Abstract
Heterosis, also known as the hybrid vigor, occurs when the mean phenotype of hybrid offspring is superior to that of its two inbred parents. The heterosis phenomenon is extensively utilized in agriculture though the molecular basis is still unknown. In an effort to understand phenotypic heterosis at the molecular level, researchers have begun to compare expression levels of thousands of genes between parental inbred lines and their hybrid offspring to search for evidence of gene expression heterosis. Standard statistical approaches for separately analyzing expression data for each gene can produce biased and highly variable estimates and unreliable tests of heterosis. To address these shortcomings, we develop a hierarchical model to borrow information across genes. Using our modeling framework, we derive empirical Bayes estimators and an inference strategy to identify gene expression heterosis. Simulation results show that our proposed method outperforms the more traditional strategy used to detect gene expression heterosis. This article has supplementary material online.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Anders, S., and Huber, W. (2010), “Differential Expression Analysis for Sequence Count Data,” Genome Biology, 11, R106.
Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K. H., Sherman, P. M., Muertter, R. N., Holko, M., Ayanbule, O., Yefanov, A., and Soboleva, A. (2011), “NCBI GEO: Archive for Functional Genomics Data Sets—10 Years on,” Nucleic Acids Research, 39, D1005–D1010.
Bassene, J. B., Froelicher, Y., Dubois, C., Ferrer, R. M., Navarro, L., Ollitrault, P., and Ancillo, G. (2010), “Non-Additive Gene Regulation in a Citrus Allotetraploid Somatic Hybrid Between C. Reticulata Blanco and C. Limon (L.) Burm,” Heredity, 105, 299–308.
Coors, J. G., and Pandey, S. (1999), The Genetics and Exploitation of Heterosis in Crops, Madison, WI: Crop Science Society of America.
Darwin, C. R. (1876), The Effects of Cross and Self Fertilization in the Vegetable Kingdom, London: Murray.
Geer, L. Y., Marchler-Bauer, A., Geer, R. C., Han, L., He, J., He, S., Liu, C., Shi, W., and Bryant, S. H. (2010), “The NCBI BioSystems Database,” Nucleic Acids Research, 38, D492–D496.
Hallauer, A. R., and Miranda, J. B. (1981), Quantitative Genetics in Maize Breeding, Ames, IA: Iowa State University Press.
Irizarray, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003), “Exploration, Normalization, and Summaries of High Density Oligonucleotide Array Probe Level Data,” Biostatistics, 4, 249–264.
Krieger, U., Lippman, Z. B., and Zamir, D. (2010), “The Flowering Gene SINGLE FLOWER TRUSS Drives Heterosis for Yield in Tomato,” Nature Genetics, 42, 459–463.
Lippman, Z. B., and Zamir, D. (2007), “Heterosis: Revisiting the Magic,” Trends in Genetics, 23, 60–66.
Lund, S. P., Nettleton, D., McCarthy, D. J., and Smyth, G. K. (2012), “Detecting Differential Expression in RNA-Sequence Data Using Quasi-Likelihood with Shrunken Dispersion Estimates,” Statistical Applications in Genetics and Molecular Biology, 11, 8.
McCarthy, D. J., Chen, Y., and Smyth, G. K. (2012), “Differential Expression Analysis of Multifactor RNA-Seq Experiments with Respect to Biological Variation,” Nucleic Acids Research, 40, 4288–4297.
McClintick, J. N., and Edenberg, H. J. (2006), “Effects of Filtering by Present Call on Analysis of Microarray Experiments,” BMC Bioinformatics, 7, 49.
Riday, H., and Brummer, E. C. (2002), “Forage Yield Heterosis in Alfalfa,” Crop Science, 42, 716–723.
Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010), “EdgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data,” Bioinformatics, 26, 139–140.
Smyth, G. (2004), “Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments,” Statistical Applications in Genetics and Molecular Biology, 3, 3.
Springer, N. M., and Stupar, R. M. (2007), “Allelic Variation and Heterosis in Maize: How do Two Halves Make More than a Whole?” Genome Research, 17, 264–275.
Storey, J. D., and Tibshirani, R. (2003), “Statistical Significance for Genomewide Studies,” Proceedings of the National Academy of Sciences, 100, 9440–9445.
Swanson-Wagner, R., DeCook, R., Jia, Y., Bancroft, T., Ji, T., Zhao, X., Nettleton, D., and Schnable, P. S. (2009), “Paternal Dominance of Trans-eQTL Influences Gene Expression Patterns in Maize Hybrids,” Science, 5956, 1118–1120.
Swanson-Wagner, R., Jia, Y., DeCook, R., Borsuk, L. A., Nettleton, D., and Schnable, P. S. (2006), “All Possible Modes of Gene Action Are Observed in a Global Comparison of Gene Expression in a Maize F 1 Hybrid and Its Inbred Parents,” Proceedings of the National Academy of Sciences, 103, 6805–6810.
Wang, J., Tian, L., Lee, H., Wei, N., Jiang, H., Watson, B., Madlung, A., Osborn, T. C., Doerge, R. W., Comai, L., and Chen, Z. J. (2006), “Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids,” Genetics, 172, 507–517.
Wohlfarth, G. W. (1993), “Heterosis for Growth Rate in Common Carp,” Aquaculture, 113, 31–46.
Yu, S. B., Li, J. X., Xu, C. G., Tan, Y. F., Gao, Y. J., Li, X. H., Zhang, Q., and Saghai Maroof, M. A. (1997), “Importance of Epistasis as the Genetic Basis of Heterosis in an Elite Rice Hybrid,” Proceedings of the National Academy of Sciences, 94, 9226–9231.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
About this article
Cite this article
Ji, T., Liu, P. & Nettleton, D. Estimation and Testing of Gene Expression Heterosis. JABES 19, 319–337 (2014). https://doi.org/10.1007/s13253-014-0173-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13253-014-0173-2