Biology of Light-Sensing Proteins in Plants and Microorganisms

  • Mineo IsekiEmail author
  • Tetsuo Takahashi


A wide variety of light-sensing proteins that are found in plants and microorganisms and that provide natural resources for engineering optogenetic tools are briefly reviewed. We include microbial rhodopsins, which absorb blue/green light; phytochromes, which absorb red/far-red light; UV-A/blue-absorbing flavoproteins (cryptochromes, LOV-domain proteins, BLUF-domain proteins); and the recently discovered UV-B sensor UVR8. Among them, the significance of channelrhodopsins and photoactivated adenylyl cyclases is emphasized.


Rhodopsin Phytochrome Cryptochrome LOV domain BLUF domain UVR8 Channelrhodopsin Photoactivated adenylyl cyclase 


  1. Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166PubMedCrossRefGoogle Scholar
  2. Asamizu E, Nakamura Y, Sato S et al (1999) A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res 6:369–373PubMedCrossRefGoogle Scholar
  3. Balashov SP, Imasheva ES, Boichenko VA et al (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309:2061–2064PubMedCentralPubMedCrossRefGoogle Scholar
  4. Barends TR, Hartmann E, Griese JJ et al (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459:1015–1018PubMedCrossRefGoogle Scholar
  5. Béjà O, Aravind L, Koonin EV et al (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906PubMedCrossRefGoogle Scholar
  6. Bogomolni RA, Spudich JL (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci U S A 79:6250–6254PubMedCentralPubMedCrossRefGoogle Scholar
  7. Borthwick HA, Hendricks SB, Parker MW et al (1952) A reversible photoreaction controlling seed germination. Proc Natl Acad Sci U S A 38:662–666PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bucher D, Buchner E (2009) Stimulating PACalpha increases miniature excitatory junction potential frequency at the Drosophila neuromuscular junction. J Neurogenet 23:220–224PubMedCrossRefGoogle Scholar
  9. Butler WL, Norris KH, Siegelman HW et al (1959) Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci U S A 45:1703–1708PubMedCentralPubMedCrossRefGoogle Scholar
  10. Christie JM, Reymond P, Powell GK et al (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698–1701PubMedCrossRefGoogle Scholar
  11. Crefcoeur RP, Yin R, Ulm R et al (2013) Ultraviolet-B-mediated induction of protein-protein interactions in mammalian cells. Nat Commun 4:1779PubMedCrossRefGoogle Scholar
  12. Davis SJ, Vener AV, Vierstra RD (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517–2520PubMedCrossRefGoogle Scholar
  13. Demarsy E, Fankhauser C (2009) Higher plants use LOV to perceive blue light. Curr Opin Plant Biol 12:69–74PubMedCrossRefGoogle Scholar
  14. Derguini F, Mazur P, Nakanishi K et al (1991) All-trans-retinal is the chromophore bound to the photoreceptor of the alga Chlamydomonas reinhardtii. Photochem Photobiol 54:1017–1021PubMedCrossRefGoogle Scholar
  15. Diehn B (1969) Action spectra of the phototactic responses in Euglena. Biochim Biophys Acta 177:136–143PubMedCrossRefGoogle Scholar
  16. Ernst OP, Lodowski DT, Elstner M et al (2014) Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 114:126–163PubMedCentralPubMedCrossRefGoogle Scholar
  17. Fankhauser C, Yeh KC, Lagarias JC et al (1999) PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284:1539–1541PubMedCrossRefGoogle Scholar
  18. Foster KW, Saranak J, Patel N et al (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas. Nature 311:756–759PubMedCrossRefGoogle Scholar
  19. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, Shu S, Neupane R, Cipriano M, Mancuso J, Tu H, Salamov A, Lindquist E, Shapiro H, Lucas S, Grigoriev IV, Cande WZ, Fulton C, Rokhsar DS, Dawson SC (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631–642PubMedCrossRefGoogle Scholar
  20. Fuhrmann M, Stahlberg A, Govorunova E et al (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J Cell Sci 114:3857–3863PubMedGoogle Scholar
  21. Gardner G, Pike CS, Rice HV et al (1971) “Disaggregation” of phytochrome in vitro-a consequence of proteolysis. Plant Physiol 48:686–693PubMedCentralPubMedCrossRefGoogle Scholar
  22. Gomelsky M, Kaplan S (1998) AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD binding domain. J Biol Chem 273:35319–35325PubMedCrossRefGoogle Scholar
  23. Gomelsky M, Klug G (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem Sci 27:497–500PubMedCrossRefGoogle Scholar
  24. Govorunova EG, Spudich EN, Lane CE et al (2011) New channelrhodopsin with a red-shifted spectrum and rapid kinetics from Mesostigma viride. MBio 2:e00115-11PubMedCentralPubMedCrossRefGoogle Scholar
  25. Grote M (2013) Purple matter, membranes and ‘molecular pumps’ in rhodopsin research (1960s–1980s). J Hist Biol 46:331–368PubMedCrossRefGoogle Scholar
