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Genome-wide proteomic profiling reveals the role of dominance protein expression in heterosis in immature maize ears.

ABSTRACT: Heterosis refers to the phenomenon in which hybrid progeny show superior performance relative to their parents. Early maize ear development shows strong heterosis in ear architecture traits and greatly affects grain yield. To explore the underlying molecular mechanisms, genome-wide proteomics of immature ears of maize hybrid ZD909 and its parents were analyzed using tandem mass tag (TMT) technology. A total of 9,713 proteins were identified in all three genotypes. Among them, 3,752 (38.6%) proteins were differentially expressed between ZD909 and its parents. Multiple modes of protein action were discovered in the hybrid, while dominance expression patterns accounted for 63.6% of the total differentially expressed proteins (DEPs). Protein pathway enrichment analysis revealed that high parent dominance proteins mainly participated in carbon metabolism and nitrogen assimilation processes. Our results suggested that the dominant expression of favorable alleles related to C/N metabolism in the hybrid may be essential for ZD909 ear growth and heterosis formation. Integrated analysis of proteomic and quantitative trait locus (QTL) data further support our DEP identification and provide useful information for the discovery of genes associated with ear development. Our study provides comprehensive insight into the molecular mechanisms underlying heterosis in immature maize ears from a proteomic perspective.

SUBMITTER: Hu X

PROVIDER: S-EPMC5700959 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The identification of QTL involved in heterosis formation is one approach to unravel the not yet fully understood genetic basis of heterosis - the improved agronomic performance of hybrid F1 plants compared to their inbred parents. The identification of candidate genes underlying a QTL is important both for developing markers and determining the molecular genetic basis of a trait, but remains difficult owing to the large number of genes often contained within individual QTL. To address this problem in heterosis analysis, we applied a meta-analysis strategy for grain yield (GY) of Zea mays L. as example, incorporating QTL-, hybrid field-, and parental gene expression data. RESULTS: For the identification of genes underlying known heterotic QTL, we made use of tight associations between gene expression pattern and the trait of interest, identified by correlation analyses. Using this approach genes strongly associated with heterosis for GY were discovered to be clustered in pericentromeric regions of the complex maize genome. This suggests that expression differences of sequences in recombination-suppressed regions are important in the establishment of heterosis for GY in F1 hybrids and also in the conservation of heterosis for GY across genotypes. Importantly functional analysis of heterosis-associated genes from these genomic regions revealed over-representation of a number of functional classes, identifying key processes contributing to heterosis for GY. Based on the finding that the majority of the analyzed heterosis-associated genes were addtitively expressed, we propose a model referring to the influence of cis-regulatory variation on heterosis for GY by the compensation of fixed detrimental expression levels in parents. CONCLUSIONS: The study highlights the utility of a meta-analysis approach that integrates phenotypic and multi-level molecular data to unravel complex traits in plants. It provides prospects for the identification of genes relevant for QTL, and also suggests a model for the potential role of additive expression in the formation and conservation of heterosis for GY via dominant, multigenic quantitative trait loci. Our findings contribute to a deeper understanding of the multifactorial phenomenon of heterosis, and thus to the breeding of new high yielding varieties.

Project description:Heterosis, which has greatly increased maize yields, is associated with gene expression patterns during key developmental stages that enhance hybrid phenotypes relative to parental phenotypes. Before heterosis can be more effectively used for crop improvement, hybrid maize developmental gene expression patterns must be better understood. Here, six maize hybrids, including the popular hybrid Zhengdan958 (ZC) from China, were studied. Maize hybrids created in-house were generated using an incomplete diallel cross (NCII)-based strategy from four elite inbred parental lines. Differential gene expression (DEG) profiles corresponding to three developmental stages revealed that hybrid partial expression patterns exhibited complementarity of expression of certain parental genes, with parental allelic expression patterns varying both qualitatively and quantitatively in hybrids. Single-parent expression (SPE) and parent-specific expression (PSE) types of qualitative variation were most prevalent, 43.73 and 41.07% of variation, respectively. Meanwhile, negative super-dominance (NSD) and positive super-dominance (PSD) types of quantitative variation were most prevalent, 31.06 and 24.30% of variation, respectively. During the early reproductive growth stage, the gene expression pattern differed markedly from other developmental stage patterns, with allelic expression patterns during seed development skewed toward low-value parental alleles in hybrid seeds exhibiting significant quantitative variation-associated superiority. Comparisons of qualitative gene expression variation rates between ZC and other hybrids revealed proportions of SPE-DEGs (41.36%) in ZC seed DEGs that significantly exceeded the average proportion of SPE-DEGs found in seeds of other hybrids (28.36%). Importantly, quantitative gene expression variation rate comparisons between ZC and hybrids, except for transgressive expression, revealed that the ZC rate exceeded the average rate for other hybrids, highlighting the importance of partial gene expression in heterosis. Moreover, enriched ZC DEGs exhibiting distinct tissue-specific expression patterns belonged to four biological pathways, including photosynthesis, plant hormone signal transduction, biology metabolism and biosynthesis. These results provide valuable technical insights for creating hybrids exhibiting strong heterosis.

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Genome-wide proteomic profiling reveals the role of dominance protein expression in heterosis in immature maize ears.

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