Single-Parent Expression Is a General Mechanism Driving Extensive Complementation of Non-syntenic Genes in Maize Hybrids

Abstract

Maize (Zea mays L.) displays an exceptional degree of structural genomic diversity [1, 2]. In addition, variation in gene expression further contributes to the extraordinary phenotypic diversity and plasticity of maize. This study provides a systematic investigation on how distantly related homozygous maize inbred lines affect the transcriptomic plasticity of their highly heterozygous F₁ hybrids. The classical dominance model of heterosis explains the superiority of hybrid plants by the complementation of deleterious parental alleles by superior alleles of the second parent at many loci [3]. Genes active in one inbred line but inactive in another represent an extreme instance of allelic diversity defined as single-parent expression [4]. We observed on average ∼1,000 such genes in all inbred line combinations during primary root development. These genes consistently displayed expression complementation (i.e., activity) in their hybrid progeny. Consequently, extreme expression complementation is a general mechanism that results on average in ∼600 additionally active genes and their encoded biological functions in hybrids. The modern maize genome is complemented by a set of non-syntenic genes, which emerged after the separation of the maize and sorghum lineages and lack syntenic orthologs in any other grass species [5]. We demonstrated that non-syntenic genes are the driving force of gene expression complementation in hybrids. Among those, the highly diversified families of bZIP and bHLH transcription factors [6] are systematically overrepresented. In summary, extreme gene expression complementation extensively shapes the transcriptomic plasticity of maize hybrids and might therefore be one factor controlling the developmental plasticity of hybrids.

Keywords: RNA sequencing; complementation; dominance; heterosis; hybrid; maize; non-syntenic; primary root; single-parent expression; transcriptomics.