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Curr Biol. 2018 Feb 5;28(3):431-437.e4. doi: 10.1016/j.cub.2017.12.027. Epub 2018 Jan 18.

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

Author information

1
Institute for Crop Science and Resource Conservation, Crop Functional Genomics, University of Bonn, Friedrich-Ebert-Allee 144, 53113 Bonn, Germany.
2
Department of Statistics, Iowa State University, 2438 Osborne Dr., Ames, IA 50011-1210, USA.
3
Institute for Crop Science and Resource Conservation, Crop Bioinformatics, University of Bonn, Katzenburgweg 2, 53115 Bonn, Germany.
4
Institute for Crop Science, Biostatistics Unit, University of Hohenheim, Fruwirthstraße 23, 70599 Stuttgart, Germany.
5
Institute for Crop Science and Resource Conservation, Crop Functional Genomics, University of Bonn, Friedrich-Ebert-Allee 144, 53113 Bonn, Germany. Electronic address: hochholdinger@uni-bonn.de.

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

PMID:
29358068
DOI:
10.1016/j.cub.2017.12.027
[Indexed for MEDLINE]
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