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Aureochromes – Blue Light Receptors

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Abstract

A variety of living organisms including bacteria, fungi, animals, and plants use blue light (BL) to adapt to changing ambient light. Photosynthetic forms (plants and algae) require energy of light for photosynthesis, movements, development, and regulation of activity. Several complex light-sensitive systems evolved in eukaryotic cells to use the information of light efficiently with photoreceptors selectively absorbing various segments of the solar spectrum, being the first components in the light signal transduction chain. They are most diverse in algae. Photosynthetic stramenopiles, which received chloroplasts from red algae during secondary symbiosis, play an important role in ecosystems and aquaculture, being primary producers. These taxa acquired the ability to use BL for regulation of such processes as phototropism, chloroplast photo-relocation movement, and photomorphogenesis. A new type of BL receptor–aureochrome (AUREO)–was identified in Vaucheria frigida in 2007. AUREO consists of two domains: bZIP (basic-region leucine zipper) domain and LOV (light-oxygen-voltage-sensing) domain, and thus this photoreceptor is a BL-sensitive transcription factor. This review presents current data on the structure, mechanisms of action, and biochemical features of aureochromes.

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Abbreviations

bHLH:

base helix-loop-helix

BL:

blue light

BLUF:

blue light sensing using FAD

bZIP:

basic-region leucine zipper

LOV:

light-oxygen-voltage-sensing

LRE:

light response elements

References

  1. Kianianmomeni, A., and Hallmann, A. (2014) Algal pho-toreceptors: in vivo functions and potential applications, Planta, 239, 1–26.

    Article  PubMed  CAS  Google Scholar 

  2. Ziegler, T., and Moglich, A. (2015) Photoreceptor engineer-ing, Front. Mol. Biosci., 2, doi: 10.3389/fmolb.2015.00030.

  3. Kianianmomeni, A., and Hallmann, A. (2016) Algal pho-tobiology: a rich source of unusual light sensitive proteins for synthetic biology and optogenetics, Methods Mol. Biol., 1408, 37–54.

    Article  PubMed  CAS  Google Scholar 

  4. Fraikin, G. Y., Strakhovskaya, M. G., and Rubin, A. B. (2013) Biological photoreceptors of light dependent regula-tory processes, Biochemistry (Moscow), 78, 1238–1253.

    Article  CAS  Google Scholar 

  5. Chattopadhyay, S., Ang, L. H., Puente, P., Deng, X. W., and Wei, N. (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression, Plant Cell, 10, 673–683.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Luo, X. M., Lin, W. H., Zhu, S., Zhu, J. Y., Sun, Y., Fan, X. Y., Cheng, M., Hao, Y., Oh, E., Tian, M., Liu, L., Zhang, M., Xie, Q., Chong, K., and Wang, Z. Y. (2010) Integration of light-and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis, Dev. Cell, 19, 872–883.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Li, J., Li G., Wang, H., and Deng, X. W. (2011) Phytochrome signaling mechanisms, Arabidopsis Book, 9, e0148; doi: 10.1199/tab.0148.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Ahmad, M., and Cashmore, A. R. (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor, Nature, 366, 162–166.

    Article  PubMed  CAS  Google Scholar 

  9. Lin, C., and Shalitin, D. (2003) Cryptochrome structure and signal transduction, Annu. Rev. Plant Biol., 54, 469–496.

    Article  PubMed  CAS  Google Scholar 

  10. Mei, Q., and Dvornyk, V. (2015) Evolutionary history of the photolyase/cryptochrome superfamily in eukaryotes, PLoS One, 10, e0135940; doi: 10.1371/journal.pone. 0135940.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Yurina, N. P., Mokerova, D. V., and Odintsova, M. S. (2013) Light-inducible stress plastid proteins of pho-totrophs, Russ. J. Plant Physiol., 60, 577–588.

    Article  CAS  Google Scholar 

  12. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010) Light-regulated plant growth and development, Curr. Top. Dev. Biol., 91, 29–66.

