Light on Algal Gene Expression
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COMMENTARY Shedding (blue) light on algal gene expression Aba Losi*† and Wolfgang Ga¨ rtner‡ *Department of Physics, University of Parma, Viale G. P. Usberti 7A, 43100 Parma, Italy; and ‡Max Planck Institute for Bioinorganic Chemistry, Stiftstrasse 34-36, D-45470 Mu¨lheim, Germany ight in the blue region of the spectrum [blue light (BL), 400– a b 480 nm] is an ubiquitous envi- bZIP LOV AUREO ronmental signal. BL can pene- Ltrate marine water to a depth greater LOV PAS PAS ZnF WC-1a than all other wavelengths, up to the Ϸ limits of the photic zone ( 1,500 m LOV HtH ELI_04755 depth) and may be linked to the evolu- tion of photosynthesis (1). BL is also HtH LOV Tmden_2087 potentially dangerous because it is readily absorbed by intracellular photo- RR LOV GAF HtH NP0654A sensitizers (e.g., porphyrin derivatives and flavins) (2). Therefore, living organ- Fig. 1. Architecture of selected LOV proteins and structure of a PAS-HtH protein. (a) Examples of LOV isms detect and respond to BL either by proteins with DNA-binding domains. From the top: AUREO from V. frigida; white-collar 1a (WC-1a) from photoprotection mechanisms or by maxi- Phycomyces blakesleeanus; helix–turn–helix (HtH) proteins from Erythrobacter litoralis (ELI04755) and mally exploiting this environmental in- Thiomicrospira denitrificans (Tmden2087); and opsin activator from the archaeon Natronomonas phara- put, e.g., to entrain circadian rhythms onis. ZnF, zinc finger; RR, response regulator; GAF, domain present in phytochrome and cGMP-specific and optimize photosynthetic efficiency. phosphodiesterases. (b) A possible conformation for a DNA-binding LOV protein. Shown is the crystal Given its high penetrability, BL is of structure of the protein TraR from Agrobacterium tumefaciens, complexed with DNA (Protein Data Bank utmost importance for marine species, ID code 1H0M) (16). The N-terminal PAS-like domain (in blue) binds N-(3-oxooctanoyl)-L-homoserine but little is known about the BL detec- lactone (in black) in a similar position as FMN within LOV domains. Dimerization is mediated both by the HtH (in red) and by the PAS-like domain, via the helical regions flanking the PAS core. tion mechanisms of sea plants. The AU- REOCHROMES (AUREOs) described by Takahashi and colleagues (3) in a frigida. This represents an important sufficient for such light activation, which recent issue of PNAS are the first BL step in the understanding of photo- leads us to question the role of LOV1. receptors identified in stramenopile al- receptor systems and BL-driven re- In all other LOV proteins, only one gae and show a clear link to the photo- sponses in these marine plants, which LOV domain is present, coupled to a morphogenesis of these organisms. originated by means of secondary endo- broad variety of effector functions, such The existence of BL photoreceptors symbiosis from red algal symbionts and as kinases and transcriptional regulators, in plants has long been proposed, but nonphotosynthetic eukaryotic hosts. The constituting modular systems presumably only recently have the flavin-binding finding of AUREOs could provide new switchable by light. Other than phot, cryptochromes and phototropins (phot) information on the phylogenetic link been characterized at a molecular level fungal BL sensors of the LOV family between these plants and other (4). Phot are conserved in higher plants are the best understood systems (9), but eukaryotes. and in several lower plant species, where recently, bacterial LOV proteins have V. frigida hosts two AUREOs they mediate a variety of BL responses also begun to be examined. YtvA from (AUREO1 and AUREO2) composed (e.g., phototropism, gametogenesis) (5). Bacillus subtilis is the first bacterial pro- What is making this research field in- of an N-terminal, DNA-binding basic tein for which the LOV paradigm has creasingly exciting is the awareness that leucine zipper (bZIP) motif and a C- been demonstrated, followed by LOV BL photoreceptors are widespread terminal LOV domain (Fig. 1a), but it proteins from proteobacteria and cy- among distant taxa and are well re- does not possess phot-encoding genes. anobacteria (7, 10). At the functional presented in both eukaryotes and pro- Conversely, a search through various level, light excitation increases the level karyotes (4, 6, 7). The common feature plant genomes rules out AUREO-like of phosphorylation in bacterial LOV conserved among phot-related proteins proteins in green plants. AUREO1 kinases, showing that a typical bacterial is the light-sensing, flavin-binding light– shows the spectral features and light- two-component system can be BL- oxygen–voltage (LOV) domain, a small induced reactions typical of the well activated (10–12). In Brucella abortus, protein unit of Ϸ110 aa belonging to known LOV paradigm. LOV domains this light-regulated kinase activity was the PerArntSim (PAS) superfamily (8). noncovalently bind a fully oxidized fla- importantly linked to the infectivity of Takahashi and colleagues (3) now show vin