  26. He Q, Cheng P, Yang Y et al (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297:840–843PubMedCrossRefGoogle Scholar
  27. Hegemann P, Gärtner W, Uhl R (1991) All-trans retinal constitutes the functional chromophore in Chlamydomonas rhodopsin. Biophys J 60:1477–1489PubMedCentralPubMedCrossRefGoogle Scholar
  28. Heintzen C, Loros JJ, Dunlap JC (2001) The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104:453–464PubMedCrossRefGoogle Scholar
  29. Hershey HP, Colbert JT, Lissemore JL et al (1984) Molecular cloning of cDNA for Avena phytochrome. Proc Natl Acad Sci U S A 81:2332–2336PubMedCentralPubMedCrossRefGoogle Scholar
  30. Hildebrand E, Dencher N (1975) Two photosystems controlling behavioural responses of Halobacterium halobium. Nature 257:46–48PubMedCrossRefGoogle Scholar
  31. Hong KP, Spitzer NC, Nicol X (2011) Improved molecular toolkit for cAMP studies in live cells. BMC Res Notes 4:241PubMedCentralPubMedCrossRefGoogle Scholar
  32. Hou SY, Govorunova EG, Ntefidou M et al (2012) Diversity of Chlamydomonas. Photochem Photobiol 88:119–128PubMedCentralPubMedCrossRefGoogle Scholar
  33. Huala E, Oeller PW, Liscum E et al (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–2123PubMedCrossRefGoogle Scholar
  34. Hughes J, Lamparter T, Mittmann F et al (1997) A prokaryotic phytochrome. Nature 386:663PubMedCrossRefGoogle Scholar
  35. Ihara K, Umemura T, Katagiri I et al (1999) Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J Mol Biol 285:163–174PubMedCrossRefGoogle Scholar
  36. Ikeuchi M, Ishizuka T (2008) Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem Photobiol Sci 7:1159–1167PubMedCrossRefGoogle Scholar
  37. Iseki M, Matsunaga S, Murakami A et al (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051PubMedCrossRefGoogle Scholar
  38. Jung KH, Trivedi VD, Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47:1513–1522PubMedCrossRefGoogle Scholar
  39. Kagawa T, Sakai T, Suetsugu N et al (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141PubMedCrossRefGoogle Scholar
  40. Kinoshita T, Doi M, Suetsugu N et al (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660PubMedCrossRefGoogle Scholar
  41. Kliebenstein DJ, Lim JE, Landry LG et al (2002) Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol 130:234–243PubMedCentralPubMedCrossRefGoogle Scholar
  42. Koumura Y, Suzuki T, Yoshikawa S, Watanabe M, Iseki M (2004) The origin of photoactivated adenylyl cyclase (PAC), the Euglena blue-light receptor: phylogenetic analysis of orthologues of PAC subunits from several euglenoids and trypanosome-type adenylyl cyclases from Euglena gracilis. Photochem Photobiol Sci 3:580–586PubMedCrossRefGoogle Scholar
  43. Lawson MA, Zacks DN, Derguini F et al (1991) Retinal analog restoration of photophobic responses in a blind Chlamydomonas reinhardtii mutant. Evidence for an archaebacterial like chromophore in a eukaryotic rhodopsin. Biophys J 60:1490–1498PubMedCentralPubMedCrossRefGoogle Scholar
  44. Liu B, Zuo Z, Liu H et al (2011) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev 25:1029–1034PubMedCentralPubMedCrossRefGoogle Scholar
  45. Liu H, Yu X, Li K et al (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–1539PubMedCrossRefGoogle Scholar
  46. Losi A, Gärtner W (2008) Bacterial bilin- and flavin-binding photoreceptors. Photochem Photobiol Sci 7:1168–1178PubMedCrossRefGoogle Scholar
  47. Mackin KA, Roy RA, Theobald DL (2014) An empirical test of convergent evolution in rhodopsins. Mol Biol Evol 31:85–95PubMedCentralPubMedCrossRefGoogle Scholar
  48. Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623PubMedCrossRefGoogle Scholar
  49. Matsunaga S, Hori T, Takahashi T et al (1998) Discovery of signaling effect of UV-B/C light in the extended UV-A/blue-type action spectra for stepdown and step-up photophobic responses in the unicellular flagellate alga Euglena gracilis. Protoplasma 201:45–52CrossRefGoogle Scholar
  50. Matsuno-Yagi A, Mukohata Y (1977) Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. Biochem Biophys Res Commun 78:237–243PubMedCrossRefGoogle Scholar
  51. Müller K, Engesser R, Schulz S et al (2013) Multi-chromatic control of mammalian gene expression and signaling. Nucleic Acids Res 41:e124PubMedCentralPubMedCrossRefGoogle Scholar
  52. Nagahama T, Suzuki T, Yoshikawa S et al (2007) Functional transplant of photoactivated adenylyl cyclase (PAC) into Aplysia sensory neurons. Neurosci Res 59:81–88PubMedCrossRefGoogle Scholar
  53. Nagel G, Ollig D, Fuhrmann M et al (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398PubMedCrossRefGoogle Scholar
  54. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667PubMedCrossRefGoogle Scholar