    Article  PubMed  CAS  Google Scholar 

  13. Huala, E., Oeller, P. W., Liscum, E., Han, I. S., Larsen, E., and Briggs, W. R. (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain, Science, 278, 2120–2123.

    Article  PubMed  CAS  Google Scholar 

  14. Christie, J. M. (2007) Phototropin blue-light receptors, Annu. Rev. Plant Biol., 58, 21–45.

    Article  PubMed  CAS  Google Scholar 

  15. Suetsugu, N., Mittmann, F., Wagner, G., Hughes, J., and Wada, M. (2005) A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution, Proc. Natl. Acad. Sci. USA, 102, 13705–13709.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Hegemann, P., Fuhrmann, M., and Kateriya, S. (2001) Algal sensory photoreceptors, J. Phycol., 37, 668–676.

    Article  CAS  Google Scholar 

  17. Foster, K. W., Saranak, J., Patel, N., Zarilli, G., Okabe, M., Kline, T., and Nakanishi, K. (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas, Nature, 311, 756–759.

    Article  PubMed  CAS  Google Scholar 

  18. Foster, K. W., and Smyth, R. D. (1980) Light antennas in phototactic algae, Microbiol. Rev., 44, 572–630.

    PubMed  PubMed Central  CAS  Google Scholar 

  19. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A. M., Bamberg, E., and Hegemann, P. (2002) Channelrhodopsin-1: a light-gated proton channel in green algae, Science, 296, 2395–2398.

    Article  PubMed  CAS  Google Scholar 

  20. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel, Proc. Natl. Acad. Sci. USA, 100, 13940–13945.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Sineshchekov, O. A., Jung, K. H., and Spudich, J. L. (2002) Two rhodopsins mediate phototaxis to low-and high-inten-sity light in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. USA, 99, 8689–8694.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Kato, H. E., Zhang, F., Yizhar, O., Ramakrishnan, C., Nishizawa, T., Hirata, K., Ito, J., Aita, Y., Tsukazaki, T., Hayashi, S., Hegemann, P., Maturana, A. D., Ishitani, R., Deisseroth, K., and Nureki, O. (2012) Crystal structure of the channelrhodopsin light-gated cation channel, Nature, 482, 369–374.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Gomelsky, M., and Klug, G. (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms, Trends Biochem. Sci., 27, 497–500.

    Article  PubMed  CAS  Google Scholar 

  24. Gomelsky, M., and Hoff, W. D. (2011) Light helps bacteria make important lifestyle decisions, Trends Microbiol., 19, 441–448.

    Article  PubMed  CAS  Google Scholar 

  25. Fraikin, G. Ya., Strakhovskaya, M. G., Belenikina, N. S., and Rubin, A. B. (2016) LOV and BLUF flavoprotein reg-ulatory photoreceptors of microorganisms and photosenso-ry actuators in optogenetic systems, Moscow Univ. Biol. Sci. Bull., 71, 50–57.

    Article  Google Scholar 

  26. Fiedler, B., Borner, T., and Wilde, A. (2005) Phototaxis in the cyanobacterium Synechocystis sp. PCC 6803: role of different photoreceptors, Photochem. Photobiol., 81, 1481–1488.

    Article  PubMed  CAS  Google Scholar 

  27. Masuda, S., and Bauer, C. E. (2002) AppA is a blue light photoreceptor that anti-represses photosynthesis gene expression in Rhodobacter sphaeroides, Cell, 110, 613–623.

    Article  PubMed  CAS  Google Scholar 

  28. Tschowri, N., Busse, S., and Hengge, R. (2009) The BLUFEAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli, Genes Dev., 23, 522–534.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Mussi, M. A., Gaddy, J. A., Cabruja, M., Arivett, B. A., Viale, A. M., Rasia, R., and Actis, L. A. (2010) The oppor-tunistic human pathogen Acinetobacter baumannii senses and responds to light, J. Bacteriol., 192, 6336–6345.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Takahashi, F., Yamagata, D., Ishikawa, M., Fukamatsu, Y., Ogura, Y., Kasahara, M., Kiyosue, T., Kikuyama, M., Wada, M., and Kataoka, H. (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stra-menopiles, Proc. Natl. Acad. Sci. USA, 104, 19625–19630.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ishikawa, M., Takahashi, F., Nozaki, H., Nagasato, C., Motomura, T., and Kataoka, H. (2009) Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes, Planta, 230, 543–552.

