title: Nonsyntenic genes drive highly dynamic complementation of gene expression in maize hybrids.
abstract: Maize (Zea mays) displays an exceptional level of structural genomic diversity, which is likely unique among higher eukaryotes. In this study, we surveyed how the genetic divergence of two maize inbred lines affects the transcriptomic landscape in four different primary root tissues of their F1-hybrid progeny. An extreme instance of complementation was frequently observed: genes that were expressed in only one parent but in both reciprocal hybrids. This single-parent expression (SPE) pattern was detected for 2341 genes with up to 1287 SPE patterns per tissue. As a consequence, the number of active genes in hybrids exceeded that of their parents in each tissue by >400. SPE patterns are highly dynamic, as illustrated by their excessive degree of tissue specificity (80%). The biological significance of this type of complementation is underpinned by the observation that a disproportionally high number of SPE genes (75 to 82%) is nonsyntenic, as opposed to all expressed genes (36%). These genes likely evolved after the last whole-genome duplication and are therefore younger than the syntenic genes. In summary, SPE genes shape the remarkable gene expression plasticity between root tissues and complementation in maize hybrids, resulting in a tissue-specific increase of active genes in F1-hybrids compared with their inbred parents.
authors.affiliation: Institute of Crop Science and Resource Conservation, Crop Functional Genomics, University of Bonn, 53113 Bonn, Germany.
authors.forename: Anja
authors.identifier: http://orcid.org/0000-0001-6465-2882
authors.initials: A
authors.lastname: Paschold
authors.affiliation: Department of Statistics, Iowa State University, Ames, Iowa 50011-1210.
authors.forename: Nick B
authors.initials: NB
authors.lastname: Larson
authors.affiliation: Institute of Crop Science and Resource Conservation, Crop Functional Genomics, University of Bonn, 53113 Bonn, Germany.
authors.forename: Caroline
authors.initials: C
authors.lastname: Marcon
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska, Lincoln, Nebraska 68588.
authors.forename: James C
authors.initials: JC
authors.lastname: Schnable
authors.affiliation: Department of Agronomy and Center for Plant Genomics, Iowa State University, Ames, Iowa 50011-3650.
authors.forename: Cheng-Ting
authors.initials: CT
authors.lastname: Yeh
authors.affiliation: Department of Molecular Biology, Max-Planck-Institute for Developmental Biology, 72076 Tuebingen, Germany.
authors.forename: Christa
authors.initials: C
authors.lastname: Lanz
authors.affiliation: Department of Statistics, Iowa State University, Ames, Iowa 50011-1210.
authors.forename: Dan
authors.initials: D
authors.lastname: Nettleton
authors.affiliation: Institute for Crop Science, Biostatistics Unit, University of Hohenheim, 70599 Stuttgart, Germany.
authors.forename: Hans-Peter
authors.initials: HP
authors.lastname: Piepho
authors.affiliation: Department of Agronomy and Center for Plant Genomics, Iowa State University, Ames, Iowa 50011-3650.
authors.forename: Patrick S
authors.initials: PS
authors.lastname: Schnable
authors.affiliation: Institute of Crop Science and Resource Conservation, Crop Functional Genomics, University of Bonn, 53113 Bonn, Germany hochholdinger@uni-bonn.de.
authors.forename: Frank
authors.identifier: http://orcid.org/0000-0002-5155-0884
authors.initials: F
authors.lastname: Hochholdinger
mesh_terms: D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D017343:Genes, Plant / Q000235:genetics*; D005838:Genotype; D006823:Hybrid Vigor / Q000235:genetics*; D006824:Hybridization, Genetic; D008390:Markov Chains; D009010:Monte Carlo Method; D018517:Plant Roots / Q000235:genetics; D003313:Zea mays / Q000235:genetics*