Abstract
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.
Highlights
Most organisms and most eukaryotes respond to light in their environment, and do so through the use of proteins specially adapted to respond to light
We have examined the biological significance of VVD photocycle length to photoadaptation and report that a double substitution mutant, 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
Summary
Most organisms and most eukaryotes respond to light in their environment, and do so through the use of proteins specially adapted to respond to light. Such photoreceptor proteins most often sense light through the use of prosthetic groups, chromophores, chosen by evolution for their ability to absorb light of relevant wavelengths, flavins for UV-A and blue light, trans-p-coumaric acid for yellow, retinals for green, and tetrapyrroles for red and infrared [1]. Absorption of light elicits photochemical changes in a chromophore resulting in conformational changes in the photoreceptor protein that initiate the intracellular signaling leading to a biological response, while at the same time leaving the photoreceptor itself unable to respond to a second light stimulus. The general biochemistry of photoreception is well understood [1] and insights into the determinants of photocycle length are emerging as described below, much less is known regarding the functional and adaptive significance of the wide range of known photocycle lengths
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