    Article  PubMed  CAS  Google Scholar 

  32. Takahashi, F., Hishinuma, T., and Kataoka, H. (2001) Blue light-induced branching in Vaucheria. Requirement of nuclear accumulation in the irradiated region, Plant Cell. Physiol., 42, 274–285.

    Article  PubMed  CAS  Google Scholar 

  33. Banerjee, A., Herman, E., Serif, M., Maestre-Reyna, M., Hepp, S., Pokorny, R., Kroth, P. G., Essen, L. O., and Kottke, T. (2016) Allosteric communication between DNA-binding and light-responsive domains of diatom class I aureochromes, Nucleic Acids Res., 44, 5957–5970.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Serif, M., Lepetit, B., Weißert, K., Kroth, P. G., and Rio Bartulos, C. (2017) A fast and reliable strategy to generate TALEN-mediated gene knockouts in the diatom Phaeodactylum tricornutum, Algal Res., 23, 186–195.

    Article  Google Scholar 

  35. Herman, E., and Kottke, T. (2015) Allosterically regulated unfolding of the A′α helix exposes the dimerization site of the blue-light-sensing aureochrome-LOV domain, Biochemistry, 54, 1484–1492.

    Article  PubMed  CAS  Google Scholar 

  36. Hisatomi, O., Nakatani, Y., Takeuchi, K., Takahashi, F., and Kataoka, H. (2014) Blue light-induced dimerization of monomeric aureochrome-1 enhances its affinity for the tar-get sequence, J. Biol. Chem., 289, 17379–17391.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Conrad, K. S., Manahan, C. C., and Crane, B. R. (2014) Photochemistry of flavoprotein light sensors, Nat. Chem. Biol., 10, 801–809.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Herrou, J., and Crosson, S. (2011) Function, structure and mechanism of bacterial photosensory LOV proteins, Nat. Rev. Microbiol., 9, 713–723.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Harper, S. M., Neil, L. C., and Gardner, K. H. (2003) Structural basis of a phototropin light switch, Science, 301, 1541–1544.

    Article  PubMed  CAS  Google Scholar 

  40. Moglich, A., and Moffat, K. (2007) Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA, J. Mol. Biol., 373, 112–126.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Nash, A. I., McNulty, R., Shillito, M. E., Swartz, T. E., Bogomolni, R. A., Luecke, H., and Gardner, K. H. (2011) Structural basis of photosensitivity in a bacterial light-oxy-gen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein, Proc. Natl. Acad. Sci. USA, 108, 9449–9454.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Vaidya, A. T., Chen, C. H., Dunlap, J. C., Loros, J. J., and Crane, B. R. (2011) Structure of a light-activated LOV pro-tein dimer that regulates transcription, Sci. Signal., 4, ra50; doi: 10.1126/scisignal.2001945.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Rodriguez-Romero, J., Hedtke, M., Kastner, C., Muller, S., and Fischer, R. (2010) Fungi, hidden in soil or up in the air: light makes a difference, Annu. Rev. Microbiol., 64, 585–610.

    Article  PubMed  CAS  Google Scholar 

  44. Schwerdtfeger, C., and Linden, H. (2003) VIVID is a flavo-protein and serves as a fungal blue light photoreceptor for photoadaptation, EMBO J., 22, 4846–4855.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Green, J., Crack, J. C., Thomson, A. J., and LeBrun, N. E. (2009) Bacterial sensors of oxygen, Curr. Opin. Microbiol., 12, 145–151.

    Article  PubMed  CAS  Google Scholar 

  46. Banerjee, A., Herman, E., Kottke, T., and Essen, L. O. (2016) Structure of a native-like aureochrome 1a LOV domain dimer from Phaeodactylum tricornutum, Structure, 24, 171–178.

