Functional conservation of light, oxygen, or voltage domains in light sensing

In Neurospora, the flavin adenine dinucleotide-containing protein WHITE COLLAR-1 is the blue-light photoreceptor for the circadian clock and other light responses. The putative chromophore-binding domain of WC-1, its light, oxygen, or voltage (LOV) domain, is similar to the LOV domains found in the plant phototropins, the Neurospora VIVID (VVD) protein, and the Arabidopsis FKF1 and its related proteins. Studies of the plant phototropins have identified 11 flavin-contacting residues that are also conserved in the LOV domains of WC-1, VVD, and FKF1. In this study, by mutating the putative WC-1 flavin-binding sites, we show that these sites are important for the light function of the protein, suggesting that the WC-1 LOV domain adapts a structure similar to that of the phototropin LOV domains. By creating a Neurospora strain in which the LOV domain of WC-1 is swapped with that of VVD, we show that the LOV domain of VVD partially replaces the function of the WC-1 LOV domain, suggesting that VVD is a wc-dependent photoreceptor in Neurospora. Furthermore, we show that the Neurosporastrains containing a chimeric WC-1 protein with the LOV domain from FKF1 or phot1 can also sense light, suggesting that FKF1 and its related proteins are light sensors in Arabidopsis. Taken together, our data suggest that these LOV domains are structurally similar protein modules involved in blue-light sensing.

[1]  G. Macino,et al.  Role of a white collar‐1–white collar‐2 complex in blue‐light signal transduction , 1999, The EMBO journal.

[2]  D. E. Somers,et al.  ZEITLUPE Encodes a Novel Clock-Associated PAS Protein from Arabidopsis , 2000, Cell.

[3]  C. Schwerdtfeger,et al.  Blue light adaptation and desensitization of light signal transduction in Neurospora crassa , 2001, Molecular microbiology.

[4]  J. Dunlap,et al.  Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. , 1994, Science.

[5]  Y Yang,et al.  Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Dunlap,et al.  Genetic and molecular analysis of circadian rhythms in Neurospora. , 2001, Annual review of physiology.

[7]  M. Merrow,et al.  Light reception and circadian behavior in ‘blind’ and ‘clock‐less’ mutants of Neurospora crassa , 2002, The EMBO journal.

[8]  G. Macino,et al.  White collar 2, a partner in blue‐light signal transduction, controlling expression of light–regulated genes in Neurospora crassa , 1997, The EMBO journal.

[9]  G. Macino,et al.  White collar‐1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. , 1996, The EMBO journal.

[10]  J. Dunlap,et al.  White Collar-1, a Circadian Blue Light Photoreceptor, Binding to the frequency Promoter , 2002, Science.

[11]  J. Dunlap,et al.  WC‐2 mediates WC‐1–FRQ interaction within the PAS protein‐linked circadian feedback loop of Neurospora , 2001, The EMBO journal.

[12]  Winslow R. Briggs,et al.  The Photocycle of a Flavin-binding Domain of the Blue Light Photoreceptor Phototropin* , 2001, The Journal of Biological Chemistry.

[13]  K. Moffat,et al.  Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Yi Liu,et al.  Coiled‐coil domain‐mediated FRQ–FRQ interaction is essential for its circadian clock function in Neurospora , 2001, The EMBO journal.

[15]  D. Bell-Pedersen,et al.  Circadian clock-controlled genes isolated from Neurospora crassa are late night- to early morning-specific. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G. Macino,et al.  Involvement of protein kinase C in the response of Neurospora crassa to blue light , 1999, Molecular and General Genetics MGG.

[17]  G. Macino,et al.  Blue light regulation in Neurospora crassa. , 1997, Fungal genetics and biology : FG & B.

[18]  Yuhong Yang,et al.  WHITE COLLAR-1, a Multifunctional NeurosporaProtein Involved in the Circadian Feedback Loops, Light Sensing, and Transcription Repression of wc-2* , 2003, The Journal of Biological Chemistry.

