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The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation.

ABSTRACT: The light response in Neurospora is mediated by the photoreceptor and circadian transcription factor White Collar Complex (WCC). The expression rate of the WCC target genes adapts in daylight and remains refractory to moonlight, despite the extraordinary light sensitivity of the WCC. To explain this photoadaptation, feedback inhibition by the WCC interaction partner VIVID (VVD) has been invoked. Here we show through data-driven mathematical modeling that VVD allows Neurospora to detect relative changes in light intensity. To achieve this behavior, VVD acts as an inhibitor of WCC-driven gene expression and, at the same time, as a positive regulator that maintains the responsiveness of the photosystem. Our data indicate that this paradoxical function is realized by a futile cycle that involves the light-induced sequestration of active WCC by VVD and the replenishment of the activatable WCC pool through the decay of the photoactivated state. Our quantitative study uncovers a novel network motif for achieving sensory adaptation and defines a core input module of the circadian clock in Neurospora.

SUBMITTER: Gin E

PROVIDER: S-EPMC4039372 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

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The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation.

Gin Elan E Diernfellner Axel C R AC Brunner Michael M Höfer Thomas T

Molecular systems biology 20130528

The light response in Neurospora is mediated by the photoreceptor and circadian transcription factor White Collar Complex (WCC). The expression rate of the WCC target genes adapts in daylight and remains refractory to moonlight, despite the extraordinary light sensitivity of the WCC. To explain this photoadaptation, feedback inhibition by the WCC interaction partner VIVID (VVD) has been invoked. Here we show through data-driven mathematical modeling that VVD allows Neurospora to detect relative ...[more]

PMID: 23712010

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Project description:Most organisms on earth sense light through the use of chromophore-bearing photoreceptive proteins with distinct and characteristic photocycle lengths, yet the biological significance of this adduct decay length is neither understood nor has been tested. In the filamentous fungus Neurospora crassa VIVID (VVD) is a critical player in the process of photoadaptation, the attenuation of light-induced responses and the ability to maintain photosensitivity in response to changing light intensities. Detailed in vitro analysis of the photochemistry of the blue light sensing, FAD binding, LOV domain of VVD has revealed residues around the site of photo-adduct formation that influence the stability of the adduct state (light state), that is, altering the photocycle length. We have examined the biological significance of VVD photocycle length to photoadaptation and report that a double substitution mutant (vvdI74VI85V), previously shown to have a very fast light to dark state reversion in vitro, shows significantly reduced interaction with the White Collar Complex (WCC) resulting in a substantial photoadaptation defect. This reduced interaction impacts photoreceptor transcription factor WHITE COLLAR-1 (WC-1) protein stability when N. crassa is exposed to light: The fast-reverting mutant VVD is unable to form a dynamic VVD-WCC pool of the size required for photoadaptation as assayed both by attenuation of gene expression and the ability to respond to increasing light intensity. Additionally, transcription of the clock gene frequency (frq) is sensitive to changing light intensity in a wild-type strain but not in the fast photo-reversion mutant indicating that the establishment of this dynamic VVD-WCC pool is essential in general photobiology and circadian biology. Thus, VVD photocycle length appears sculpted to establish a VVD-WCC reservoir of sufficient size to sustain photoadaptation while maintaining sensitivity to changing light intensity. The great diversity in photocycle kinetics among photoreceptors may be viewed as reflecting adaptive responses to specific and salient tasks required by organisms to respond to different photic environments.

Dataset Information

The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation.

Publications

The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation.

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