Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in Neurospora

Abstract

Light is an important environmental cue that affects physiology and development of Neurospora crassa. The light-sensing transcription factor (TF) WCC, which consists of the GATA-family TFs WC1 and WC2, is required for light-dependent transcription. SUB1, another GATA-family TF, is not a photoreceptor but has also been implicated in light-inducible gene expression. To assess regulation and organization of the network of light-inducible genes, we analyzed the roles of WCC and SUB1 in light-induced transcription and nucleosome remodeling. We show that SUB1 co-regulates a fraction of light-inducible genes together with the WCC. WCC induces nucleosome eviction at its binding sites. Chromatin remodeling is facilitated by SUB1 but SUB1 cannot activate light-inducible genes in the absence of WCC. We identified FF7, a TF with a putative O-acetyl transferase domain, as an interaction partner of SUB1 and show their cooperation in regulation of a fraction of light-inducible and a much larger number of non light-inducible genes. Our data suggest that WCC acts as a general switch for light-induced chromatin remodeling and gene expression. SUB1 and FF7 synergistically determine the extent of light-induction of target genes in common with WCC but have in addition a role in transcription regulation beyond light-induced gene expression.

TheNeurosporaTranscription Factor ADV-1 Transduces Light Signals and Temporal Information to Control Rhythmic Expression of Genes Involved in Cell Fusion

“…Combining genes from all time points revealed that ADV-1 potentially controls the expression of 1029 unique gene targets (Table S3), representing ∼10% of the predicted 9730 N. crassa genes. Several of the predicted ADV-1 target genes are also predicted targets of the WCC, and/or of two downstream TFs that are direct targets of the WCC, CSP-1, and SUB-1, suggesting combinatorial control for these genes (Smith et al 2010; Sancar et al 2011, 2015a) (Table S3). The distribution of ADV-1 binding peaks for each time point, based on their positions relative to the transcriptional start site from the annotated genes in the N. crassa genome (http://www.broad.mit.edu/annotation/genome/neurospora/), were examined (Figure S2A).…”

“…Furthermore, the poor overlap between the differentially expressed genes and the direct targets of ADV-1 revealed that binding does not necessarily equate with a change in mRNA levels. This may be due to binding and compensation by other TFs, such as WCC, SUB-1, and CSP-1 (Sancar et al 2011, 2015a; Smith et al 2010) (Table S3), and/or may reflect that regulatory mechanisms other than light are also important for controlling the expression of these ADV-1 targets.…”

“…These early light-induced TFs would in turn control the expression of late light-responsive genes. Consistent with this model, the sub-1 gene, encoding a GATA-family TF, is an early light-induced gene whose promoter is bound by the WCC, and deletion of sub-1 alters light responses for many late light-inducible genes (Chen et al 2009; Smith et al 2010; Sancar et al 2015a). Furthermore, regulatory hierarchy can also explain evening-phase-specific gene expression.…”

Seeing the world differently: variability in the photosensory mechanisms of two model fungi

“…Additionally, a certain subset of genes in a sub - 1 mutant have altered amplitude of induction which suggests that factors other than SUB-1 are required for activating these genes, and that SUB-1 takes up an ancillary role as a modulator of gene expression (Chen et al , 2010a). This ancillary role was brought to the fore when it was found that for a subset of light-induced genes, although WCC was primarily essential for induction, SUB-1 facilitates chromatin remodeling by interacting with a transcription factor FF-7 (containing a putative O-acetyl transferase domain) in combination with WCC, thereby modulating the extent of induction of their common target genes (Sancar et al , 2015). Interestingly, SUB-1 and FF-7 regulate the expression a much greater fraction of non-light induced genes, suggesting that this might be a general transcription regulatory module that is co-opted during the light response.…”

Histone Deacetylase HDA-2 Regulates Trichoderma atroviride Growth, Conidiation, Blue Light Perception, and Oxidative Stress Responses

“…Recently, it was demonstrated that light activation of WC-1 and -2 is related to nucleosome removal at their target promoters. Furthermore, sub-1 (a WC-1-and -2-dependent gene that codes for a GATA-type transcription factor) is necessary for efficient remodeling of certain nucleosomes (31).…”