[19]  D. Bell-Pedersen,et al.  vvd is required for light adaptation of conidiation-specific genes of Neurospora crassa, but not circadian conidiation. , 2001, Fungal genetics and biology : FG & B.

[20]  J. Christie,et al.  Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. , 2000, Biochemistry.

[21]  J. Dunlap,et al.  Light and clock expression of the Neurospora clock gene frequency is differentially driven by but dependent on WHITE COLLAR-2. , 2002, Genetics.

[22]  J. Christie,et al.  Phototropins 1 and 2: versatile plant blue-light receptors. , 2002, Trends in plant science.

[23]  S. Kay,et al.  A Role for LKP2 in the Circadian Clock of Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010332. , 2001, The Plant Cell Online.

[24]  P. Hegemann,et al.  Phot-LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. , 2003, Biophysical journal.

[25]  Masakatsu Watanabe,et al.  A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis , 2002, Nature.

[26]  A. Sancar,et al.  Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. , 2000, Annual review of biochemistry.

[27]  E. N. Pugh,et al.  Molecular mechanisms of vertebrate photoreceptor light adaptation , 1999, Current Opinion in Neurobiology.

[28]  Yi Liu,et al.  Alternative Initiation of Translation and Time-Specific Phosphorylation Yield Multiple Forms of the Essential Clock Protein FREQUENCY , 1997, Cell.

[29]  Keith Moffat,et al.  Photoexcited Structure of a Plant Photoreceptor Domain Reveals a Light-Driven Molecular Switch Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010475. , 2002, The Plant Cell Online.

[30]  E. Huala,et al.  Blue-light photoreceptors in higher plants. , 1999, Annual review of cell and developmental biology.

[31]  J. Dunlap.  Molecular Bases for Circadian Clocks , 1999, Cell.

[32]  Keith Moffat,et al.  The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. , 2003, Biochemistry.

[33]  M. Carlile,et al.  The Photobiology of Fungi , 1965 .

[34]  J. Dunlap,et al.  The PAS Protein VIVID Defines a Clock-Associated Feedback Loop that Represses Light Input, Modulates Gating, and Regulates Clock Resetting , 2001, Cell.

[35]  P Reymond,et al.  Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. , 1998, Science.

[36]  P. Lakin-Thomas,et al.  Circadian rhythms in Neurospora crassa: biochemistry and genetics. , 1990, Critical reviews in microbiology.

[37]  Gerald Richter,et al.  Blue Light Perception in Plants , 2003, The Journal of Biological Chemistry.

[38]  K. Gardner,et al.  White Collar-1, a DNA Binding Transcription Factor and a Light Sensor , 2002, Science.

[39]  K. Gardner,et al.  PAS Domain-Mediated WC-1/WC-2 Interaction Is Essential for Maintaining the Steady-State Level of WC-1 and the Function of Both Proteins in Circadian Clock and Light Responses of Neurospora , 2002, Molecular and Cellular Biology.

[40]  C. Schwerdtfeger,et al.  Localization and light-dependent phosphorylation of white collar 1 and 2, the two central components of blue light signaling in Neurospora crassa. , 2000, European journal of biochemistry.

[41]  Jennifer J. Loros,et al.  Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript , 1995, Cell.

[42]  J. Dunlap,et al.  Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. , 2003, Genetics.

[43]  P. Oeller,et al.  Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. , 1997, Science.

[44]  J. Dunlap,et al.  Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. , 1997, Science.

[45]  T Roenneberg,et al.  Circadian regulation of the light input pathway in Neurospora crassa , 2001, The EMBO journal.

[46]  J. Christie,et al.  LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B. Bartel,et al.  FKF1, a Clock-Controlled Gene that Regulates the Transition to Flowering in Arabidopsis , 2000, Cell.

[48]  A. Cashmore,et al.  Cryptochromes: blue light receptors for plants and animals. , 1999, Science.

[49]  Yi Liu,et al.  Thermally Regulated Translational Control of FRQ Mediates Aspects of Temperature Responses in the Neurospora Circadian Clock , 1997, Cell.