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Transcriptomic plasticity of maize hybrids and their parental inbred lines at the interface of genotype and development

Subject Area Plant Breeding and Plant Pathology
Term from 2010 to 2019
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 166916654
 
Final Report Year 2019

Final Report Abstract

F1-hybrids are more vigorous than their homozygous, genetically distinct parents, a phenomenon known as heterosis. In the present DFG project, we discovered that an extreme instance of gene expression complementation is widespread in maize. We designated the observation that hundreds of maize genes are active in only one of the two parental inbred lines as single parent expression (SPE) and demonstrated that these genes are almost always active in the corresponding F1-hybrids. This type of gene expression complementation is consistent with the dominance model for heterosis. Only a small fraction of SPE patterns are due to genomic presence absence variations i.e. that lack of these genes in one genotype. In most instances, only the allele active in one inbred line was active in the hybrid. Our initial study was executed in whole seedling roots of the genotypes B73 and Mo17 and their reciprocal hybrids. In follow up experiments, we surveyed how the genetic divergence of these two maize inbred lines affects the transcriptomic landscape in four different primary root tissues of its F1-hybrid progeny. We observed in all tissues hundreds of SPE patterns. As a consequence, the number of active genes in hybrids exceeded that of their parents in each tissue by >400. SPE patterns are highly dynamic as illustrated by their excessive degree of tissue-specificity (80%). The biological significance of this type of complementation is underpinned by the observation that a disproportionally high number of SPE genes is nonsyntenic – as opposed to all expressed genes. Non-syntenic genes likely evolved after the last whole genome duplication and are therefore younger than the syntenic genes. Moreover, we demonstrated that SPE patterns are substantially more stable to expression changes by water deficit treatment than other genotype-specific expression profiles. Subsequently, we extended our analysis to a distantly related panel of homozygous maize inbred lines and to three different stages of root development. We observed on average ~1,000 SPE patterns for all inbred line combinations during primary root development. By this analysis, we demonstrated that extreme expression complementation is a general mechanism that results in hundreds of additionally active genes and their encoded biological functions in hybrids. We also demonstrated that non-syntenic genes are the driving force of gene expression complementation in hybrids in all surveyed instances. Among those, the highly diversified families of bZIP and bHLH transcription factors were systematically overrepresented. In summary, we demonstrated that extreme gene expression complementation extensively shapes the transcriptomic plasticity of maize hybrids and might therefore be one factor controlling the developmental plasticity of hybrids.

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