Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in <i>Neurospora crassa</i>

Brenna, Andrea; Grimaldi, Benedetto; Filetici, Patrizia; Ballario, Paola

doi:10.1091/mbc.e12-02-0142

Cited by 46 publications

(50 citation statements)

References 40 publications

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“…This suggests that the WCC recruited to the PLRE in the light recruits functional coactivators other than SWI/SNF to modify the PLRE in frq transcription. Additionally and consistent with this, the PLRE is located adjacent to the TSS site and WCC acts on these regions neither by looping of the DNA to bring activators to the TSS, nor by wholesale remodeling of chromatin, although epigenetic modifications have been noted [32], [39], [59]. This suggests that major remodeling and looping induced by SWI/SNF are principal factors distinguishing circadian activators at the C box versus light activators at the PLRE .…”

Section: Discussionmentioning

confidence: 57%

Neurospora WC-1 Recruits SWI/SNF to Remodel frequency and Initiate a Circadian Cycle

et al. 2014

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In the negative feedback loop comprising the Neurospora circadian oscillator, the White Collar Complex (WCC) formed from White Collar-1 (WC-1) and White Collar-2 (WC-2) drives transcription of the circadian pacemaker gene frequency (frq). Although FRQ-dependent repression of WCC has been extensively studied, the mechanism by which the WCC initiates a circadian cycle remains elusive. Structure/function analysis of WC-1 eliminated domains previously thought to transactivate frq expression but instead identified amino acids 100–200 as essential for frq circadian expression. A proteomics-based search for coactivators with WCC uncovered the SWI/SNF (SWItch/Sucrose NonFermentable) complex: SWI/SNF interacts with WCC in vivo and in vitro, binds to the Clock box in the frq promoter, and is required both for circadian remodeling of nucleosomes at frq and for rhythmic frq expression; interestingly, SWI/SNF is not required for light-induced frq expression. These data suggest a model in which WC-1 recruits SWI/SNF to remodel and loop chromatin at frq, thereby activating frq expression to initiate the circadian cycle.

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Section: Discussionmentioning

confidence: 57%

Neurospora WC-1 Recruits SWI/SNF to Remodel frequency and Initiate a Circadian Cycle

et al. 2014

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“…This acetylation is carried out by histone acetyltransferase (HAT) NGF-1, and NGF-1 directly interacts with WC-1. Given that NGF-1 was found to interact with “dark” WC-1/2 heterodimer, a model has been proposed wherein light activation of the WCC/NGF-1 complex leads to conformational changes in WCC (converting it to “light” WCC) which in turn leads to an enhancement of HAT activity of NGF-1 (Brenna et al , 2012). More recently, H3K9me3 DNA methylation by methyltransferase DIM-5 and HP1 has been identified to be a component in the repression of light-induced gene expression (Ruesch et al , 2014), and there is higher light-induced transcription of two genes, frq and vvd , in a dim-5 mutant.…”

Section: N Crassa: a Model Organism For Studying Photobiologymentioning

confidence: 99%

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

Dasgupta

Fuller

Dunlap

et al. 2015

Environmental Microbiology

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Summary Light plays an important role for most organisms on this planet, serving either as a source of energy or information for the adaptation of biological processes to specific times of day. The fungal kingdom is estimated to contain well over a million species, possibly ten-fold more, and it is estimated that a majority of the fungi respond to light, eliciting changes in several physiological characteristics including pathogenesis, development and secondary metabolism. Two model organisms for photobiological studies have taken center-stage over the last few decades – Neurospora crassa and Aspergillus nidulans. In this review, we will first discuss our understanding of the light response in N. crassa, about which the most is known, and will then juxtapose N. crassa with A. nidulans which, as will be described below, provides an excellent template for understanding photosensory cross-talk. Finally, we will end with a commentary on the variability of the light response among other relevant fungi, and how our molecular understanding in the aforementioned model organisms still provides a strong base for dissecting light responses in such species.

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“…T. atroviride contains the classical HDAC classes I, II, and III (28). A connection between light responses and histone acetylation in filamentous fungi has been demonstrated in N. crassa, in which both WC-1 and NGF-1 (orthologous to Gcn5p) physically interact to promote light-induced acetylation of residue K14 of histone H3 associated with the promoter of the al-3 gene (29,30). Recently, it was demonstrated that light activation of WC-1 and -2 is related to nucleosome removal at their target promoters.…”

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confidence: 99%

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

Osorio-Concepción

Cristóbal‐Mondragón

Gutiérrez–Medina

et al. 2017

Appl Environ Microbiol

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Fungal blue-light photoreceptors have been proposed as integrators of light and oxidative stress. However, additional elements participating in the integrative pathway remain to be identified. In Trichoderma atroviride, the blue-light regulator (BLR) proteins BLR-1 and -2 are known to regulate gene transcription, mycelial growth, and asexual development upon illumination, and recent global transcriptional analysis revealed that the histone deacetylase-encoding gene hda-2 is induced by light. Here, by assessing responses to stimuli in wild-type and Δhda-2 backgrounds, we evaluate the role of HDA-2 in the regulation of genes responsive to light and oxidative stress. Δhda-2 strains present reduced growth, misregulation of the con-1 gene, and absence of conidia in response to light and mechanical injury. We found that the expression of hda-2 is BLR-1 dependent and HDA-2 in turn is essential for the transcription of early and late light-responsive genes that include blr-1, indicating a regulatory feedback loop. When subjected to reactive oxygen species (ROS), Δhda-2 mutants display high sensitivity whereas Δblr strains exhibit the opposite phenotype. Consistently, in the presence of ROS, ROS-related genes show high transcription levels in wild-type and Δblr strains but misregulation in Δhda-2 mutants. Finally, chromatin immunoprecipitations of histone H3 acetylated at Lys9/ Lys14 on cat-3 and gst-1 promoters display low accumulation of H3K9K14ac in Δblr and Δhda-2 strains, suggesting indirect regulation of ROS-related genes by HDA-2. Our results point to a mutual dependence between HDA-2 and BLR proteins and reveal the role of these proteins in an intricate gene regulation landscape in response to blue light and ROS.

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Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in Neurospora crassa

Cited by 46 publications

References 40 publications

Neurospora WC-1 Recruits SWI/SNF to Remodel frequency and Initiate a Circadian Cycle

Neurospora WC-1 Recruits SWI/SNF to Remodel frequency and Initiate a Circadian Cycle

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

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

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