Abstract
BackgroundHybridization is a prominent process in the evolution of crop plants that can give rise to gene expression variation, phenotypic novelty and heterosis. Maize is the most successful crop in utilizing heterosis. The development of hybrid maize ears exhibits strong heterotic vigor and greatly affects maize yield. However, a comprehensive perspective on transcriptional variation and its correlation with heterosis during maize ear development is not available.ResultsUsing RNA sequencing technology, we investigated the transcriptome profiles of maize ears in the spikelet and floret differentiation stages of hybrid ZD808 and its parents CL11 and NG5. Our results revealed that 53.9% (21,258) of maize protein-coding genes were transcribed in at least one genotype. In both development stages, significant numbers of genes were differentially expressed between the hybrid and its parents. Gene expression inheritance analysis revealed approximately 80% of genes were expressed additively, which suggested that the complementary effect may play a foundation role in maize ear heterosis. Among non-additively expressed genes, NG5-dominant genes were predominant. Analyses of the allele-specific gene expression in hybrid identified pervasive allelic imbalance and significant preferential expression of NG5 alleles in both developmental stages. The results implied that NG5 may provide beneficial alleles that contribute greatly to heterosis. Further comparison of parental and hybrid allele-specific expression suggested that gene expression variation is largely attributable to cis-regulatory variation in maize. The cis-regulatory variations tend to preserve the allelic expression levels in hybrid and result in additive expression. Comparison between the two development stages revealed that allele-specific expression and cis-/trans-regulatory variations responded differently to developmental cues, which may lead to stage-specific vigor phenotype during maize ear development.ConclusionOur research suggests that cis-regulated additive expression may fine-tune gene expression level into an optimal status and play a foundation role in maize ear heterosis. Our work provides a comprehensive insight into transcriptional variation and its correlation with heterosis during maize ear development. The knowledge gained from this study presents novel opportunity to improve our maize varieties.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3296-8) contains supplementary material, which is available to authorized users.
Highlights
Hybridization is a prominent process in the evolution of crop plants that can give rise to gene expression variation, phenotypic novelty and heterosis
Characterizing the ear traits of ZD808 and its parental lines To dissect the relationship between global gene expression changes and heterosis during ear development, the immature ears of ZD808 (HYB) and its parent lines in spikelet and floret differentiation stages were collected for transcriptome analysis (Fig. 1a)
We observed significant midparent heterosis (MPH) and best-parent heterosis (BPH) (p < 0.01) for the ear length, ear diameter, kernel number per row and grain yield at the mature stage (Table 1). These results indicate that ZD808 displays a strong hybrid vigor than both parents and the degree of heterosis for ear traits was larger in the spikelet differentiation stage
Summary
Hybridization is a prominent process in the evolution of crop plants that can give rise to gene expression variation, phenotypic novelty and heterosis. A comprehensive perspective on transcriptional variation and its correlation with heterosis during maize ear development is not available. Heterosis refers to the superior performance in biomass, yield, or other agronomic traits of hybrids relative to their parents [1, 2]. This phenomenon has revolutionized crop breeding and production by increasing yields from 15 to 50% [3, 4]. With the development of omics technologies, studies in hybrids using genomic, transcriptomic, epigenomic and proteomic approaches have provided a new perspective into the molecular mechanisms of heterosis [1, 10, 11]
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