Journal of Plant Research

, Volume 129, Issue 2, pp 189–197 | Cite as

Blue-light-regulated transcription factor, Aureochrome, in photosynthetic stramenopiles

  • Fumio TakahashiEmail author
JPR Symposium The Cutting Edge of Photoresponse Mechanisms: Photoreceptor and Signaling Mechanism


During the course of evolution through various endosymbiotic processes, diverse photosynthetic eukaryotes acquired blue light (BL) responses that do not use photosynthetic pathways. Photosynthetic stramenopiles, which have red algae-derived chloroplasts through secondary symbiosis, are principal primary producers in aquatic environments, and play important roles in ecosystems and aquaculture. Through secondary symbiosis, these taxa acquired BL responses, such as phototropism, chloroplast photo-relocation movement, and photomorphogenesis similar to those which green plants acquired through primary symbiosis. Photosynthetic stramenopile BL receptors were undefined until the discovery in 2007, of a new type of BL receptor, the aureochrome (AUREO), from the photosynthetic stramenopile alga, Vaucheria. AUREO has a bZIP domain and a LOV domain, and thus BL-responsive transcription factor. AUREO orthologs are only conserved in photosynthetic stramenopiles, such as brown algae, diatoms, and red tide algae. Here, a brief review is presented of the role of AUREOs as photoreceptors for these diverse BL responses and their biochemical properties in photosynthetic stramenopiles.


Aureochrome Blue light LOV Photosynthetic stramenopiles Transcription factor Vaucheria 





Blue light


Basic leucine zipper





This work was supported by PRESTO Japan Science and Technology Corporation and a grant-in-aid for scientific research (26440156), from the Ministry of Education, Culture, Sports, Science and Technology, Japan. I thank Dr. Ian G. Gleadall (Tohoku University) for critical reading of the manuscript. I am grateful to Dr. Hironao Kataoka (Tohoku University) and Dr. Masahiro Kasahara (Ritsumeikan University) for helpful comments and discussion.


