SignificanceOur study exploits time—the relatively unexplored fourth dimension of gene regulatory networks (GRNs)—to learn the temporal transcriptional logic underlying dynamic nitrogen (N) signaling in plants. We introduce several conceptual innovations to the analysis of time-series data in the area of predictive GRNs. Our resulting network now provides the “transcriptional logic” for transcription factor perturbations aimed at improving N-use efficiency, an important issue for global food production in marginal soils and for sustainable agriculture. More broadly, the combination of the time-based approaches we develop and deploy can be applied to uncover the temporal “transcriptional logic” for any response system in biology, agriculture, or medicine.

Significance Cellular signals evoke rapid and broad changes in gene regulatory networks. To uncover these network dynamics, we developed an approach able to monitor primary targets of a transcription factor (TF) based solely on gene regulation, in the absence of detectable binding. This enabled us to follow the transient propagation of a nitrogen (N) nutrient signal as a direct impact of the master TF Basic Leucine Zipper 1 (bZIP1). Unexpectedly, the largest class of primary targets that exhibit transient associations with bZIP1 is uniquely relevant to the rapid and dynamic propagation of the N signal. Our ability to uncover this transient network architecture has revealed the “dark matter” of dynamic N nutrient signaling in plants that has previously eluded detection.

BackgroundHistone methylation modifies the epigenetic state of target genes to regulate gene expression in the context of developmental and environmental changes. Previously, we used a positive genetic screen to identify an Arabidopsis mutant, cli186, which was impaired in carbon and light signaling. Here, we report a deletion of the Arabidopsis histone methyltransferase SDG8 in this mutant (renamed sdg8-5), which provides a unique opportunity to study the global function of a specific histone methyltransferase within a multicellular organism.ResultsTo assess the specific role of SDG8, we examine how the global histone methylation patterns and transcriptome were altered in the sdg8-5 deletion mutant compared to wild type, within the context of transient light and carbon treatments. Our results reveal that the sdg8 deletion is associated with a significant reduction of H3K36me3, preferentially towards the 3′ end of the gene body, accompanied by a reduction in gene expression. We uncover 728 direct targets of SDG8 that have altered methylation in the sdg8-5 mutant and are also bound by SDG8. As a group, this set of SDG8 targets is enriched in specific biological processes including defense, photosynthesis, nutrient metabolism and energy metabolism. Importantly, 64% of these SDG8 targets are responsive to light and/or carbon signals.ConclusionsThe histone methyltransferase SDG8 functions to regulate the H3K36 methylation of histones associated with gene bodies in Arabidopsis. The H3K36me3 mark in turn is associated with high-level expression of a specific set of light and/or carbon responsive genes involved in photosynthesis, metabolism and energy production.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0640-2) contains supplementary material, which is available to authorized users.

SummaryShoot apical meristem (SAM) structure varies markedly within the land plants. The SAMs of many seedless vascular plants contain a conspicuous inverted, pyramidal cell called the apical cell (AC), which is unidentified in angiosperms.In this study, we use transcriptomic sequencing with precise laser microdissections of meristem subdomains to define the molecular signatures of anatomically distinct zones from the AC-type SAMs of a lycophyte (Selaginella moellendorffii) and a monilophyte (Equisetum arvense). The two model species for this study represent vascular plant lineages that diverged > 400 million yr ago.Our data comprise comprehensive molecular signatures for the distinct subdomains within AC-type SAMs, an anatomical anomaly whose functional significance has been debated in the botanical literature for over two centuries.Moreover, our data provide molecular support for distinct gene expression programs between the AC-type SAMs of Selaginella and Equisetum, as compared with the SAM transcriptome of the angiosperm maize. The results are discussed in light of the functional significance and evolutionary success of the AC-type SAM within the embryophytes.

The evolution of novel features, such as eyes or wings, that allow organisms to exploit their environment in new ways can lead to increased diversification rates. Therefore, understanding the genetic and developmental mechanisms involved in the origin of these key innovations has long been of interest to evolutionary biologists. In flowering plants, floral nectar spurs are a prime example of a key innovation, with the independent evolution of spurs associated with increased diversification rates in multiple angiosperm lineages due to their ability to promote reproductive isolation via pollinator specialization. As none of the traditional plant model taxa have nectar spurs, little is known about the genetic and developmental basis of this trait. Nectar spurs are a defining feature of the columbine genus Aquilegia (Ranunculaceae), a lineage that has experienced a relatively recent and rapid radiation. We use a combination of genetic mapping, gene expression analyses, and functional assays to identify a gene crucial for nectar spur development, POPOVICH (POP), which encodes a C2H2 zinc-finger transcription factor. POP plays a central role in regulating cell proliferation in the Aquilegia petal during the early phase (phase I) of spur development and also appears to be necessary for the subsequent development of nectaries. The identification of POP opens up numerous avenues for continued scientific exploration, including further elucidating of the genetic pathway of which it is a part, determining its role in the initial evolution of the Aquilegia nectar spur, and examining its potential role in the subsequent evolution of diverse spur morphologies across the genus.