Biological photosensors

This issue of Photochemical & Photobiological Sciences is devoted to biological photosensors. All the articles have been refereed and edited according to routine journal procedure.

Various photosensors have evolved that monitor the environmental light quality, quantity, and direction. Photosensors allow organisms the optimal use of the light conditions for growth and development and/or the protection from light damage. This is an area of very rapid development in the last few years. One of the most exciting developments has been the molecular identification of the long sought after blue-light detecting photosensors in plants and other organisms, including bacteria and fungi. Based on wonderfully carried out experiments on the phototropic curvature of plant organs, Darwin concluded in 1881 in his book The Power of Movement in Plants that the photoreceptor for plant phototropism was different from that for photosynthesis.¹ In 1886, Sachs² showed that wavelengths between 400 and 500 nm were responsible for the response. The molecular identification 120 years later of the cryptochromes and the LOV (light, oxygen, or voltage) sensing domains in phototropins, controlling among other photoresponses coleoptile photomovement, has introduced new paradigms in this area of knowledge. The chromophore, flavin mononucleotide (FMN) in the LOV domains and flavin adenine dinucleotide (FAD) in cryptochromes, is non-covalently bound to the protein.³ This is contrary to the then known photosensors phytochromes, rhodopsins, and photoactive yellow protein in each of which the chromophore is covalently bound to the protein. The primary photochemical reaction is not a cis–trans isomerisation, contrary to the case of the open-chain tetrapyrrole in phytochromes, of retinal in rhodopsins, and of p-coumaric anion in photoactive yellow protein. In the FMN-containing LOV domains, the FMN triplet state formed upon blue light excitation reacts with a nearby cysteine, forming a long-lived adduct which changes the protein conformation and relatively slowly returns to the parent state. This is the first discovery of the participation of an excited triplet state in a life-essential reaction.

A very exciting development in the last decade has been the accumulated evidence, which has shown that photoreception in the vertebrate eye is not confined to the rods and cones. Non-rod, non-cone ocular photoreceptors in mammals and fish perform the photoperception centred at 480 nm. These photosensors regulate, among other reactions, the circadian system and a pupillary light reflex. The retinal protein melanopsin is the strongest candidate for the blue-light sensor in mammals and fish.⁴ The discovery of the use by birds of their UV vision for mate selection⁵ has also changed the views about the diversity of roles played by retinal sensors.⁶

New developments in the area of retinal sensor proteins have included the discovery of channel-1 (ChR1) and channel-2 (ChR2) retinal proteins in Chlamydomonas reinhardtii, originally called chlamyopsins Cop3 and Cop4.⁷ On the basis of photoinduced electrical currents it was proposed that ChR2 may be the sensory photoreceptor preferentially used when the cells are exposed to dim light for longer time periods. From the fact that ChR2 triggers much larger photocurrents than ChR1 it was concluded that the degradation of ChR2 at higher light irradiances protects cells from the detrimental effects of continuously inward flowing cations, especially protons and calcium. This study revealed also that light signal transduction in C. reinhardtii is very likely triggered by ion fluxes.⁷

Another major finding in the area of blue-light sensors was the discovery of photoactivated adenylyl cyclase (PAC), the blue-light receptor flavoprotein (containing as co-factor FAD) identified as the photoreceptor for photoavoidance in the unicellular flagellate, Euglena gracilis.⁸ It was also recently shown that the flavoprotein AppA from the purple bacterium Rhodobacter sphaeroides represents a new class of photoreceptor that controls photosynthesis gene expression in response to blue-light intensity, as well as to changes in the cellular redox state. AppA was shown to mediate these effects by deactivating the photosynthesis gene repressor, PpsR.⁹ Recently, a novel photocycle for this sensor was proposed; photochemical excitation of the FAD co-factor may result in strengthening of a hydrogen bond between the flavin and Tyr 21 leading to a stable local conformational change in AppA.¹⁰ FAD has also been shown to be the co-factor in white collar-1 (WC-1) proposed to be the blue-light photoreceptor for the circadian clock and other light responses in Neurospora,¹¹ albeit in this case FAD is hosted by a phototropin-like LOV domain.

Other recent exciting discoveries have been (i) chimeric proteins containing both a phytochrome module binding an open-chain tetrapyrrole and a LOV domain hosting a flavin,¹² that explains the additive character of the red- and blue-signals in Adiantum, (ii) the finding of phytochromes in cyanobacteria,¹³ and in other phototropic and even heterotrophic bacteria,^14,15 (iii) the photoinduced cytosol–nucleus translocation of phytochrome¹⁶ and the finding of the long sought after protein interacting partners of phytochrome^17,18 as well as (iv) the new modes of attachment of some open-chain tetrapyrrol chromophores to the apoprotein.¹⁹ A novel phototropic response of the seed pods of Brassica napus L. to supplementary UV-A and UV-B radiation was reported and the possible involvement of a new photosensor was suggested.²⁰

Last, but not least, crystallisation of several sensory proteins and particular domains, such as LOV domains,²¹ rhodopsin,²² sensory rhodopsin with its transducer²³ as well as of some of the photoproducts²⁴ resulting from excitation of the sensory pigments, has fundamentally added to the knowledge of the structure-function relationship in photosensors.

The contributions to this special Photochem. Photobiol. Sci. issue cover several of the above-mentioned aspects of biological photosensors using different approaches. These approaches include physiological observations, molecular biology studies, the effect of mutations, studies of the sensor phototransformations in vitro by transient absorption, fluorescence, electron spin resonance, X-Ray, Fourier-transform, infra-red and Raman spectroscopies, phylogenetic analysis, and others. Several contributions demonstrate the synergistic effect of multidisciplinary approaches to solve the challenging questions in this area. In many of the contributions open questions are posed and future research directions to answer these are suggested.

We are very glad to have obtained such an excellent set of papers handling almost all known photosensors and we hope that this collection will serve as a guide and inspiration for future activities in these fascinating aspects of photobiology and photochemistry.

References

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