant D, Fincher R (1994) Identification of quantitative trait loci using a small sample of topcrossed and F4 progeny from maize. Crop Sci 34:882–896

    Article  Google Scholar 

  • Bingham ET (1998) Role of chromosome blocks in heterosis and estimates of dominance and overdominance. In: Lamkey KR, Staub JE (eds) Concepts and breeding of heterosis in crop plants. Crop Science Society of America, Madison, pp 71–87

    Google Scholar 

  • Bruce AB (1910) The Mendelian theory of heredity and the augmentation of vigor. Science 32:627–628

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2004) Multimodel interference: understanding AIC and BIC in model selection. Soc Methods Res 33:261–304

    Article  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  Google Scholar 

  • Cockerham CC, Zeng Z-B (1996) Design III with marker loci. Genetics 143:1437–1456

    CAS  PubMed  Google Scholar 

  • Comstock RE, Robinson HF (1952) Estimation of average dominance of genes. In: Gowen JW (ed) Heterosis. Iowa State College Press, Ames, pp 495–516

    Google Scholar 

  • Coors JG, Pandey S (eds) (1999) The genetics and exploitation of heterosis in crops. American Society of Agronomy, Madison

    Google Scholar 

  • Crow JF (1948) Alternative hypotheses of hybrid vigor. Genetics 33:477–487

    Google Scholar 

  • Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28:454–455

    Article  PubMed  CAS  Google Scholar 

  • Falke KC, Melchinger AE, Flachenecker C, Kusterer B, Frisch M (2006) Comparison of linkage maps from F2 and three times intermated generations in two populations of European flint maize (Zea mays L.). Theor Appl Genet 113:857–866

    Article  CAS  PubMed  Google Scholar 

  • Frascaroli E, Canè MA, Landi P, Pea G, Gianfranceschi L, Villa M, Morgante M, Pè ME (2007) Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics 176:625–644

    Article  CAS  PubMed  Google Scholar 

  • Frascaroli E, Canè MA, Pè ME, Pea G, Morgante M, Landi P (2009) QTL detection in maize testcross progenies as affected by related and unrelated testers. Theor Appl Genet 118:993–1004

    Article  PubMed  Google Scholar 

  • Frova C, Krajewski P, Di Fonzo N, Villa M, Sar-Gorla M (1999) Genetic analysis of drought tolerance in maize by molecular markers. I. Yield components. Theor Appl Genet 99:280–288

    Article  Google Scholar 

  • Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. PNAS 99:9573–9578

    CAS  PubMed  Google Scholar 

  • Garcia AAF, Wang S, Melchinger AE, Zeng Z-B (2008) Quantitative trait loci mapping and the genetic basis of heterosis in maize and rice. Genetics 180:1707–1724

    Article  PubMed  Google Scholar 

  • Graham GI, Wolfe DW, Stuber CW (1997) Characterization of a yield quantitative trait locus on chromosome five of maize by fine mapping. Crop Sci 37:1601–1610

    CAS  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  CAS  PubMed  Google Scholar 

  • Hallauer AR, Miranda JB (1981) Quantitative genetics in maize breeding. Iowa State University Press, Ames

    Google Scholar 

  • Hayes BJ, Goddard ME (2001) The distribution of the effects of genes affecting quantitative traits in livestock. Genet Sel Evol 33:209–229

    Article  CAS  PubMed  Google Scholar 

  • Holland JB (1998) EPISTACY: a SAS program for detecting two locus epistatic interactions using genetic marker information. J Hered 89:374–375

    Article  Google Scholar 

  • Hull FH (1945) Recurrent selection for specific combining ability in corn. J Am Soc Agron 37:134–145

    Google Scholar 

  • Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

    CAS  PubMed  Google Scholar 

  • Jiang C, Zeng Z-B (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140:1111–1127

    CAS  PubMed  Google Scholar 

  • Jinks JL, Jones RM (1958) Estimation of components of heterosis. Genetics 43:223–234

    CAS  PubMed  Google Scholar 

  • Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479

    CAS  PubMed  Google Scholar 

  • Kearsey MJ, Jinks JL (1968) A general method of detecting additive, dominance and epistatic variation for metrical traits. I. Theory. Heredity 23:403–409

    Article  CAS  PubMed  Google Scholar 

  • Knapp SJ, Bridges WC (1987) Confidence interval estimators for heritability for several mating and experimental designs. Theor Appl Genet 73:759–763

    Article  Google Scholar 

  • Kusterer B, Piepho H-P, Utz HF, Schön CC, Muminovic J, Meyer RC, Altman T, Melchinger AE (2007) Heterosis for biomass-related traits in Arabidopsis investigated by QTL analysis of the triple test cross design with recombinant inbred lines. Genetics 177:1839–1850

    Article  CAS  PubMed  Google Scholar 

  • LeDeaux JR, Graham GI, Stuber CW (2006) Stability of QTL involved in heterosis in maize when mapped under several stress conditions. Maydica 51:151–167

    Google Scholar 

  • Lu H, Romero-Severson J, Bernardo R (2003) Genetic basis of heterosis explored by simple sequence repeat markers in a random-mated maize population. Theor Appl Genet 107:494–502

