Skip to main content
SpringerLink
Log in

Genetic basis of grain yield heterosis in an “immortalized F2” maize population

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Genetic basis of grain yield heterosis relies on the cumulative effects of dominance, overdominance, and epistasis in maize hybrid Yuyu22.

Abstract

Heterosis, i.e., when F1 hybrid phenotypes are superior to those of the parents, continues to play a critical role in boosting global grain yield. Notwithstanding our limited insight into the genetic and molecular basis of heterosis, it has been exploited extensively using different breeding approaches. In this study, we investigated the genetic underpinnings of grain yield and its components using “immortalized F2” and recombinant inbred line populations derived from the elite hybrid Yuyu22. A high-density linkage map consisting of 3,184 bins was used to assess (1) the additive and additive-by-additive effects determined using recombinant inbred lines; (2) the dominance and dominance-by-dominance effects from a mid-parent heterosis dataset; and (3) the various genetic effects in the “immortalized F2” population. Compared with a low-density simple sequence repeat map, the bin map identified more quantitative trait loci, with higher LOD scores and better accuracy of detecting quantitative trait loci. The bin map showed that, among all traits, dominance was more important to heterosis than other genetic effects. The importance of overdominance/pseudo-overdominance was proportional to the amount of heterosis. In addition, epistasis contributed to heterosis as well. Phenotypic variances explained by the QTLs detected were close to the broad-sense heritabilities of the observed traits. Comparison of the analyzed results obtained for the “immortalized F2” population with those for the mid-parent heterosis dataset indicated identical genetic modes of action for mid-parent heterosis and grain yield performance of the hybrid.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Chen W, Zhang Y, Liu X, Chen B, Tu J, Fu T (2007) Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F2 populations. Theor Appl Genet 115:849–858

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Comstock RE, Robinson HF (1948) The components of genetic variance in populations. Biometrics 4:254–266

    Article  PubMed  CAS  Google Scholar 

  • Comstock RE, Robinson HF (1952) Estimation of average dominance of genes. In: Gowen JW (ed) Heterosis. ISU Press, Ames, pp 494–516

    Google Scholar 

  • Coors JG, Pandey S (1999) Genetics and exploitation of heterosis in crops. ASA, CSSA, SSSA, Madison

    Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Crow JF, Coors JG, Pandey S (1952) Heterosis. In: Gowen JW (ed) Dominance and overdominance. Iowa State College Press, Ames, pp 282–297

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Duvick DN (1999) The genetics and exploitation of heterosis in crops. In: Coors JG, Pandey S (eds) Crop Science Society of America, Madison, pp 19–29

  • East E (1908) Inbreeding in corn in Reports of the Connecticut Agricultural Experiment Station for Years 1907–1908. Connecticut Agricultural Experiment Station, New Haven, pp 419–428

    Google Scholar 

  • Falconer DS (1981) Introduction to quantitative genetics, 2nd edn. Longman, London

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Essex

    Google Scholar 

  • Ganal M, Durstewitz G, Polley A, Berard A, Buckler ES, Charcosset A, Clarke JD, Graner E, Hansen M, Joets J et al (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping and genetic mapping to compare with the B73 reference genome. PLoS ONE 6:e28334

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gardner CO, Lonquist JH (1959) Linkage and the degree of dominance of genes controlling quantitative characters in maize. Agron J 51:524–528

    Article  Google Scholar 

  • Goff SA, Zhang Q (2013) Heterosis in elite hybrid rice: speculation on the genetic and biochemical mechanisms. Curr Opin Plant Biol 16:221–227

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guo M, Rupe MA, Dieter JA, Zou JJ, Spielbauer D, Duncan KE, Howard RJ, Hou ZL, Simmons CR (2010) Cell Number Regulator 1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22:1057–1073

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guo T, Li H, Yan J, Tang J, Li J, Zhang Z, Zhang L, Wang J (2012) Performance prediction of F1 hybrids between recombinant inbred lines derived from two elite maize inbred lines. Theor Appl Genet 126:189–201

    Article  PubMed  Google Scholar 

  • Hallauer AR, Russell WA, Lamkey KR (1988) Corn breeding. In: Sprague GF, Dudley JW (eds) Corn and corn improvement, 3rd edn. ASA, CSSA, and SSSA, Madison, pp 469–564

    Google Scholar 

  • Hase T, Kimata Y, Matsumura T, Sakakibara H (1991) Molecular cloning and differential expression of the maize ferredoxin family. Plant Physiol 96:77–83

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho HP, Hochholdinger F (2008) Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organspecific patterns of nonadditive gene expression and conserved expression trends. Genetics 179:1275–1283

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hua J, Xing Y, Xu C, Sun X, Yu S, Zhang Q (2002) Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. Genetics 162:1885–1895

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hua J, Xing Y, Wu W, Xu C, Sun X et al (2003) Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 100:2574–2579

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Larièpe A, Mangin B, Jasson S, Combes V, Dumas F et al (2012) The genetic basis of heterosis: multiparental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). Genetics 190:795–811

    Article  PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li Z, Pinson SRM, Paterson AH, Park WD, Stansel JW (1997b) Genetics of hybrid sterility and hybrid breakdown in an inter-subspecific rice (Oryza sativa L.) population. Genetics 145:1139–1148

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    Article  PubMed  CAS  Google Scholar 

  • Liu R, Wang B, Guo W, Wang L, Zhang T (2011) Differential gene expression and associated QTL mapping for cotton yield based on a cDNA-AFLP transcriptome map in an immortalized F2. Theor Appl Genet 123:439–454