    Article  PubMed  CAS  Google Scholar 

  47. Salomon, M., Christie, J. M., Knieb, E., Lempert, U., and Briggs, W. R. (2000) Photochemical and mutational analy-sis of the FMN-binding domain of the plant blue light receptor, phototropin, Biochemistry, 39, 9401–9410.

    Article  PubMed  CAS  Google Scholar 

  48. Heintz, U., and Schlichting, I. (2016) Blue light-induced LOV domain dimerization enhances the affinity of aure-ochrome 1a for its target DNA sequence, eLife, 5, e11860; doi: 10.7554/eLife.11860.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mitra, D., Yang, X., and Moffat, K. (2012) Crystal struc-tures of aureochrome1 LOV suggest new design strategies for optogenetics, Structure, 20, 698–706.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Essen, L. O., Franz, S., and Banerjee, A. (2017) Structural and evolutionary aspects of algal blue light receptors of the cryptochrome and aureochrome type, J. Plant Physiol., 217, 27–37.

    Article  PubMed  CAS  Google Scholar 

  51. Chen, Z., Yang, M. K., Li, C. Y., Wang, Y., Zhang, J., Wang, D. B., Zhang, X. E., and Ge, F. (2014) Phosphoproteomic analysis provides novel insights into stress responses in Phaeodactylum tricornutum, a model diatom, J. Proteome Res., 13, 2511–2523.

    Article  PubMed  CAS  Google Scholar 

  52. Herman, E., Sachse, M., Kroth, P. G., and Kottke, T. (2013) Blue-light-induced unfolding of the Jα helix allows for the dimerization of aureochrome-LOV from the diatom Phaeodactylum tricornutum, Biochemistry, 52, 3094–3101.

    Article  PubMed  CAS  Google Scholar 

  53. Harper, S. M., Christie, J. M., and Gardner, K. H. (2004) Disruption of the LOV–Jα helix interaction activates pho-totropin kinase activity, Biochemistry, 43, 16184–16192.

    Article  PubMed  CAS  Google Scholar 

  54. Kroth, P. G., Wilhelm, C., and Kottke, T. (2017) An update on aureochromes: phylogeny–mechanism–function, J. Plant Physiol., 217, 20–26.

    Article  PubMed  CAS  Google Scholar 

  55. Akiyama, Y., Nakasone, Y., Nakatani, Y., Hisatomi, O., and Terazima, M. (2016) Time-resolved detection of light-induced dimerization of monomeric aureochrome-1 and change in affinity for DNA, J. Phys. Chem., 120, 7360–7370.

    Article  CAS  Google Scholar 

  56. Toyooka, T., Hisatomi, O., Takahashi, F., Kataoka, H., and Terazima, M. (2011) Photoreactions of aureochrome-1, Biophys. J., 100, 2801–2809.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Takahashi, F. (2016) Blue-light-regulated transcription fac-tor, Aureochrome, in photosynthetic stramenopiles, J. Plant Res., 129, 189–197.

    PubMed  CAS  Google Scholar 

  58. Hisatomi, O., Terauchi, K., Zikihara, K., Ookubo, Y., Nakatani, Y., Takahashi, F., Tokutomi, S., and Kataoka, H. (2013) Blue light-induced conformational changes in a light-regulated transcription factor, Aureochrome-1, Plant Cell. Physiol., 54, 93–106.

    Article  PubMed  CAS  Google Scholar 

  59. Deng, Y., Yao, J., Fu, G., Guo, H., and Duan, D. (2014) Isolation, expression, and characterization of blue light recep-tor AUREOCHROME gene from Saccharina japonica (Laminariales, Phaeophyceae), Mar. Biotechnol., 16, 135–143.

    Article  CAS  Google Scholar 

  60. Ishikawa, M., Kataoka, H., and Takahashi, F. (2012) Analysis of light-dependent cell morphology and an accumulation response in Ochromonas danica, Cytologia, 77, 465–473.

