We performed a genome-wide analysis of ASE in three tissues of an elite rice hybrid grown under four conditions. The analysis identified 3,270 genes showing various patterns of ASE in response to developmental and environmental cues, which provides a glimpse of the ASE landscape in the hybrid genome. We showed that the ASE patterns may have distinct implications in the genetic basis of heterosis, especially in light of the classical dominance and overdominance hypotheses. The genes showing ASE provide the candidates for future studies of the genetic and molecular mechanism of heterosis.
Utilization of heterosis has greatly increased the productivity of many crops worldwide. Although tremendous progress has been made in characterizing the genetic basis of heterosis using genomic technologies, molecular mechanisms underlying the genetic components are much less understood. Allele-specific expression (ASE), or imbalance between the expression levels of two parental alleles in the hybrid, has been suggested as a mechanism of heterosis. Here, we performed a genome-wide analysis of ASE by comparing the read ratios of the parental alleles in RNA-sequencing data of an elite rice hybrid and its parents using three tissues from plants grown under four conditions. The analysis identified a total of 3,270 genes showing ASE (ASEGs) in various ways, which can be classified into two patterns: consistent ASEGs such that the ASE was biased toward one parental allele in all tissues/conditions, and inconsistent ASEGs such that ASE was found in some but not all tissues/conditions, including direction-shifting ASEGs in which the ASE was biased toward one parental allele in some tissues/conditions while toward the other parental allele in other tissues/conditions. The results suggested that these patterns may have distinct implications in the genetic basis of heterosis: The consistent ASEGs may cause partial to full dominance effects on the traits that they regulate, and direction-shifting ASEGs may cause overdominance. We also showed that ASEGs were significantly enriched in genomic regions that were differentially selected during rice breeding. These ASEGs provide an index of the genes for future pursuit of the genetic and molecular mechanism of heterosis.
Figure 1: Summary and features of ASEGs. (A) Numbers of ASEGs in shoot, flag leaf, and panicle under four conditions. (B–D) Four-way Venn diagrams displaying the numbers of ASEGs in shoot (B), flag leaf (C), and panicle (D) under HTLD, LTLD, HTSD, and LTSD. The numbers of ASEGs that were detected in all four conditions are indicated as shoot (I), flag leaf (II), and panicle (III). (E) Three-way Venn diagram showing the numbers of ASEGs that overlap in the three tissues based on the ASEGs of groups I, II, and III in B–D. The 261 genes that showed consistent ASE in terms of the direction of expression bias in all three tissues at all four growth conditions are regarded as consistent ASEGs. (F) Features of consistent ASEGs with high, moderate, low, and modifier impact variations that are caused by SNPs and indels between ZS97RS1 and MH63RS1. The unique numbers of the impact categories are indicated, with certain overlapping among the subclassifications within each impact category. del, deletion; in, insertion.