mononucleotide (FMN) molecule in the bacterium for mammalian cells (12). the presence of LOV proteins in the the dark, absorbing maximally at 447 In Caulobacter crescentus, a LOV kinase photosynthetic stramenopiles Vaucheria nm. BL triggers a photocycle that in- is the BL receptor that regulates cell– frigida and Fucus distichus and in a volves the transient formation of an cell attachment (10). Takahashi and diatomean species, Thalassiosira pseud- FMN–cysteine C(4a) thiol adduct, onana. These novel phot-related pro- slowly reverting to the dark state on teins have been named AUREO in a seconds-to-hours timescale (7). Author contributions: A.L. and W.G. wrote the paper. reference to the typical golden-yellow The architecture of AUREO under- The authors declare no conflict of interest. color of stramenopiles. The authors scores the modularity of LOV proteins. See companion article on page 19625 in issue 49 of volume identified the sequence of AUREOs, In phot, two LOV domains (LOV1 and 104. their photoinduced reactions, and their LOV2) are coupled to a kinase effector †To whom correspondence should be addressed. E-mail: light-driven regulation of gene expres- module whose activity is enhanced upon aba.losi@fis.unipr.it. sion and photomorphogenesis in V. light activation. LOV2 is necessary and © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0710523105 PNAS ͉ January 8, 2008 ͉ vol. 105 ͉ no. 1 ͉ 7–8 Downloaded by guest on September 28, 2021 colleagues al. (3) show that BL treat- HtH transcriptional regulators also bind nal transduction (7). The ability to ment of AUREO1 strongly enhances to DNA as dimers or multimers and addi- homo- or heterodimerize is a feature binding to its target DNA sequence, im- tionally contain a sensing/acceptor do- typical of PAS domains and has also plying that AUREO1 functions as a BL- main, typically a PAS (e.g., in TraR) (16) been observed, in some cases, for LOV regulated transcriptional factor. The link or a response regulator domain (e.g., in domains, probably with functional signif- icance (7). It has been suggested that to a photomorphogenetic function for NarL) (17). Dimerization allows target the -scaffold mediates dimerization AUREO 1—in this case BL-induced site recognition, and activation of the sen- sor domain is thought to unmask binding and also is involved in direct interac- branching during plant development—is tions with partner domains and/or with elegantly established by RNAi experi- sites for DNA through alternative confor- mation of the interdomain linker region. the N- and C-terminal regions flanking ments. AUREO2 does not bind a flavin the LOV core, thus representing a com- The conformational flexibility of the chromophore in vitro and appears to petitive surface for multiple possible linker region is underscored by the struc- function as a secondary switch during partners. In phot-LOV2, the helical ture of the TraR dimer bound to DNA, BL-induced branching. linker region folds beneath the - scaffold and becomes unfolded upon AUREO: Not Just Another Leucine Zipper BL photoreceptors are light activation (19). In the crystal struc- To our knowledge, AUREOs are the ture of YtvA–LOV, the linker instead protrudes outside of the LOV core, and first example of a PAS domain coupled widespread among the -scaffold is engaged in the tight to a bZIP DNA-binding motif. More LOV–LOV dimer (20). In full-length commonly associated with PAS domains distant taxa and are YtvA, the -scaffold is involved in intra- are basic helix–loop–helix (bHlH), protein/interdomain interactions, and helix–turn–helix (HtH), and Zn-finger well represented in both there is no light-induced unfolding of motifs. All of these proteins contain the linker, whose exact orientation re- helical dimerization regions, which are eukaryotes and mains to be determined (21). essential for DNA recognition and bind- prokaryotes. Light-Switching of Genes by the ing. bZIPs dimerize through the stereo- Versatile LOV Module typical leucine zipper sequence, forming The photomorphogenesis process de- a coiled-coil structure, whereas at the N scribed for V. frigida by Takahashi and terminus, the basic region interacts with where the two PAS-like domains are ar- ranged asymmetrically to each other be- colleagues (3) relies on BL-regulated DNA via a classical scissor-like motif. direct activation of genes by AUREO, Through hetero- and/or homodimeriza- cause of a different orientation of the linker (Fig. 1b). Finally, we note that fun- eventually resulting in a specific growth tion networks, bZIP proteins increase gal white-collar 1 (WC-1; see Fig. 1), a pattern. Up to now, no DNA-binding their sequence specificity (13). It is also bacterial LOV-transcriptional regulator Zn-finger photoreceptor LOV protein, is has been studied, although such regula- becoming clear that high specificity is active as a dimer, where dimerization is acquired with the cooperation of addi- tors are well represented within the mediated by the nonphotosensing PAS group (7) and, together with AUREOs, tional proteins or domains, forming the domains (18).