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

View Article: PubMed Central - PubMed

ABSTRACT

Background: Hybridization 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.

Results: Using 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.

Conclusion: Our 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 material: The online version of this article (doi:10.1186/s12864-016-3296-8) contains supplementary material, which is available to authorized users.

No MeSH data available.


Venn diagram comparison and hierarchical cluster analysis of differentially expressed genes among genotypes. Venn diagram comparison of differential expressed genes between the hybrid and its parents in the spikelet (a) and floret differentiation stages (b) of maize immature ear. c Hierarchical cluster analysis of differentially expressed genes among genotypes. The color key represents log10(RPKM + 1). Red indicates high relative expression and blue indicates low relative expression. S denotes the spikelet differentiation stage, F denotes the floret differentiation stage
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Fig2: Venn diagram comparison and hierarchical cluster analysis of differentially expressed genes among genotypes. Venn diagram comparison of differential expressed genes between the hybrid and its parents in the spikelet (a) and floret differentiation stages (b) of maize immature ear. c Hierarchical cluster analysis of differentially expressed genes among genotypes. The color key represents log10(RPKM + 1). Red indicates high relative expression and blue indicates low relative expression. S denotes the spikelet differentiation stage, F denotes the floret differentiation stage

Mentions: Using a Venn diagram to compare DEGs between hybrid and its parents reveals that 59.3% (5298 and 2147) and 61.8% (4733 and 1525) DEGs between CL11 and NG5, respectively, are differentially expressed between HYB and CL11 in the spikelet and floret differentiation stages, whereas only 30.5% (1684 and 2147) and 9.6% (971 and 1525) are differentially expressed between HYB and NG5. A total of 24.7% (2147 of 12,550) and 15.1% (1525 of 10,120) of DEGs were shared by the three comparisons (Fig. 2a and b). The results show that DEGs are common existence and differ among genotypes and developmental stages. Hierarchical clustering of DEGs showed that different developmental stages of the same genotype tend to cluster together, and the gene expression patterns in the hybrid were more similar to those in the paternal line NG5 in both developmental stages (Fig. 2c). This result corresponds to the more robust ear phenotype of NG5 observed at corresponding stages (Fig. 1a and b).Fig. 2


Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages
Venn diagram comparison and hierarchical cluster analysis of differentially expressed genes among genotypes. Venn diagram comparison of differential expressed genes between the hybrid and its parents in the spikelet (a) and floret differentiation stages (b) of maize immature ear. c Hierarchical cluster analysis of differentially expressed genes among genotypes. The color key represents log10(RPKM + 1). Red indicates high relative expression and blue indicates low relative expression. S denotes the spikelet differentiation stage, F denotes the floret differentiation stage
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC5120533&req=5

Fig2: Venn diagram comparison and hierarchical cluster analysis of differentially expressed genes among genotypes. Venn diagram comparison of differential expressed genes between the hybrid and its parents in the spikelet (a) and floret differentiation stages (b) of maize immature ear. c Hierarchical cluster analysis of differentially expressed genes among genotypes. The color key represents log10(RPKM + 1). Red indicates high relative expression and blue indicates low relative expression. S denotes the spikelet differentiation stage, F denotes the floret differentiation stage
Mentions: Using a Venn diagram to compare DEGs between hybrid and its parents reveals that 59.3% (5298 and 2147) and 61.8% (4733 and 1525) DEGs between CL11 and NG5, respectively, are differentially expressed between HYB and CL11 in the spikelet and floret differentiation stages, whereas only 30.5% (1684 and 2147) and 9.6% (971 and 1525) are differentially expressed between HYB and NG5. A total of 24.7% (2147 of 12,550) and 15.1% (1525 of 10,120) of DEGs were shared by the three comparisons (Fig. 2a and b). The results show that DEGs are common existence and differ among genotypes and developmental stages. Hierarchical clustering of DEGs showed that different developmental stages of the same genotype tend to cluster together, and the gene expression patterns in the hybrid were more similar to those in the paternal line NG5 in both developmental stages (Fig. 2c). This result corresponds to the more robust ear phenotype of NG5 observed at corresponding stages (Fig. 1a and b).Fig. 2

View Article: PubMed Central - PubMed

ABSTRACT

Background: Hybridization 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.

Results: Using 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.

Conclusion: Our 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 material: The online version of this article (doi:10.1186/s12864-016-3296-8) contains supplementary material, which is available to authorized users.

No MeSH data available.