Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids.

The dominance model of heterosis explains the superior performance of F1-hybrids via the complementation of deleterious alleles by beneficial alleles in many genes. Genes active in one parent but inactive in the second lead to single-parent expression (SPE) complementation in maize (Zea mays L.) hybrids. In this study, SPE complementation resulted in approximately 700 additionally active genes in different tissues of genetically diverse maize hybrids on average. We established that the number of SPE genes is significantly associated with mid-parent heterosis (MPH) for all surveyed phenotypic traits. In addition, we highlighted that maternally (SPE_B) and paternally (SPE_X) active SPE genes enriched in gene co-expression modules are highly correlated within each SPE type but separated between these two SPE types. While SPE_B-enriched co-expression modules are positively correlated with phenotypic traits, SPE_X-enriched modules displayed a negative correlation. Gene ontology term enrichment analyses indicated that SPE_B patterns are associated with growth and development, whereas SPE_X patterns are enriched in defense and stress response. In summary, these results link the degree of phenotypic MPH to the prevalence of gene expression complementation observed by SPE, supporting the notion that hybrids benefit from SPE complementation via its role in coordinating maize development in fluctuating environments.

Robust non-syntenic gene expression patterns in diverse maize hybrids during root development.

Distantly related maize (Zea mays L.) inbred lines exhibit an exceptional degree of structural genomic diversity, which is probably unique among plants. This study systematically investigated the developmental and genotype-dependent regulation of the primary root transcriptomes of a genetically diverse panel of maize F1-hybrids and their parental inbred lines. While we observed substantial transcriptomic changes during primary root development, we demonstrated that hybrid-associated gene expression patterns, including differential, non-additive, and allele-specific transcriptome profiles, are particularly robust to these developmental fluctuations. For instance, differentially expressed genes with preferential expression in hybrids were highly conserved during development in comparison to their parental counterparts. Similarly, in hybrids a major proportion of non-additively expressed genes with expression levels between the parental values were particularly conserved during development. Importantly, in these expression patterns non-syntenic genes that evolved after the separation of the maize and sorghum lineages were systemically enriched. Furthermore, non-syntenic genes were substantially linked to the conservation of all surveyed gene expression patterns during primary root development. Among all F1-hybrids, between ~40% of the non-syntenic genes with unexpected allelic expression ratios and ~60% of the non-syntenic differentially and non-additively expressed genes were conserved and therefore robust to developmental changes. Hence, the enrichment of non-syntenic genes during primary root development might be involved in the developmental adaptation of maize roots and thus the superior performance of hybrids.

Transcriptomic data from panarthropods shed new light on the evolution of insulator binding proteins in insects : Insect insulator proteins.

BACKGROUND: Body plan development in multi-cellular organisms is largely determined by homeotic genes. Expression of homeotic genes, in turn, is partially regulated by insulator binding proteins (IBPs). While only a few enhancer blocking IBPs have been identified in vertebrates, the common fruit fly Drosophila melanogaster harbors at least twelve different enhancer blocking IBPs. We screened recently compiled insect transcriptomes from the 1KITE project and genomic and transcriptomic data from public databases, aiming to trace the origin of IBPs in insects and other arthropods. RESULTS: Our study shows that the last common ancestor of insects (Hexapoda) already possessed a substantial number of IBPs. Specifically, of the known twelve insect IBPs, at least three (i.e., CP190, Su(Hw), and CTCF) already existed prior to the evolution of insects. Furthermore we found GAF orthologs in early branching insect orders, including Zygentoma (silverfish and firebrats) and Diplura (two-pronged bristletails). Mod(mdg4) is most likely a derived feature of Neoptera, while Pita is likely an evolutionary novelty of holometabolous insects. Zw5 appears to be restricted to schizophoran flies, whereas BEAF-32, ZIPIC and the Elba complex, are probably unique to the genus Drosophila. Selection models indicate that insect IBPs evolved under neutral or purifying selection. CONCLUSIONS: Our results suggest that a substantial number of IBPs either pre-date the evolution of insects or evolved early during insect evolution. This suggests an evolutionary history of insulator binding proteins in insects different to that previously thought. Moreover, our study demonstrates the versatility of the 1KITE transcriptomic data for comparative analyses in insects and other arthropods.

Transcriptome profiling of barley and tomato shoot and root meristems unravels physiological variations underlying photoperiodic sensitivity.

The average sowing date of crops in temperate climate zones has been shifted forwards by several days, resulting in a changed photoperiod regime at the emergence stage. In the present study, we performed a global transcriptome profiling of plant development genes in the seedling stage of root and shoot apical meristems of a photoperiod-sensitive species (barley) and a photoperiod insensitive species (tomato) in short-day conditions (8h). Variant expression indicated differences in physiological development under this short day-length regime between species and tissues. The barley tissue transcriptome revealed reduced differentiation compared to tomato. In addition, decreased photosynthetic activity was observed in barley transcriptome and leaf chlorophyll content under 8h conditions, indicating a slower physiological development of shoot meristems than in tomatoes. The photomorphogenesis controlling cryptochrome gene cry1, with an effect on physiological differentiation, showed an underexpression in barley compared to tomato shoot meristems. This might lead to a cascade of suspended sink-source activities, which ultimately delay organ development and differentiation in barley shoot meristems under short photoperiods.

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

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.