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.
Here, we report the systematic exploration and modeling of interactions between light and sugar signaling. The data set analyzed explores the interactions of sugar (sucrose) with distinct light qualities (white, blue, red, and far-red) used at different fluence rates (low or high) in etiolated seedlings and mature green plants. Boolean logic was used to model the effect of these carbon/light interactions on three target genes involved in nitrogen assimilation: asparagine synthetase (ASN1 and ASN2) and glutamine synthetase (GLN2). This analysis enabled us to assess the effects of carbon on light-induced genes (GLN2/ASN2) versus light-repressed genes (ASN1) in this pathway. New interactions between carbon and blue-light signaling were discovered, and further connections between red/far-red light and carbon were modeled. Overall, light was able to override carbon as a major regulator of ASN1 and GLN2 in etiolated seedlings. By contrast, carbon overrides light as the major regulator of GLN2 and ASN2 in light-grown plants. Specific examples include the following: Carbon attenuated the blue-light induction of GLN2 in etiolated seedlings and also attenuated the white-, blue-, and red-light induction of GLN2 and ASN2 in light-grown plants. By contrast, carbon potentiated far-red-light induction of GLN2 and ASN2 in light-grown plants. Depending on the fluence rate of far-red light, carbon either attenuated or potentiated light repression of ASN1 in light-grown plants. These studies indicate the interaction of carbon with blue, red, and far-red-light signaling and set the stage for further investigation into modeling this complex web of interacting pathways using systems biology approaches.Light is an important environmental signal that is directly perceived by the plant through photoreceptors and is essential for driving photosynthesis. As such, light provides the reducing power for carbon fixation, nitrogen assimilation, amino acid biosynthesis, and other necessary metabolic pathways. Information about light quality, intensity, and duration is measured through numerous photoreceptors (Mancinelli, 1994;Smith, 1994). Phytochromes are the primary red-light photoreceptors. The blue-light, UV-A/B photoreceptors include the cryptochromes, phototropin, and other yet unidentified photoreceptors (for review, see Briggs and Huala, 1999). The various qualities of light perceived through these photoreceptors control diverse developmental programs in plants such as seed germination, hypocotyl elongation, shade avoidance, circadian rhythms, flowering, chloroplast differentiation, and cotyledon expansion (for review, see Fankhauser and Chory, 1997;Briggs and Huala, 1999;Neff et al., 2000). The most well-characterized photoreceptors are the phytochromes. In Arabidopsis, five different phytochromes exist (phyA-E), each containing both overlapping and unique biological functions. PhyA is predominately involved in physiological responses to continuous far-red light, whereas phyB is involved in responses to red light. Additionally, phyA me...
Background: Light and carbon are two important interacting signals affecting plant growth and development. The mechanism(s) and/or genes involved in sensing and/or mediating the signaling pathways involving these interactions are unknown. This study integrates genetic, genomic and systems approaches to identify a genetically perturbed gene network that is regulated by the interaction of carbon and light signaling in Arabidopsis.
The photosystem II reaction center chlorophyll protein D2, is encoded by the chloroplast gene psbD. PsbD is transcribed from at least three different promoters, one which is activated by high fluence blue light. Sequences within 130 base pairs (bp) of the psbD blue light-responsive promoter (BLRP) are highly conserved in higher plants. In this study, the structure of the psbD BLRP was analyzed in detail using deletion and site-directed mutagenesis and in vitro transcription. Deletion analysis showed that a 53-bp DNA region of the psbD BLRP, from ؊57 to ؊5, was sufficient for transcription in vitro. Mutation of a putative prokaryotic ؊10 element (TATTCT) located from ؊7 to ؊12 inhibited transcription from the psbD BLRP. In contrast, mutation of a putative prokaryotic ؊35 element, had no influence on transcription. Mutation of a TATATA sequence located between the barley psbA ؊10 and ؊35 elements significantly reduced transcription from this promoter. However, site-directed mutation of sequences located between ؊35 and ؊10 had no effect on transcription from the psbD BLRP. Transcription from the psbD BLRP was previously shown to require a 22-bp sequence, termed the AAG-box, located between ؊36 and ؊57. The AAG-box specifically binds the protein complex AGF. Site-directed mutagenesis identified two different sequence motifs in the AAGbox that are important for transcription in vitro. Based on these results, we propose that positive factors bind to the AAG-box and interact with the chloroplast-encoded RNA polymerase to promote transcription from the psbD BLRP. Transcription from the psbD BLRP is thus similar to type II bacterial promoters that use activating proteins to stimulate transcription. Transcription of the psbD BLRP was ϳ6.5-fold greater in plastid extracts from illuminated versus dark-grown plants. This suggests that light-induced activation of this promoter in vivo involves factors interacting with the 53-bp psbD BLRP in vitro.Photosystem II contains at least four plastid-encoded chlorophyll apoproteins (D1, D2, CP47, CP43). Among these, D2 and D1 form a heterodimer, which houses the photosystem II reaction center chlorophyll P680. D1 and D2 are relatively unstable in illuminated plants (1-5). Therefore, synthesis of D1 and D2 is selectively elevated in mature barley chloroplasts in order to maintain the levels of these subunits and PSII function (5, 6). Maintenance of high rates of D1 and D2 synthesis in mature barley chloroplasts is paralleled by the retention of elevated levels of psbA and psbD mRNAs, which encode these proteins (6 -8). D1 mRNA levels remain high in mature barley chloroplasts primarily due to the high stability of its mRNA, although transcription from psbA is also increased by light (9 -12). Maintenance of high levels of psbD mRNA results primarily from the activation of psbD transcription by blue light combined with a small increase in RNA stability (5, 13).The chloroplast genome in most higher plants is circular and ranges in size from 120 to 217 kilobase pairs (reviewed in Refs. 14 ...
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