Submitted to: Proceedings of the National Academy of Sciences
Publication Type: Peer reviewed journal
Publication Acceptance Date: 6/25/2012
Publication Date: 7/24/2012
Publication URL: http://handle.nal.usda.gov/10113/58008
Citation: Chodavarapu, R.K., Feng, S., Ding, B., Simon, S.A., Lopez, D., Jia, Y., Wang, G., Meyers, B.C., Jacobsen, S.E., Pellegrini, M. 2012. Transcriptome and methylome interactions in rice hybrids. Proceedings of the National Academy of Sciences. 109:30-36. Interpretive Summary: Hybrid rice has been shown to have higher yields than conventional inbred rice and is being commercialized in several countries. This yield advantage is believed to be due to heterosis which is caused by presence of two different alleles, or versions of the same gene, at many locations along the chromosome. The different alleles are inherited from the two parent cultivars that are crossed to make the hybrid. However, the molecular basis of heterosis in hybrid rice is not well understood. DNA methylation is mechanism that can often lead to the repression of gene expression and may contribute to the extra vigor that is observed in hybrid progeny. In order to understand the molecular basis of rice heterosis, genetic maps were generated using different methods including genome cytosine methylation profiles (BS-Seq) and transcriptional profiles (RNA-seq). These were generated to characterize two rice cultivars that come from different subspecies, Oryza sativa spp japonica (Nipponbare) and Oryza sativa spp indica (93-11) and their two reciprocal hybrid offspring. Using a combination of BS-Seq and RNA-seq we were able to evaluate patterns of methylation and transcription in the hybrids and compare these with the patterns in the two parental cultivars. We identified genes with both allele-specific expression patterns that were strongly inherited as well as those that were differentially expressed between hybrids and the corresponding parental chromosome. Our data suggest that much of the difference in gene expression levels between the parent cultivars and hybrid offspring is likely due to modifications in how DNA is copied and processed from generation to generation. These findings will lead to a better understanding of how different methylation patterns from rice inbred parents may ‘interact’ during the generation of their hybrid progeny.
Technical Abstract: DNA methylation is a heritable epigenetic mark that controls gene expression, is responsive to environmental stresses, and in plants, also may play a role in heterosis. To determine the degree to which DNA methylation is inherited in rice, and how it both influences and is affected by transcription, we performed genome-wide measurements of these patterns through an integrative analysis of BS-seq,RNA-seq, and siRNA-seq data in two inbred parents of the Japonica (Nipponbare, NPB) and Indica (93-11)subspecies of rice and their hybrid offspring. We show that SNPs occur at a rate of about 1/253 bp between the two parents and that these are faithfully transmitted into the hybrids. We used the presence of these SNPs to reconstruct the two chromosomes in the hybrids according to their parental origin. We found that unlike genetic inheritance, epigenetic heritability is quite variable. Cytosines were found to be differentially methylated (epimutated) at a rate of 7.48% (1/15 cytosines) between the NPB and 93-11 parental strains. We also observed that 0.79% of cytosines were epimutated between the parents and their corresponding hybrid chromosomes. We found that these epimutations are often clustered on the chromosomes, with clusters representing 20% of all epimutations between parental ecotypes, and 2 to 5% in F1 plants. Epimutation clusters are also strongly associated with regions where the production of siRNA differs between parents. Finally, we identified genes with both allele-specific expression patterns that were strongly inherited as well as those differentially expressed between hybrids and the corresponding parental chromosomes. We conclude that much of the misinheritance of expression levels is likely due to epimutations and trans effects.