Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis


Heterosis, or hybrid vigor, has been widely exploited in plant breeding for many decades, but the molecular mechanisms underlying the phenomenon remain unknown. In this study, we applied genome-wide transcript profiling to gain a global picture of the ways in which a large proportion of genes are expressed in the immature ear tissues of a series of 16 maize hybrids that vary in their degree of heterosis. Key observations include: (1) the proportion of allelic additively expressed genes is positively associated with hybrid yield and heterosis; (2) the proportion of genes that exhibit a bias towards the expression level of the paternal parent is negatively correlated with hybrid yield and heterosis; and (3) there is no correlation between the over- or under-expression of specific genes in maize hybrids with either yield or heterosis. The relationship of the expression patterns with hybrid performance is substantiated by analysis of a genetically improved modern hybrid (Pioneer® hybrid 3394) versus a less improved older hybrid (Pioneer® hybrid 3306) grown at different levels of plant density stress. The proportion of allelic additively expressed genes is positively associated with the modern high yielding hybrid, heterosis and high yielding environments, whereas the converse is true for the paternally biased gene expression. The dynamic changes of gene expression in hybrids responding to genotype and environment may result from differential regulation of the two parental alleles. Our findings suggest that differential allele regulation may play an important role in hybrid yield or heterosis, and provide a new insight to the molecular understanding of the underlying mechanisms of heterosis.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6


  1. Auger DL, Gray AD, Ream TS, Kato A, Coe EH Jr, Birchler JA (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169:389–9397

  2. Bao J, Le S, Chen C, Zhang X, Zhang Y, Liu S, Clark T, Wang J, Cao M, Yang H, Wang S, Yu J (2005) Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol 138:1216–1231

  3. Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register JC III, Tingey S, Rafalski A (2002) Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547

  4. Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. The Plant Cell 15:2236–2239

  5. Birchler JA, Riddle NC, Auger DL, Veitia RA (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226

  6. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. The Plant Cell 17:343–360

  7. Bruce W, Desbons P, Crasta O, Folkerts O (2001) Gene expression profiling of two related maize inbred lines with contrasting root-lodging traits. J Exp Bot 52:459–468

  8. Bruce W, Folkerts O, Garnaat C, Crasta O, Roth B, Bowen B (2000) Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. The Plant Cell 12:65–80

  9. Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Raflaski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize lines. BMC Genet 3:19

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

  11. Cong B, Liu J, Tanksley SD (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc Natl Acad Sci 99:13606–13611

  12. Cowles CR, Hirschhorn JN, Altshuler D, Lander ES (2002) Detection of regulatory variation in mouse genes. Nat Genet 32:432–437

  13. Crasta OR, Folkerts O (2003) Open architecture expression profiling of plant transcriptomes and gene discovery using GeneCalling® technology. In: Grotewold E (ed) Plant functional genomics: methods and protocols. Humana, Totawa, NJ, pp 381–394

  14. Doebley J (2004) The genetics of maize evolution. Ann Rev Genet 38:37–59

  15. Doss S, Schadt EE, Drake TA, Lusis AJ (2005) cis-acting expression quantitative trait loci in mice. Genome Res 15:681–691

  16. Duvick DN (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat Genet Rev 2:69–74

  17. Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). In: Sparks DN (ed) Adv Agron, Vol. 86. Academic, San Diego, pp 83–145

  18. Duvick DN, Smith JSC, Cooper M (2004) Long-term selection in a commercial hybrid maize breeding program. In: Janick J (ed) Plant breeding reviews, Vol. 24, part 2. Long term selection: crops, animals, and bacteria. Wiley, New York, pp 109–151

  19. Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, Giavalisco P, Nieselt-Struwe K, Muchmore E, Varki A, Ravid R, Doxiadis G, Bontrop R, Pääbo S (2002) Intra- and interspecific variation in primate gene expression patterns. Science 296:340–343

  20. Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci 99:9573–9578

  21. Gall T, Darlu LP, Escobar-Páramo P, Picard B, Denamur E (2005) Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species. Genome Res 15:260–268

  22. Gardner CO, Harvey PH, Comstock RE, Robinson HF (1953) Dominance of genes controlling quantitative characters in maize. Agron J 45:186–191

  23. Gibson G, Weir B (2005) The quantitative genetics of transcription. Trends Genet 21:616–623

  24. Gibson G, Riley-Berger R, Harshman L, Kopp A, Vacha S, Nuzhdin S, Wayne M (2004) Extensive sex-specific non-additivity of gene expression in Drosophila melanogaster. Genetics 167:1791–1799