    Article  Google Scholar 

  61. Huysman, M. J., Fortunato, A. E., Matthijs, M., Costa, B. S., Vanderhaeghen, R., Van den Daele, H., Sachse, M., Inze, D., Bowler, C., Kroth, P. G., Wilhelm, C., Falciatore, A., Vyverman, W., and De Veylder, L. (2013) Aureochome1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in Diatoms (Phaeodactylum tricornutum), Plant Cell., 25, 215–228.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Schellenberger Costa, B., Sachse, M., Jungandreas, A., Bartulos, C. R., Gruber, A., Jakob, T., Kroth, P. G., and Wilhelm, C. (2013) Aureochrome 1a is involved in the pho-toacclimation of the Diatom Phaeodactylum tricornutum, PLoS One, 8, e74451.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Glantz, S. T., Carpenter, E. J., Melkonian, M., Gardner, K. H., Boyden, E. S., Wong, G. K.-S., and Chow, B. Y. (2016) Functional and topological diversity of LOV domain pho-toreceptors, Proc. Natl. Acad. Sci. USA, 113, 1442–1451.

    Article  CAS  Google Scholar 

  64. Archibald, J. M. (2015) Endosymbiosis and eukaryotic cell evolution, Curr. Biol., 25, 911–921.

    Article  CAS  Google Scholar 

  65. Di Roberto, R. B., and Peisajovich, S. G. (2014) The role of domain shuffling in the evolution of signaling networks, J. Exp. Zool. B Mol. Dev. Evol., 322, 65–72.

    Article  PubMed  Google Scholar 

  66. Li, F.-W., Rothfels, C. J., Melkonian, M., Villarreal, J. C., Stevenson, D. W., Graham, S. W., Wong, G. K. S., Mathews, S., and Pryer, K. M. (2015) The origin and evo-lution of phototropins, Front. Plant Sci., 6, 637.

    PubMed  PubMed Central  Google Scholar 

  67. Janouskovec, J., Horak, A., Obornik, M., Lukes, J., and Keeling, P. J. (2010) A common red algal origin of the api-complexan, dinoflagellate, and heterokont plastids, Proc. Natl. Acad. Sci. USA, 107, 10949–10954.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Suetsugu, N., and Wada, M. (2013) Evolution of three LOV blue light receptor families in green plants and photosyn-thetic stramenopiles: phototropin, ZTL/FKF1/LKP2 and aureochrome, Plant Cell Physiol., 54, 8–23.

    Article  PubMed  CAS  Google Scholar 

  69. Kasahara, M., Torii, M., Fujita, A., and Tainaka, K. (2010) FMN binding and photochemical properties of plant puta-tive photoreceptors containing two LOV domains, LOV/LOV proteins, J. Biol. Chem., 285, 34765–34772.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Kagawa, T., Kasahara, M., Abe, T., Yoshida, S., and Wada, M. (2004) Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoid-ance movement, Plant Cell. Physiol., 45, 416–426.

    Article  PubMed  CAS  Google Scholar 

  71. Grusch, M., Schelch, K., Riedler, R., Reichhart, E., Differ, C., Berger, W., Ingles-Prieto, A., and Janovjak, H. (2014) Spatiotemporally precise activation of engineered receptor tyrosine kinases by light, EMBO J., 33, 1713–1726.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Muller, K., and Weber, W. (2013) Optogenetic tools for mammalian systems, Mol. BioSyst., 9, 596–608.

    Article  PubMed  CAS  Google Scholar 

  73. Pathak, G. P., Vrana, J. D., and Tucker, C. L. (2013) Optogenetic control of cell function using engineered pho-toreceptors, Biol. Cell, 105, 59–72.

    Article  PubMed  CAS  Google Scholar 

  74. Ye, H., Daoud-El Baba, M., Peng, R. W., and Fussenegger, M. (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice, Science, 332, 1565–1568.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to E. M. Chekunova.

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Original Russian Text © A. B. Matiiv, E. M. Chekunova, 2018, published in Biokhimiya, 2018, Vol. 83, No. 6, pp. 839-851.

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Matiiv, A.B., Chekunova, E.M. Aureochromes – Blue Light Receptors. Biochemistry Moscow 83, 662–673 (2018). https://doi.org/10.1134/S0006297918060044

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