Stability of Single-Parent Gene Expression Complementation in Maize Hybrids upon Water Deficit Stress

Abstract

Heterosis is the superior performance of F1 hybrids compared with their homozygous, genetically distinct parents. In this study, we monitored the transcriptomic divergence of the maize (Zea mays) inbred lines B73 and Mo17 and their reciprocal F1 hybrid progeny in primary roots under control and water deficit conditions simulated by polyethylene glycol treatment. Single-parent expression (SPE) of genes is an extreme instance of gene expression complementation, in which genes are active in only one of two parents but are expressed in both reciprocal hybrids. In this study, 1,997 genes only expressed in B73 and 2,024 genes only expressed in Mo17 displayed SPE complementation under control and water deficit conditions. As a consequence, the number of active genes in hybrids exceeded the number of active genes in the parental inbred lines significantly independent of treatment. SPE patterns were substantially more stable to expression changes by water deficit treatment than other genotype-specific expression profiles. While, on average, 75% of all SPE patterns were not altered in response to polyethylene glycol treatment, only 17% of the remaining genotype-specific expression patterns were not changed by water deficit. Nonsyntenic genes that lack syntenic orthologs in other grass species, and thus evolved late in the grass lineage, were significantly overrepresented among SPE genes. Hence, the significant overrepresentation of nonsyntenic genes among SPE patterns and their stability under water limitation might suggest a function of these genes during the early developmental manifestation of heterosis under fluctuating environmental conditions in hybrid progeny of the inbred lines B73 and Mo17.

Highly Genotype- and Tissue-specific Single-Parent Expression Drives Dynamic Gene Expression Complementation in Maize Hybrids

“…These results indicate a vital role of constitutively expressed syntenic genes for the maintenance of basic cellular function. In contrast, we found PAV SPE and non-PAV SPE genes are highly enriched in the non-syntenic gene space and depleted for genes with possible functions from the curated gene set, consistent with previous findings (Swanson-Wagner et al, 2010;Paschold et al, 2014;Marcon et al, 2017;Baldauf et al, 2018).…”

“…Transcriptome divergence between maize inbred parents and their F 1 -hybrid progeny has been previously investigated (Guo et al, 2004;Swanson-Wagner et al, 2006;Springer and Stupar, 2007b;Stupar et al, 2008;Paschold et al, 2012;Paschold et al, 2014;Baldauf et al, 2016;Marcon et al, 2017;Waters et al, 2017;Baldauf et al, 2018). While these studies provided insights into transcriptional variation between inbreds and hybrids and its potential role in heterosis, they were performed in one or a handful of parent-hybrid triplets or only a single tissue.…”

“…Non-syntenic genes may also play an important role in the ability of hybrids to deal with abiotic stress conditions (Marcon et al, 2017). While syntenic and non-syntenic genes seem to be specialized in different aspects of plant life, the interaction of syntenic and non-syntenic genes in different developmental stages can have an important impact on phenotype.…”

“…Furthermore, the enrichment of non-syntenic genes in non-PAV SPE and PAV SPE gene sets, along with the enrichment for expression complementation in the hybrids across genotypes and tissues for these genes, could contribute to the superior adaptation of hybrid plants to environmental stresses. The high genotype-and tissuespecific nature of non-PAV SPE and PAV SPE genes could also contribute to the diversified manifestation of heterosis across traits, environments, and genetic combinations (Flint-Garcia et al, 2009;Schnable and Springer, 2013;Marcon et al, 2017;Li et al, 2018).…”

“…More recently, the role of single parent expression (SPE) genes in heterosis has been investigated (Paschold et al, 2012;Paschold et al, 2014;Baldauf et al, 2016;Marcon et al, 2017;Baldauf et al, 2018). SPE refers to a situation in which expression can only be detected in one of the two parental lines of a hybrid.…”