A Genome-Wide Transcription Analysis Reveals a Close Correlation of Promoter INDEL Polymorphism and Heterotic Gene Expression in Rice Hybrids

Abstract

Heterosis, or hybrid vigor, refers to the phenomenon in which hybrid progeny of two inbred varieties exhibits enhanced growth or agronomic performance. Although a century-long history of research has generated several hypotheses regarding the genetic basis of heterosis, the molecular mechanisms underlying heterosis and heterotic gene expression remain elusive. Here, we report a genome-wide gene expression analysis of two heterotic crosses in rice, taking advantage of its fully sequenced genomes. Approximately 7-9% of the genes were differentially expressed in the seedling shoots from two sets of heterotic crosses, including many transcription factor genes, and exhibited multiple modes of gene action. Comparison of the putative promoter regions of the ortholog genes between inbred parents revealed extensive sequence variation, particularly small insertions/deletions (INDELs), many of which result in the formation/disruption of putative cis-regulatory elements. Together, these results suggest that a combinatorial interplay between expression of transcription factors and polymorphic promoter cis-regulatory elements in the hybrids is one plausible molecular mechanism underlying heterotic gene action and thus heterosis in rice.

A transcriptomic analysis of superhybrid rice LYP9 and its parents

“…For example, we found that the DG HP involved in the carbohydrate-metabolism pathway had a larger fraction of up-regulated genes than downregulated genes, similar to the recent studies (23,27). However, of the genes taking part in oxidative phosphorylation, there were more down-regulated genes identified in the hybrid than in the parental lines.…”

“…We indeed found that 187 TFs exhibited differential expression in the hybrid compared with either parent. It is quite a coincidence that a recent study using seedling tissue of 2 hybrid triads, based on the genomic sequence of 93-11 and nipponbare, also suggested that altered gene expression caused by interactions between transcription factors and the allelic promoter region in the hybrids was one plausible mechanism underlying heterosis in rice (23). Moreover, we noticed that among those differentially expressed TFs, the AP2-EREBP family-potential targets of miRNA (24)-is overrepresented.…”

“…The analysis of nonadditive gene expression indicates that allelic expression in hybrids may not just be a combination of alleles from the 2 parents but is rather regulated by other genes or epistatic mechanisms. Nonadditive gene expression was also considered as midparent heterosis or heterotic expression (10,23).…”

Transcriptome and methylome interactions in rice hybrids

“…The two varieties of rice that we studied demonstrate significant heterosis, a phenomenon whereby matings by more distant plants, intra-or interspecies, result in offspring with superior agronomic traits, such as tiller number and dry weight (9,(23)(24)(25). Previous studies of heterosis have revealed possible mechanisms to account for the increased vigor, but the mechanisms that underlie this complex phenotype are still poorly understood, and the role of DNA methylation in heterosis is unclear (26)(27)(28)(29).…”

Assessing the Influence of Adjacent Gene Orientation on the Evolution of Gene Upstream Regions inArabidopsis thaliana

“…Constraints on indel polymorphisms in intergenic regions have been demonstrated in Drosophila melanogaster (Ometto et al 2005). In rice, a study of genes displaying cis-regulatory differences in a heterotic F 1 cross were shown to be associated with indel variation and not single nucleotide polymorphism (Zhang et al 2008). Indel polymorphism may therefore alter cis-regulatory function more strongly than single nucleotide polymorphism.…”