  1. Adl SM, Simpson AGB, Farmer MA et al (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451CrossRefPubMedGoogle Scholar
  2. Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166CrossRefPubMedGoogle Scholar
  3. Aihara Y, Yamamoto T, Okajima K et al (2012) Mutations in N-terminal flanking region of blue light-sensing light-oxygen and voltage 2 (LOV2) domain disrupt Its repressive activity on kinase domain in the Chlamydomonas phototropin. J Biol Chem 287:9901–9909PubMedCentralCrossRefPubMedGoogle Scholar
  4. Blatt MR (1983) The action spectrum for chloroplast movements and evidence for blue-light-photoreceptor cycling in the alga Vaucheria. Planta 159:267–276CrossRefPubMedGoogle Scholar
  5. Blatt MR, Briggs WR (1980) Blue-light-induced cortical fiber reticulation concomitant with chloroplast aggregation in the alga Vaucheria sessilis. Planta 147:355–362CrossRefPubMedGoogle Scholar
  6. Blatt MR, Wessells NK, Briggs WR (1980) Actin and cortical fiber reticulation in the siphonaceous alga Vaucheria sessilis. Planta 147:363–375CrossRefPubMedGoogle Scholar
  7. Buggeln RG (1974) Negative phototropism of the haptera of Alaria esculenta (Laminarieales). J Phycol 10:80–82Google Scholar
  8. Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57:953–994PubMedCentralPubMedGoogle Scholar
  9. Chapman S, Faulkner C, Kaiserli E et al (2008) The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc Natl Acad Sci USA 105:20038–20043PubMedCentralCrossRefPubMedGoogle Scholar
  10. Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45CrossRefPubMedGoogle Scholar
  11. Christie JM, Reymond P, Powell GK et al (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698–1701CrossRefPubMedGoogle Scholar
  12. Christie JM, Swartz TE, Bongmolni RA, Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32:205–219CrossRefPubMedGoogle Scholar
  13. Clauss H (1971) Wachstum von Dictyota dichotoma in Rot- und Blaulicht. Naturwissenschaften 58:272CrossRefPubMedGoogle Scholar
  14. Cock JM, Sterck L, Rouzé P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621CrossRefPubMedGoogle Scholar
  15. Costa BS, Jungandreas A, Jakob T, Weisheit W, Mittag M, Wilhelm C (2013a) Blue light is essential for high light acclimation and photoprotection in the diatom Phaeodactylum tricornutum. J Exp Bot 64:483–493CrossRefGoogle Scholar
  16. Costa BS, Sachse M, Jungandreas A et al (2013b) Aureochrome 1a is involved in the photoacclimation of the diatom Phaeodactylum tricornutum. PLoS One 8:e74451CrossRefGoogle Scholar
  17. Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2–10CrossRefPubMedGoogle Scholar
  18. Dring MJ, Lüning K (1975a) A photoperiodic response mediated by blue light in the brown alga Scytosiphon lomentaria. Planta 125:25–32CrossRefPubMedGoogle Scholar
  19. Dring MJ, Lüning K (1975b) Induction of two-dimensional growth and hair formation by blue light in the brown alga Scytosiphon lomentaria. Z Pflanzenphysiol 75:107–117CrossRefGoogle Scholar
  20. Fischer-Arnold (1963) Untersuchungen über die Chloroplastenbewegung bei Vaucheria sessilis. Protoplasma 56:495–520CrossRefGoogle Scholar
  21. Fu G, Nagasato C, Yamagishi T, Oka S, Cock JM, Motomura T (2014) Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 165:662–675CrossRefPubMedGoogle Scholar
  22. Furukawa T, Watanabe M, Shihira-Ishikawa I (1998) Green- and blue-light-mediated chloroplast migration in the centric diatom Pleurosira laevis. Protoplasma 203:214–220CrossRefGoogle Scholar
  23. Furuya M (1993) Phytochromes: their molecular species, gene families, and functions. Annu Rev Plant Physiol 44:617–645CrossRefGoogle Scholar
  24. Green JB, Li W-Y, Manhart JR et al (2000) Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol 124:331–342PubMedCentralCrossRefPubMedGoogle Scholar
  25. Grusch M, Schelch K, Riedler et al (2014) Spatio-temporally precise activation of engineered receptor tyrosine kinases by light. EMBO J 33:1713–1726PubMedCentralCrossRefPubMedGoogle Scholar
  26. Häder DP, Colombetti G, Leuci F, Quaglia M (1981) Phototaxis in flagellates, Euglena gracilis and Ochromonas danica. Arch Microbiol 130:78–82CrossRefGoogle Scholar
  27. Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301:1541–1544CrossRefPubMedGoogle Scholar
  28. Haupt W, Schönfeld I (1962) Über das Wirkungsspektrum der “negative Phototaxis” der Vaucheria-Chloroplasten. Ber Dtsch Bot Ges 75:14–23Google Scholar
  29. He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297:840–843CrossRefPubMedGoogle Scholar
  30. Herman E, Kottke T (2015) Allosterically regulated unfolding of the A’α helix exposes the dimerization site of the blue-light-sensing Aureochrome-LOV domain. Biochemistry 54:1484–1492CrossRefPubMedGoogle Scholar