    Article  CAS  PubMed  Google Scholar 

  • McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li HH et al (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740

    Article  CAS  PubMed  Google Scholar 

  • Melchinger AE, Utz HF, Schön CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149:383–403

    CAS  PubMed  Google Scholar 

  • Melchinger AE, Utz HF, Piepho H-P, Zeng Z-B, Schön CC (2007) The role of epistasis in the manifestation of heterosis: a system-oriented approach. Genetics 117:1815–1825

    Article  Google Scholar 

  • Melchinger AE, Utz HF, Schön CC (2008) Genetic expectations of quantitative trait loci main and interaction effects obtained with the triple testcross design and their relevance for the analysis of heterosis. Genetics 178:2265–2274

    Article  CAS  PubMed  Google Scholar 

  • Melchinger AE, Dhillon BS, Mi X (2010) Variation of the parental genome contribution in segregating populations derived from biparental crosses and its relationship with heterosis of their Design III progenies. Theor Appl Genet (this volume)

  • Mode CJ, Robinson HF (1959) Pleiotropism and the genetic variance and covariance. Biometrics 15:518–537

    Article  Google Scholar 

  • Powers L (1944) An expansion of Jones’ theory for the explanation of heterosis. Am Nat 78:275–280

    Article  Google Scholar 

  • Radoev M, Becker HC, Ecke W (2008) Genetic analysis of heterosis for yield and yield components in rapeseed (Brassica napus L.) by quantitative trait locus mapping. Genetics 179:1547–1558

    Article  CAS  PubMed  Google Scholar 

  • Reif JC, Kusterer B, Piepho H-P, Meyer RC, Altman T, Schön CC, Melchinger AE (2009) Unraveling epistasis with triple testcross progenies of near isogenic lines. Genetics 181:247–257

    Article  PubMed  Google Scholar 

  • Schön CC, Utz HF, Groh S, Truberg B, Openshaw S, Melchinger AE (2004) Quantitative trait locus mapping based on resampling in a vast maize testcross experiment and its relevance to quantitative genetics for complex traits. Genetics 167:485–498

    Article  PubMed  Google Scholar 

  • Searle SR (1971) Linear models. Wiley, New York

    Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Am Breed Assoc Rep 4:296–301

    Google Scholar 

  • Shull GH (1909) A pure-line method of corn breeding. Am Breed Assoc Rep 5:51–59

    Google Scholar 

  • Stuber CM, Lincoln SE, Wolfe DW, Helentjaris T, Lander ES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132:823–839

    CAS  PubMed  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. PNAS 103:6805–6810

    Article  CAS  PubMed  Google Scholar 

  • Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol Biol 48:697–712

    Article  CAS  PubMed  Google Scholar 

  • Utz HF, Melchinger AE (1996) PLABQTL: a program for composite interval mapping of QTL. J Agric Genomics 2:1–5

    Google Scholar 

  • Utz HF, Melchinger AE, Schön CC (2000) Bias and sampling error of the estimated proportion of genotypic variance explained by quantitative trait loci determined from experimental data in maize using cross validation and validation with independent samples. Genetics 154:1839–1849

    PubMed  Google Scholar 

  • Visscher PM (2008) Sizing up human height variation. Nat Genet 40:489–490

    Article  CAS  PubMed  Google Scholar 

  • Visscher PM, Thompson R, Haley CS (1996) Confidence intervals in QTL mapping by bootstrapping. Genetics 143:1013–1020

    CAS  PubMed  Google Scholar 

  • Williams W (1959) Heterosis and the genetics of complex characters. Nature 184:527–530

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zhu S, Rossnagel BG, Kaeppler HF (2004) Genetic analysis of quantitative trait loci for groat protein and oil content in oat. Crop Sci 44:254–260

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to R. Bernardo, C.W. Stuber, and Z.-B. Zeng for providing the raw data for Pop1 and Pop2 and to E. Frascaroli for providing heritability estimates for Pop3. We thank G. Haseneyer and D. Campell for their help with the linkage map comparisons, and an anonymous reviewer for suggestions. This research was financed by the Deutsche Forschungsgemeinschaft (DFG) within the priority program SPP 1149 “Heterosis in Plants” (Research Grant ME931/4-3).

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Authors and Affiliations

  1. Department of Plant Breeding, Center of Life and Food Sciences Weihenstephan, Technische Universität München, 85350, Freising, Germany

    Chris C. Schön

  2. Institute of Plant Breeding, Seed Science and Population Genetics, University of Hohenheim, 70599, Stuttgart, Germany

    Baldev S. Dhillon, H. Friedrich Utz & Albrecht E. Melchinger

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  1. Chris C. Schön
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  2. Baldev S. Dhillon
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  3. H. Friedrich Utz
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  4. Albrecht E. Melchinger
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Correspondence to Albrecht E. Melchinger.

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Communicated by H. Becker.

Contribution to the special issue “Heterosis in Plants”.

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Schön, C.C., Dhillon, B.S., Utz, H.F. et al. High congruency of QTL positions for heterosis of grain yield in three crosses of maize. Theor Appl Genet 120, 321–332 (2010). https://doi.org/10.1007/s00122-009-1209-9

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