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

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Abstract

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.

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Acknowledgments

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.

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Author notes

  1. Oswald Crasta

    Present address: Virginia Bioinformatics Institute, Virginia, VA, 24061, USA

  2. Ben Bowen

    Present address: Gene-fx, Inc., Berkeley, CA, 94705, USA

Authors and Affiliations

  1. Pioneer Hi-Bred International, Inc., 7250 NW 62nd Avenue, Johnston, IA, 50131, USA

    Mei Guo, Mary A. Rupe, Xiaofeng Yang, Christopher Zinselmeier, Oscar S. Smith & Ben Bowen

  2. CuraGen Corp., New Haven, CT, USA

    Oswald Crasta

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  1. Mei Guo
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Correspondence to Mei Guo.

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Communicated by F. van Eeuwijk

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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). https://doi.org/10.1007/s00122-006-0335-x

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  • DOI: https://doi.org/10.1007/s00122-006-0335-x

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