Biological Significance of Photoreceptor Photocycle Length: VIVID Photocycle Governs the Dynamic VIVID-White Collar Complex Pool Mediating Photo-adaptation and Response to Changes in Light Intensity

English version České info

Sensing light from the environment using a variety of photoreceptors is of great adaptive significance for most eukaryotes. A key feature of photoreceptors is the photocycle length, the time taken to decay from the initial signaling light state back to the receptive dark state; however, the significance of photocycle length, or adduct decay length, has not been tested in a biological setting. The photocycle length is determined by the chemical environment of the active site where a photon absorbing chromophore forms an adduct with a conserved amino acid. There is clear evidence of evolutionary selection for a particular photocycle length even between photoreceptors containing the same prototypic light-sensing domains suggesting functional relevance. Using defined in vitro mutations that change the photocycle length of the VIVID (VVD) protein over 4 orders of magnitude we were able to ascribe a pivotal role of the native photochemistry of the protein in its function as a photoreceptor in the light and circadian biology of Neurospora crassa. This study links in vitro photochemical studies with in vivo function and provides evidence that the true evolutionary and functional significance of native photochemistry of photoreceptors can be enhanced by studying photocycle mutants in their native systems.

Vyšlo v časopise: Biological Significance of Photoreceptor Photocycle Length: VIVID Photocycle Governs the Dynamic VIVID-White Collar Complex Pool Mediating Photo-adaptation and Response to Changes in Light Intensity. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005215
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005215

Souhrn

Zdroje

1. Briggs W, Spudich J. Handbook of Photosensory Receptors. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim; 2005.

2. Kennis JTM, van Stokkum IHM, Crosson S, Gauden M, Moffat K, van Grondelle R. The LOV2 Domain of Phototropin: A Reversible Photochromic Switch. J Am Chem Soc. 2004;126 : 4512–4513. 15070357

3. Pudasaini A, Zoltowski BD. Zeitlupe Senses Blue-Light Fluence To Mediate Circadian Timing in Arabidopsis thaliana. Biochemistry (Mosc). 2013;52 : 7150–7158. doi: 10.1021/bi401027n 24033190

4. Losi A, Polverini E, Quest B, Gärtner W. First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys J. 2002;82 : 2627–2634. 11964249

5. Christie JM. Phototropin Blue-Light Receptors. Annu Rev Plant Biol. 2007;58 : 21–45. 17067285

6. Cheng P, He Q, Yang Y, Wang L, Liu Y. Functional conservation of light, oxygen, or voltage domains in light sensing. Proc Natl Acad Sci. 2003;100 : 5938–5943. 12719523

7. Suetsugu N, Wada M. Evolution of Three LOV Blue Light Receptor Families in Green Plants and Photosynthetic Stramenopiles: Phototropin, ZTL/FKF1/LKP2 and Aureochrome. Plant Cell Physiol. 2012;54 : 8–23. doi: 10.1093/pcp/pcs165 23220691

8. Demarsy E, Fankhauser C. Higher plants use LOV to perceive blue light. Curr Opin Plant Biol. 2009;12 : 69–74. doi: 10.1016/j.pbi.2008.09.002 18930433

9. Herrou J, Crosson S. Function, structure and mechanism of bacterial photosensory LOV proteins. Nat Rev Microbiol. 2011;9 : 713–723. doi: 10.1038/nrmicro2622 21822294

10. Conrad KS, Manahan CC, Crane BR. Photochemistry of flavoprotein light sensors. Nat Chem Biol. 2014;10 : 801–809. doi: 10.1038/nchembio.1633 25229449

11. Crosson S, Rajagopal S, Moffat K. The LOV Domain Family: Photoresponsive Signaling Modules Coupled to Diverse Output Domains †. Biochemistry (Mosc). 2003;42 : 2–10.

12. Schleicher E, Kowalczyk RM, Kay CWM, Hegemann P, Bacher A, Fischer M, et al. On the Reaction Mechanism of Adduct Formation in LOV Domains of the Plant Blue-Light Receptor Phototropin. J Am Chem Soc. 2004;126 : 11067–11076. 15339193

13. Freddolino PL, Gardner KH, Schulten K. Signaling mechanisms of LOV domains: new insights from molecular dynamics studies. Photochem Photobiol Sci. 2013;12 : 1158. doi: 10.1039/c3pp25400c 23407663

14. Hisatomi O, Takeuchi K, Zikihara K, Ookubo Y, Nakatani Y, Takahashi F, et al. Blue Light-Induced Conformational Changes in a Light-Regulated Transcription Factor, Aureochrome-1. Plant Cell Physiol. 2012;54 : 93–106. doi: 10.1093/pcp/pcs160 23220692

15. Nakasako M, Iwata T, Matsuoka D, Tokutomi S. Light-Induced Structural Changes of LOV Domain-Containing Polypeptides from Arabidopsis Phototropin 1 and 2 Studied by Small-Angle X-ray Scattering †. Biochemistry (Mosc). 2004;43 : 14881–14890. 15554695

16. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, Dunlap JC, et al. Conformational Switching in the Fungal Light Sensor Vivid. Science. 2007;316 : 1054–1057. 17510367

17. Lee C -⁠ T, Malzahn E, Brunner M, Mayer MP. Light-Induced Differences in Conformational Dynamics of the Circadian Clock Regulator VIVID. J Mol Biol. 2014;426 : 601–610. doi: 10.1016/j.jmb.2013.10.035 24189053

18. Möglich A, Moffat K. Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J Mol Biol. 2007;373 : 112–126. 17764689

19. Schwerdtfeger C, Linden H. Blue light adaptation and desensitization of light signal transduction in Neurospora crassa. Mol Microbiol. 2001;39 : 1080–1087. 11251826

20. Zoltowski BD, Vaccaro B, Crane BR. Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol. 2009;5 : 827–834. doi: 10.1038/nchembio.210 19718042

21. Corchnoy SB, Swatrz T, Lewis JW, Szundi I, Briggs WR, Bogomolni RA. Intramolecular Proton Transfers and Structural Changes during the Photocycle of the LOV2 Domain of Phototropin 1. J Biol Chem. 2002;278 : 724–731. 12411437

22. Swartz TE, Corchnoy SB, Christie JM, Lewis JW, Szundi I, Briggs WR, et al. The Photocycle of a Flavin-binding Domain of the Blue Light Photoreceptor Phototropin. J Biol Chem. 2001;276 : 36493–36500. 11443119

23. Chan RH, Lewis JW, Bogomolni RA. Photocycle of the LOV-STAS Protein from the Pathogen Listeria monocytogenes. Photochem Photobiol. 2013;89 : 361–369. doi: 10.1111/php.12004 23025752

24. Zayner JP, Sosnick TR. Factors that control the chemistry of the LOV domain photocycle. PloS One. 2014;9: e87074. doi: 10.1371/journal.pone.0087074 24475227

25. Chen C-H, DeMay BS, Gladfelter AS, Dunlap JC, Loros JJ. Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proc Natl Acad Sci. 2010;107 : 16715–16720. doi: 10.1073/pnas.1011190107 20733070

26. Heintzen C, Loros JJ, Dunlap JC. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell. 2001;104 : 453–464. 11239402

27. Zoltowski BD, Crane BR. Light Activation of the LOV Protein Vivid Generates a Rapidly Exchanging Dimer † ‡. Biochemistry (Mosc). 2008;47 : 7012–7019. doi: 10.1021/bi8007017 18553928

28. Talora C, Franchi L, Linden H, Ballario P, Macino G. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 1999;18 : 4961–4968. 10487748

29. Froehlich AC, Liu Yi, Loros JJ, Dunlap JC. White Collar-1, a Circadian Blue Light Photoreceptor, Binding to the frequency Promoter. Science. 2002;297 : 815–819. 12098706

30. He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y. White Collar-1, a DNA Binding Transcription Factor and a Light Sensor. Science. 2002;297 : 840–843. 12098705

31. Chen C -⁠ H, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ. Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J. 2009;28 : 1029–1042. doi: 10.1038/emboj.2009.54 19262566

32. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, Tag AG, et al. Transcription Factors in Light and Circadian Clock Signaling Networks Revealed by Genomewide Mapping of Direct Targets for Neurospora White Collar Complex. Eukaryot Cell. 2010;9 : 1549–1556. doi: 10.1128/EC.00154-10 20675579

33. Wu C, Yang F, Smith KM, Peterson M, Dekhang R, Zhang Y, et al. Genome-Wide Characterization of Light-Regulated Genes in Neurospora crassa. G3amp58 GenesGenomesGenetics. 2014;4 : 1731–1745.

34. Lamb JS, Zoltowski BD, Pabit SA, Li L, Crane BR, Pollack L. Illuminating Solution Responses of a LOV Domain Protein with Photocoupled Small-Angle X-Ray Scattering. J Mol Biol. 2009;393 : 909–919. doi: 10.1016/j.jmb.2009.08.045 19712683

35. Malzahn E, Ciprianidis S, Káldi K, Schafmeier T, Brunner M. Photoadaptation in Neurospora by Competitive Interaction of Activating and Inhibitory LOV Domains. Cell. 2010;142 : 762–772. doi: 10.1016/j.cell.2010.08.010 20813262

36. Hunt SM, Thompson S, Elvin M, Heintzen C. VIVID interacts with the WHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora. Proc Natl Acad Sci. 2010;107 : 16709–16714. doi: 10.1073/pnas.1009474107 20807745

37. Schwerdtfeger C, Linden H. VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J. 2003;22 : 4846–4855. 12970196

38. Elvin M, Loros JJ, Dunlap JC, Heintzen C. The PAS/LOV protein VIVID supports a rapidly dampened daytime oscillator that facilitates entrainment of the Neurospora circadian clock. Genes Dev. 2005;19 : 2593–2605. 16264193

39. Chen C -⁠ H, Loros JJ. Neurospora sees the light: light signaling components in a model system. Commun Integr Biol. 2009;2 : 448–451. 19907715

