Universality and regulation of gene expression complementation and its association with the phenotypic manifestation of heterosis in maize hybrids

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The observation that F1-hybrids are more vigorous than their parents is commonly referred to as heterosis or hybrid vigor. Maize, which provides the highest annual global kernel yield of all cereal species, is exclusively hybrid based in the major corn producing countries. The exploitation of hybrid vigor is considered as one of the most important innovations in modern agriculture because of its eminent economic importance. Nevertheless, the underlying molecular mechanisms remain largely enigmatic. In previous work, we observed an extreme form of gene expression complementation in hybrids for hundreds of genes that we designated single parent expression (SPE). Genes displaying such expression patterns are only active in one parent but always in the hybrid and thus are consistent with the dominance model of heterosis. As a consequence of these expression patterns, hybrids display hundreds of additionally active genes compared to their parental inbred lines. In the first part of this project, we will apply RNA-Seq to demonstrate that SPE complementation is universally observed and displays significant plasticity in belowground versus aboveground, seedling compared to mature and vegetative versus generative tissues in a distinct panel of genotypes. Subsequently, we will apply genomic evolutionary rate profiling to test the hypothesis that the inactive alleles in SPE patterns represent in general deleterious alleles, which would be in accordance with the dominance model of heterosis. In the second part of this project, we aim to understand the regulation of SPE complementation and its role in the phenotypic manifestation of heterosis. To this end we will take advantage of a maize recombinant inbred line population backcrossed to their parental inbred lines to identify key regulators of SPE genes by the determination of trans-eQTL regulatory networks via RNA-seq. Recombinant inbred lines backcrossed to their parents contain on average 50% heterozygous genes, whereas SPE patterns are expected to be reduced on average to only 75% in these genotypes compared to crosses of the two parental lines. Hence, in these populations the influence of heterozygosity and extreme dominance on heterosis can be separated. The variation of the number of SPE patterns in different recombinant inbred lines will allow testing their influence on phenotypic performance of the studied traits. Finally, high-resolution SNP markers obtained by the RNA-seq experiment will be used to identify loci underlying some of the heterotic traits quantified in this project by QTL mapping. In summary, these experiments will contribute to the mechanistic understanding of the molecular basis of heterosis and will provide knowledge that will facilitate the exploitation of heterosis in breeding and thus maize improvement.