Transcriptomic regulation of hybrid vigor in immortalized backcross populations of maize (<em>Zea mays</em> L.)

Abstract

Heterosis is the phenomenon that heterozygous F₁-hybrids outperform their distinct homozygous parental inbred lines for many agronomically important traits. Despite its economic importance and utilization for almost 100 years, the molecular mechanisms underlying heterosis are not fully understood. It has been demonstrated that genes with expression differences between parents and their hybrid progeny are involved in heterosis. However, quantitative associations between gene expression differences and heterosis are scarce, and the regulation of these differences is not yet established. This thesis aimed to close these knowledge gaps and advance the molecular understanding of heterosis. We analyzed 112 lines of the intermated B73xMo17 recombinant inbred line (IBM-RIL) population of maize and their backcrosses to B73 and Mo17. These backcross hybrids contain heterozygous and homozygous genomic regions and allow for the identification of genomic locations regulating specific gene expression patterns.<br /> In chapter 3 of this thesis we investigated single parent expression (SPE). These genes, which are active in only one of the parents and in the hybrid, explained up to 29% of the heterotic variance in the backcross hybrids. This pattern of expression complementation in hybrids is consistent with the dominance model of heterosis. Moreover, expression quantitative loci (eQTL), regulating SPE genes are predominantly located in heterozygous regions of the genome, highlighting the importance of the genomic architecture of regulatory elements for gene expression. As a consequence, heterozygosity leads to a higher number of active genes in the backcross hybrids by SPE complementation. Finally, we identified an SPE gene that regulates lateral root density in hybrids. Notably, the activity of this gene depends on the presence of a Mo17 allele in the eQTL that regulates it. This highlights the pivotal role of distantly located regulatory elements for the activity of heterosis-associated genes.<br /> In chapter 4 we analyzed non-additive gene expression, a pattern in which genes in the hybrid are expressed significantly different from the average of the two parents. In most instances, these genes exceeded the mean of the parental expression. Non-additive gene expression explained up to 27% of the heterotic variance. Consistent with our observation for SPE genes, complementation of non-additive genes is consistent with the dominance model and is regulated almost exclusively by eQTL in heterozygous genomic regions. Moreover, regulation of non-additively expressed genes depends on the genetic origin of the higher expressed parent.<br /> In summary, gene expression complementation contributes substantially to heterosis, likely by increasing the number of active genes by SPE or by higher expression levels of non-additive genes in the hybrids. Heterozygosity and the genetic architecture of hybrids might be aspects of how genetic variation is translated into vigorous hybrids via the regulation of heterosis-associated gene expression patterns.