40. Baker CL, Loros JJ, Dunlap JC. The circadian clock of Neurospora crassa: Neurospora crassa circadian clock. FEMS Microbiol Rev. 2012;36 : 95–110. doi: 10.1111/j.1574-6976.2011.00288.x 21707668

41. Collopy PD, Colot HV, Park G, Ringelberg C, Crew CM, Borkovich KA, et al. High-Throughput Construction of Gene Deletion Cassettes for Generation of Neurospora crassa Knockout Strains. In: Sharon A, editor. Molecular and Cell Biology Methods for Fungi. Totowa, NJ: Humana Press; 2010. pp. 33–40. http://www.springerlink.com/index/10.1007/978-1-60761-611-5_3

42. Baima S, Macino G, Morelli G. Photoregulation of the albino-3 gene in Neurospora crassa. J Photochem Photobiol B. 1991;11 : 107–115. 1837560

43. Vaidya AT, Chen C-H, Dunlap JC, Loros JJ, Crane BR. Structure of a light-activated LOV protein dimer that regulates transcription. Sci Signal. 2011;4: ra50. doi: 10.1126/scisignal.2001945 21868352

44. Schafmeier T, Diernfellner A, Schafer A, Dintsis O, Neiss A, Brunner M. Circadian activity and abundance rhythms of the Neurospora clock transcription factor WCC associated with rapid nucleo-cytoplasmic shuttling. Genes Dev. 2008;22 : 3397–3402. doi: 10.1101/gad.507408 19141472

45. Shi M, Collett M, Loros JJ, Dunlap JC. FRQ-Interacting RNA Helicase Mediates Negative and Positive Feedback in the Neurospora Circadian Clock. Genetics. 2009;184 : 351–361. doi: 10.1534/genetics.109.111393 19948888

46. Hong CI, Ruoff P, Loros JJ, Dunlap JC. Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus. Genes Dev. 2008;22 : 3196–3204. doi: 10.1101/gad.1706908 18997062

47. Dunlap JC, Loros JJ. How fungi keep time: circadian system in Neurospora and other fungi. Curr Opin Microbiol. 2006;9 : 579–587. 17064954

48. Dunlap JC. Proteins in the Neurospora Circadian Clockworks. J Biol Chem. 2006;281 : 28489–28493. 16905532

49. Liu Y, Bell-Pedersen D. Circadian Rhythms in Neurospora crassa and Other Filamentous Fungi. Eukaryot Cell. 2006;5 : 1184–1193. 16896204

50. Lee K, Loros JJ, Dunlap JC. Interconnected Feedback Loops in the Neurospora Circadian System. Science. 2000;289 : 107–110. 10884222

51. He Q, Shu H, Cheng P, Wang L, Liu Y. Light-independent Phosphorylation of WHITE COLLAR-1 Regulates Its Function in the Neurospora Circadian Negative Feedback Loop. J Biol Chem. 2005;280 : 17526–17532. 15731099

52. Chen C-H, Dunlap JC, Loros JJ. Neurospora illuminates fungal photoreception. Fungal Genet Biol. 2010;47 : 922–929. doi: 10.1016/j.fgb.2010.07.005 20637887

53. Belden WJ, Larrondo LF, Froehlich AC, Shi M, Chen C-H, Loros JJ, et al. The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev. 2007;21 : 1494–1505. 17575051

54. Bünning E, Moser I. Interference of moonlight with the photoperiodic measurement of time by plants, and their adaptive reaction. Proc Natl Acad Sci. 1969;62 : 1018–1022. 16591742

55. Corrochano LM. Fungal photoreceptors: sensory molecules for fungal development and behaviour. Photochem Photobiol Sci. 2007;6 : 725. 17609765

56. Zhang J, Stankey RJ, Vierstra RD. Structure-Guided Engineering of Plant Phytochrome B with Altered Photochemistry and Light Signaling. PLANT Physiol. 2013;161 : 1445–1457. doi: 10.1104/pp.112.208892 23321421

57. Medzihradszky M, Bindics J, Adam E, Viczian A, Klement E, Lorrain S, et al. Phosphorylation of Phytochrome B Inhibits Light-Induced Signaling via Accelerated Dark Reversion in Arabidopsis. Plant Cell. 2013;25 : 535–544. doi: 10.1105/tpc.112.106898 23378619

58. Gin E, Diernfellner ACR, Brunner M, Höfer T. The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation. Mol Syst Biol. 2013;9.

59. Káldi K, González BH, Brunner M. Transcriptional regulation of the Neurospora circadian clock gene wc-1 affects the phase of circadian output. EMBO Rep. 2006;7 : 199–204. 16374510

60. Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, Macino G. White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J. 1996;15 : 1650. 8612589

61. Franchi L, Fulci V, Macino G. Protein kinase C modulates light responses in Neurospora by regulating the blue light photoreceptor WC-1: PKC effects on the WC-1 photoreceptor. Mol Microbiol. 2005;56 : 334–345. 15813728

62. Crosthwaite SK, Loros JJ, Dunlap JC. Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell. 1995;81 : 1003–1012. 7600569