  25. Guo M, Birchler JA (1994) Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science 266:1999–2002

  26. Guo M, Rupe MA, Danilevskaya ON, Yang X, Hu Z (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. The Plant J 36:30–44

  27. Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. The Plant Cell 16:1707–1716

  28. Horton P (2000) Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. J Exp Bot 51:475–485

  29. Janick J (1999) Exploitation of heterosis: uniformity and stability. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops (American Society of Agronomy, Inc. Crop Science Society of America, Inc.) Madison, pp 319–333

  30. Knight JC (2004) Allele-specific gene expression uncovered. Trends Genet 20:113–116

  31. Kollipara KP, Saab IN, Wych RD, Lauer MJ, Singletary GW (2002) Expression profiling of reciprocal maize hybrids divergent for cold germination and desiccation tolerance. Plant Physiol 129:974–992

  32. Labate JA, Lamkey KR, Lee M, Woodman WW (1997) Molecular genetic diversity after reciprocal recurrent selection in BSSS and BCCB1 maize populations. Crop Sci 37:416–423

  33. Leonardi A, Damerval C, Herbert Y, Gallais A, de Vienne D (1991) Association of protein amount polymorphism (PAP) among maize lines with performances of their hybrids. Theor Appl Genet 82:552–560

  34. Ogura A, Ikeo K, Gojobori T (2004) Comparative analysis of gene expression for convergent evolution of camera eye between octopus and human. Genome Res 14:1555–1561

  35. Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197

  36. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL (2003) Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742–1745

  37. Romagnoli S, Maddaloni M, Livini C, Motto M (1990) Relationship between gene expression and hybrid vigor in primary root tips of young maize (Zea mays L) plantlets. Theor Appl Genet 80:767–775

  38. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, Colinayo V, Ruff TG, Milligan SB, Cavet G, Linsley PS, Mao M, Stoughton RB, Friend SH (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422:297–302

  39. Shimkets RA, Lowe DG, Tai JT, Sehl P, Jin H, Yang R, Predki PF, Rothberg BEG, Murtha MT, Roth ME, Shenoy SG, Windemuth A, Simpson JW, Simons JF, Daley MP, Gold SA, McKenna MP, Hillan K, Went GT, Rothberg JM (1999) Gene expression analysis by transcript profiling coupled to a gene database query. Nat Biotech 17:798–803

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

  41. Smith OS, Smith JSC (1992) Measurement of genetic diversity among maize hybrids; a comparison of isozymic, RFLP, pedigree, and heterosis data. Maydica 37:53–60

  42. Smith OS, Smith JSC, Bowen SL, Tenborg RA, Wall SJ (1990) Similarities among a group of elite maize inbreds as measured by pedigree, F1 grain yield, heterosis, and RFLPs. Theor Appl Genet 80:833–840

  43. Song RT, Messing J (2003) Gene expression of a gene family in maize based on non-collinear haplotypes. Proc Natl Acad Sci 100:9055–9060

  44. 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

  45. Szalma SJ, Buckler ES IV, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110:1324–1333

  46. Tsaftaris AS (1995) Molecular aspects of heterosis in plants. Physiol Plant 94:362–370

  47. Tsaftaris AS, Kafka M, Polidoros A, Tani E (1999) Epigenetic changes in Maize DNA and Heterosis. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. (American Society of Agronomy, Inc. Crop Science Society of America, Inc.) Madison, pp 195–203

  48. Vuylsteke M, van Eeuwijk F, van Hummelen P, Kuiper M, Zabeau M (2005) Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 171:1267–1275

  49. Wittkopp P, Belinda J, Haerum K, Andrew GC (2004) Evolutionary changes in cis and trans gene regulation. Nature 430:85–88

  50. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW (2002) Allelic variation in human gene expression. Science 297:1143

  51. Yvert G, Brem RB, Whittle J, Akey JM, Foss E, Smith FN, Mackelprang R, Kruglyak L (2003) Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet 35:57–64

Download references


We thank S. Zhao, W. Bruce, and B. Zeka for tissue sampling and RNA preparation; R. Luedtke, D. Ritland, and L. Heetland for field experiment support; O. Folkerts, T. Jarvie, P. Pochart, G. Vijayadamodar, and D. Marks for their support in the GeneCalling technology and database development from the CuraGen Corporation. We specially thank D. Duvick and J. Birchler for critical reading of the manuscript.

Author information

Correspondence to Mei Guo.

Additional information

Communicated by F. van Eeuwijk

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Guo, M., Rupe, M.A., Yang, X. et al. Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113, 831–845 (2006).

Download citation


  • Maize Hybrid
  • Allelic Expression
  • Paternal Parent
  • Inbred Parent
  • Heterotic Pool