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

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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.


The allele-specific expression analysis in hybrid in the spikelet and floret differentiation stages. The proportions of genes with monoallelic expression, preferential allelic expression and biallelic expression profiles in hybrid in the spikelet (a) and floret differentiation stage (b) of maize ear
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Fig4: The allele-specific expression analysis in hybrid in the spikelet and floret differentiation stages. The proportions of genes with monoallelic expression, preferential allelic expression and biallelic expression profiles in hybrid in the spikelet (a) and floret differentiation stage (b) of maize ear

Mentions: The transcriptional activities of different alleles in a hybrid can differ considerably, and this is an important source of the variation in gene expression. To infer hybrid ASE levels, parent-specific SNPs were detected in each parent and used to discern alleles in the hybrid. After applying quality control criteria, we found that 44,675 and 38,957 of SNPs located in gene bodies had a minimum read coverage of 10 in the hybrid at the spikelet and floret differentiation stages, respectively. A total of 12,637 and 11,993 genes, which represented 32.0 and 30.4% of protein coding genes, respectively, were marked by the filtered SNPs (Table 4). Normalized mapped read-depth coverage at SNP sites in the hybrid and parental alignments was used to quantify the expression of alleles. Allelic bias in the hybrid was identified for each SNP if the allelic ratio differed significantly from the expected allelic ratio of 1.0 (binomial exact test, adjust p-value < 0.05). For convenience, we used CL11HYB and NG5HYB to represent the expression levels of the corresponding allele in the hybrid. In the spikelet differentiation stage of maize ear, 7126 genes (56.4% of 12,637 analyzed genes) were identified as having significant allelic bias. Of these, 2514 (35.3%) genes displayed CL11HYB bias and 4612 (64.7%) genes displayed NG5HYB bias (Fig. 4 and Additional file 9). In the floret differentiation stage, we identified 6625 (52.4%) ASE genes; 2967 (44.8%) genes exhibited CL11HYB bias and 3658 (55.2%) genes exhibited NG5HYB bias (Fig. 4 and Additional file 10). These results indicated a strong expression bias toward NG5HYB in both developmental stages, suggesting that the NG5 genome contributes greatly to gene expression in the hybrid.Table 4


Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages
The allele-specific expression analysis in hybrid in the spikelet and floret differentiation stages. The proportions of genes with monoallelic expression, preferential allelic expression and biallelic expression profiles in hybrid in the spikelet (a) and floret differentiation stage (b) of maize ear
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: The allele-specific expression analysis in hybrid in the spikelet and floret differentiation stages. The proportions of genes with monoallelic expression, preferential allelic expression and biallelic expression profiles in hybrid in the spikelet (a) and floret differentiation stage (b) of maize ear
Mentions: The transcriptional activities of different alleles in a hybrid can differ considerably, and this is an important source of the variation in gene expression. To infer hybrid ASE levels, parent-specific SNPs were detected in each parent and used to discern alleles in the hybrid. After applying quality control criteria, we found that 44,675 and 38,957 of SNPs located in gene bodies had a minimum read coverage of 10 in the hybrid at the spikelet and floret differentiation stages, respectively. A total of 12,637 and 11,993 genes, which represented 32.0 and 30.4% of protein coding genes, respectively, were marked by the filtered SNPs (Table 4). Normalized mapped read-depth coverage at SNP sites in the hybrid and parental alignments was used to quantify the expression of alleles. Allelic bias in the hybrid was identified for each SNP if the allelic ratio differed significantly from the expected allelic ratio of 1.0 (binomial exact test, adjust p-value < 0.05). For convenience, we used CL11HYB and NG5HYB to represent the expression levels of the corresponding allele in the hybrid. In the spikelet differentiation stage of maize ear, 7126 genes (56.4% of 12,637 analyzed genes) were identified as having significant allelic bias. Of these, 2514 (35.3%) genes displayed CL11HYB bias and 4612 (64.7%) genes displayed NG5HYB bias (Fig. 4 and Additional file 9). In the floret differentiation stage, we identified 6625 (52.4%) ASE genes; 2967 (44.8%) genes exhibited CL11HYB bias and 3658 (55.2%) genes exhibited NG5HYB bias (Fig. 4 and Additional file 10). These results indicated a strong expression bias toward NG5HYB in both developmental stages, suggesting that the NG5 genome contributes greatly to gene expression in the hybrid.Table 4

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.