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.
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.
- Comstock RE, Robinson HF (1952) Estimation of average dominance of genes. In: Gowen JW (ed) Heterosis. Iowa State College Press, Ames, Iowa, pp. 494–516Google Scholar
- 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 83–145Google Scholar
- 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 109–151Google Scholar
- 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 319–333Google Scholar
- 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 17:798–803CrossRefGoogle Scholar
- Shull GH (1908) The composition of a field of maize. Am Breed Assoc Rep 4:296–301Google Scholar
- Smith OS, Smith JSC (1992) Measurement of genetic diversity among maize hybrids; a comparison of isozymic, RFLP, pedigree, and heterosis data. Maydica 37:53–60Google Scholar
- 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 195–203Google Scholar