  55. Nicol X, Hong KP, Spitzer NC (2011) Spatial and temporal second messenger codes for growth cone turning. Proc Natl Acad Sci U S A 108:13776–13781PubMedCentralPubMedCrossRefGoogle Scholar
  56. Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat New Biol 233:149–152PubMedCrossRefGoogle Scholar
  57. Raffelberg S, Wang L, Gao S et al (2013) A LOV-domain-mediated blue-light-activated adenylate (adenylyl) cyclase from the cyanobacterium Microcoleus chthonoplastes PCC 7420. Biochem J 55:359–365CrossRefGoogle Scholar
  58. Rice HV, Briggs WR, Jackson-White CJ (1973) Purification of oat and rye phytochrome. Plant Physiol 51:917–926PubMedCentralPubMedCrossRefGoogle Scholar
  59. Rizzini L, Favory JJ, Cloix C et al (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106PubMedCrossRefGoogle Scholar
  60. Ryu MH, Moskvin OV, Siltberg-Liberles J et al (2010) Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J Biol Chem 285:41501–41508PubMedCentralPubMedCrossRefGoogle Scholar
  61. Sakamoto M, Wada A, Akai A et al (1998) Evidence for the archaebacterial-type conformation about the bond between the beta-ionone ring and the polyene chain of the chromophore retinal in chlamyrhodopsin. FEBS Lett 434:335–338PubMedCrossRefGoogle Scholar
  62. Schröder-Lang S, Schwärzel M, Seifert R et al (2007) Fast manipulation of cellular cAMP level by light in vivo. Nat Methods 4:39–42PubMedCrossRefGoogle Scholar
  63. Shu X, Royant A, Lin MZ et al (2009) Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324:804–807PubMedCentralPubMedCrossRefGoogle Scholar
  64. Sineshchekov OA, Jung KH, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 99:8689–8694PubMedCentralPubMedCrossRefGoogle Scholar
  65. Spudich EN, Spudich JL (1982) Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-transduction mutants of Halobacterium halobium. Proc Natl Acad Sci U S A 79:4308–4312PubMedCentralPubMedCrossRefGoogle Scholar
  66. Spudich JL, Yang CS, Jung KH et al (2000) Retinylidene proteins: structures and functions from archaea to humans. Annu Rev Cell Dev Biol 16:365–392PubMedCrossRefGoogle Scholar
  67. Stierl M, Stumpf P, Udwari D et al (2011) Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa. J Biol Chem 286:1181–1188PubMedCentralPubMedCrossRefGoogle Scholar
  68. Suzuki T, Yamasaki K, Fujita S et al (2003) Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun 301:711–717PubMedCrossRefGoogle Scholar
  69. Swartz TE, Tseng TS, Frederickson MA et al (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317:1090–1093PubMedCrossRefGoogle Scholar
  70. Takahashi F, Yamagata D, Ishikawa M et al (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci U S A 104:19625–19630PubMedCentralPubMedCrossRefGoogle Scholar
  71. Takahashi T, Tomioka H, Kamo N et al (1985) A photosystem other than PS370 also mediates the negative phototaxis of Halobacterium halobium. FEMS Microbiol Lett 28:161–164CrossRefGoogle Scholar
  72. Takahashi T, Yoshihara K, Watanabe M et al (1991) Photoisomerization of retinal at 13-ene is important for phototaxis of Chlamydomonas reinhardtii: simultaneous measurements of phototactic and photophobic responses. Biochem Biophys Res Commun 178:1273–1279PubMedCrossRefGoogle Scholar
  73. Tomioka H, Takahashi T, Kamo N et al (1986) Flash spectrophotometric identification of a fourth rhodopsin-like pigment in Halobacterium halobium. Biochem Biophys Res Commun 139:389–395PubMedCrossRefGoogle Scholar
  74. van der Horst GT, Muijtjens M, Kobayashi K et al (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627–630PubMedCrossRefGoogle Scholar
  75. Vierstra RD, Quail PH (1982) Native phytochrome: inhibition of proteolysis yields a homogeneous monomer of 124 kilodaltons from Avena. Proc Natl Acad Sci USA 79:5272–5276PubMedCentralPubMedCrossRefGoogle Scholar
  76. Weissenberger S, Schultheis C, Liewald JF et al (2011) PACα–an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans. J Neurochem 116:616–625PubMedCrossRefGoogle Scholar
  77. Yasukawa H, Sato A, Kita A, Kodaira K, Iseki M, Takahashi T, Shibusawa M, Watanabe M, Yagita K (2013) Identification of photoactivated adenylyl cyclases in Naegleria australiensis and BLUF-containing protein in Naegleria fowleri. J Gen Appl Microbiol 59:361–369PubMedCrossRefGoogle Scholar
  78. Yatsuhashi H, Hashimoto T, Shimizu S (1982) Ultraviolet action spectrum for anthocyanin formation in broom sorghum first internodes. Plant Physiol 70:735–741PubMedCentralPubMedCrossRefGoogle Scholar
  79. Zhang F, Prigge M, Beyrière F et al (2008) Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat Neurosci 11:631–633PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  1. 1.Faculty of Pharmaceutical SciencesToho UniversityChibaJapan

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