    Article  PubMed  CAS  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ (1989) Transcription, organization, and sequence of an auxin regulated gene cluster in soybean. Plant Cell 1:229–239

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Melchinger AE, Utz HF, Piepho HP, Zeng Z, Schön CC (2007) The role of epistasis in the manifestation of heterosis: a systems-oriented approach. Genetics 177:1815–1825

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Minvielle F (1987) Dominance is not necessary for heterosis: a two-locus model. Genet Res 49:245–247

    Article  Google Scholar 

  • Moll RH, Lindsey MF, Robinson HF (1964) Estimates of genetic variances and level of dominance in maize. Genetics 49:411–423

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pan Q, Ali F, Yang X, Li J, Yan J (2012) Exploring the genetic characteristics of two recombinant inbred line populations via high-density SNP markers in maize. PLoS ONE 7(12):e52777

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Paschold A, Jia Y, Marcon C, Lund S, Larson NB et al (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 22:2445–2454

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rahman A, Wong KS, Jane JL, Myers AM, James MG (1998) Characterization of SU1 isoamylase, a determinant of storage starch structure in maize. Plant Physiol 117:425–435

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Richey FD (1942) Mock-dominance and hybrid vigor. Science 96:280

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Springer NM (2013) Progress toward understanding heterosis in crop plants. Ann Rev Plant Biol 64:71–88

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Stuber CW (1994) Heterosis in plant breeding. Plant Breed Rev 12:227–251

    Google Scholar 

  • Stuber CW, Lincoln SE, Wolff 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM (2008) Gene expression analysis in maize hybrids and hybrids with varying levels of heterosis. BMC Plant Biol 8:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Swanson-Wagner RA, Jia Y, Decook R, Borsuk LA, Nettleton D et al (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. Proc Natl Acad Sci USA 103:6805–6810

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takatsuji H (1998) Zinc–finger transcription factors in plants. Cell Mol Life Sci 54:582–596

    Article  PubMed  CAS  Google Scholar 

  • Tang J, Yan J, Ma X, Teng W, Wu W et al (2010) Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theor Appl Genet 120:333–340

    Article  PubMed  Google Scholar 

  • Wang J, van Ginkel M, Podlich D, Ye G, Trethowan R, Pfeiffer W, De Lacy IH, Cooper M, Rajaram S (2003) Comparison of two breeding strategies by computer simulation. Crop Sci 43:1764–1773

    Article  Google Scholar 

  • Wang J, van Ginkel M, Trethowan R, Ye G, Delacy I, Podlich D, Cooper M (2004) Simulating the effects of dominance and epistasis on selection response in the CIMMYT Wheat Breeding Program using QuCim. Crop Sci 44:2006–2018

    Article  Google Scholar 

  • Wei G, Tao Y, Liu GZ, Chen C, Luo RY, Xia HA, Gan Q, Zeng HP, Lu ZK, Han YN et al (2009) A transcriptomic analysis of super hybrid rice LYP9 and its parents. Proc Natl Acad Sci USA 106:7695–7701

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Xie W, Feng Q, Yu H, Huang X, Zhao Q et al (2010) Parent-independent genotyping for constructing an ultra high-density linkage map based on population sequencing. Proc Natl Acad Sci USA 107:10578–10583

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61:421–442

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Tang H, Huang Y, Zheng Y, Li J (2006) QTL mapping and epistatic analysis for yield and yield components using molecular markers with an elite maize hybrid. Euphytica 149:121–131

    Article  CAS  Google Scholar 

  • Yan J, Yang X, Shah T, Sanchez-Villeda H, Li J, Warburton M, Zhou Y, Crouch JH, Xu Y (2010) High-throughput SNP genotyping with the GoldenGate assay in maize. Mol Breed 25:441–451

    Article  CAS  Google Scholar 

  • Yu SB, Li JX, Xu CG, Tan YF, Gao YJ et al (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  PubMed Central  Google Scholar 

  • Zhang L, Li H, Li Z, Wang J (2008) Interactions between markers can be caused by the dominance effect of QTL. Genetics 180:1177–1190

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou G, Chen Y, Yao W, Zhang C, Xie W, Hua J, Xing Y, Xiao J, Zhang Q (2012) Genetic composition of yield heterosis in an elite rice hybrid Proc. Proc Natl Acad Sci USA 109:15847–15852

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors gratefully thank the editor Dr. Thomas Lubberstedt and two anonymous reviewers for their valuable suggestions. This research was supported by the National Hi-Tech Research and Development Program of China (2012AA10A307) and the National Basic Research Program of China.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. National Maize Improvement Center, China Agricultural University, Beijing, 100193, China

    Tingting Guo, Xiaohong Yang & Jiansheng Li

  2. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Ning Yang, Hao Tong, Qingchun Pan & Jianbing Yan

  3. Institute of Crop Science, The National Key Facility for Crop Gene Resources and Genetic Improvement, and CIMMYT China, Chinese Academy of Agricultural Sciences, No. 12 Zhongguancun South Street, Beijing, 100081, China

    Tingting Guo & Jiankang Wang

  4. College of Agronomy, Henan Agricultural University, Zhengzhou, 450002, China

    Jihua Tang

Authors
  1. Tingting Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hao Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qingchun Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaohong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jihua Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jiankang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiansheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jianbing Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jianbing Yan.

Additional information

Communicated by Thomas Lubberstedt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 7828 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, T., Yang, N., Tong, H. et al. Genetic basis of grain yield heterosis in an “immortalized F2” maize population. Theor Appl Genet 127, 2149–2158 (2014). https://doi.org/10.1007/s00122-014-2368-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-014-2368-x

Keywords

Search

Navigation