Global RNA sequencing reveals that genotype-dependent allele-specific expression contributes to differential expression in rice F1 hybrids

Abstract

BackgroundExtensive studies on heterosis in plants using transcriptome analysis have identified differentially expressed genes (DEGs) in F1 hybrids. However, it is not clear why yield in heterozygotes is superior to that of the homozygous parents or how DEGs are produced. Global allele-specific expression analysis in hybrid rice has the potential to answer these questions.ResultsWe report a genome-wide allele-specific expression analysis using RNA-sequencing technology of 3,637–3,824 genes from three rice F1 hybrids. Of the expressed genes, 3.7% exhibited an unexpected type of monoallelic expression and 23.8% showed preferential allelic expression that was genotype-dependent in reciprocal crosses. Those genes exhibiting allele-specific expression comprised 42.4% of the genes differentially expressed between F1 hybrids and their parents. Allele-specific expression accounted for 79.8% of the genes displaying more than a 10-fold expression level difference between an F1 and its parents, and almost all (97.3%) of the genes expressed in F1, but non-expressed in one parent. Significant allelic complementary effects were detected in the F1 hybrids of rice.ConclusionsAnalysis of the allelic expression profiles of genes at the critical stage for highest biomass production from the leaves of three different rice F1 hybrids identified genotype-dependent allele-specific expression genes. A cis-regulatory mechanism was identified that contributes to allele-specific expression, leading to differential gene expression and allelic complementary effects in F1 hybrids.

Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase

“…On the other hand, high-throughput gene-expression profiling in heterotic cross combinations has been carried out in both maize and rice, and a large number of genes have been found to be differentially expressed in the hybrids and their parents (17); some of these genes were reported to display nonadditive expression, in support of over-dominance, but others were mainly additive, supporting the dominance hypothesis. In addition, allelic variation in gene expression in hybrids has been reported in maize and rice (18). However, very few of the data obtained from high-throughput transcriptome analysis have been integrated with phenotypic profiles or mapped to single genetic loci associated with yield heterosis.…”

Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids

“…Nonadditive gene expression is the result of allelic interactions that modify regulatory networks that lead to gene activity patterns different from average parental values (Stupar and Springer, 2006). Furthermore, unexpected allelic expression patterns were observed in hybrids that deviated from the allelic ratios of their parents (Guo et al, 2004;Stupar and Springer, 2006;Springer and Stupar, 2007;Paschold et al, 2012;Song et al, 2013). Although nonadditive expression patterns and unexpected allelic ratios have been observed in hybrids of different species, none of these expression types have yet been associated with the evolutionary origin of these genes.…”

Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages

“…In the rice hybrid Xieyou9308, 17% of transcripts showed significant allelic bias at the tillering and heading stages [56]. A similar study of a reciprocal F1 hybrid between rice Nipponbare and 93–11 revealed that 22.7% of genes exhibited significant allelic expression differences [57]. In Arabidopsis , about 40% of genes showed allelic expression differences in the hybrid [58].…”