  31. Herman E, Sachse M, Kroth PG, Kottke T (2013) Blue-light-induced unfolding of the Jα helix allows for the dimerization of Aureochrome-LOV from the diatom Phaeodactylum tricornutum. Biochemistry 52:3094–3101CrossRefPubMedGoogle Scholar
  32. Hisatomi O, Terauchi K, Zikihara K et al (2013) Blue light-induced conformational changes in a light-regulated transcription factor, Aureochrome-1. Plant Cell Physiol 54:93–106CrossRefPubMedGoogle Scholar
  33. Hisatomi O, Nakatani Y, Takeuchi K, Takahashi F, Kataoka H (2014) Blue light-induced dimerization of monomeric Aureochrome-1 enhances its affinity for the target sequence. J Biol Chem 289:17379–17391PubMedCentralCrossRefPubMedGoogle Scholar
  34. Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–2123CrossRefPubMedGoogle Scholar
  35. Huang Y, Wang L, Zheng M, Zheng M, Tong Y, Li Y (2014) Overexpression of NgAUREO1, the gene coding for aurechrome 1 from Nannochloropsis gaditana, into Saccharomyces cerevisiae leads to a 1.6-fold increase in lipid accumulation. Biotech Lett 36:575–579CrossRefGoogle Scholar
  36. Hurd AM (1920) Effect of unilateral monochromatic light and group orientation on the polarity of geminating Fucus spore. Bot Gaz 70:25–50CrossRefGoogle Scholar
  37. Huysman MJJ, Martens C, Vandepoele K et al (2010) Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling. Genome Biol 11:e1003064CrossRefGoogle Scholar
  38. Huysman MJJ, Fortunato AE, Matthijs M et al (2013) AUREOCHROME1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in diatoms (Phaeodactylum tricornutum). Plant Cell 25:215–228PubMedCentralCrossRefPubMedGoogle Scholar
  39. Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89PubMedCentralCrossRefPubMedGoogle Scholar
  40. Iseki M, Matsunaga S, Murakami A et al (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051CrossRefPubMedGoogle Scholar
  41. Ishikawa M, kataoka H, Takahashi F (2012) Analysis of light -dependent cell morphology and an accumulation response in Ochromonas danica. Cytologia 77:465–474CrossRefGoogle Scholar
  42. Ishikawa M, Takahashi F, Nozaki H, Nagasato C, Motomura T, Kataoka H (2009) Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes. Planta 230:543–552CrossRefPubMedGoogle Scholar
  43. Jaffe LF (1958) Tropistic responses of zygotes of the Fucaceae to polarized light. Exp Cell Res 15:282–299CrossRefPubMedGoogle Scholar
  44. Jakoby M, Weisshaar B, Dröge-Laser W et al (2002) bZIP transcription factor Arabidopsis. Trends Plant Sci 7:106–111CrossRefPubMedGoogle Scholar
  45. Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954CrossRefPubMedGoogle Scholar
  46. Kadota A, Yamada N, Suetsugu et al (2008) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106:13106–13111CrossRefGoogle Scholar
  47. Kagawa T, Sakai T, Suetsugu N et al (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141CrossRefPubMedGoogle Scholar
  48. Kagawa T, Kasahara M, Abe T, Yoshida S, Wada M (2004) Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol 45:416–426CrossRefPubMedGoogle Scholar
  49. Kasahara M, Swartz TE, Olney MA et al (2002) Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, Rice, and Chlamydomonas reinhardtii. Plant Physiol 129:762–773PubMedCentralCrossRefPubMedGoogle Scholar
  50. Kasahara M, Trii M, Fujita A, Tainaka K (2010) FMN binding and photochemical properties of plant putative photoreceptors containing two LOV domains, LOV/LOV proteins. J Biol Chem 285:34765–34772PubMedCentralCrossRefPubMedGoogle Scholar
  51. Kashojiya S, Okajima K, Shimada T, Tokutomi S (2015) Essential role of the A’α/Aβ gap in the N-terminal upstream of LOV2 for the blue light signaling from LOV2 to kinase in Arabidopsis photototropin1, a plant blue light receptor. PLoS One 10:e0124284PubMedCentralCrossRefPubMedGoogle Scholar
  52. Kataoka H (1975a) Phototropism in Vaucheria geminata I. The action spectrum. Plant Cell Physiol 16:427–437Google Scholar
  53. Kataoka H (1975b) Phototropism in Vaucheria geminate II. The mechanism of bending and branching. Plant Cell Physiol 16:439–448Google Scholar
  54. Kataoka H (1977) Second positive- and negative phototropism in Vaucheria geminate. Plant Cell Physiol 18:473–476Google Scholar
  55. Kataoka H (1981) Expansion of Vaucheria cell apex caused by blue or red light. Plant Cell Physiol 22:583–595Google Scholar
  56. Kataoka H (1988) Negative phototropism in Vaucheria terrestris regulated by calcium I. Dependence on background blue light and external calcium concentration. Plant Cell Physiol 29:1323–1330Google Scholar
  57. Kataoka H, Watanabe M (1993) Negative phototropism in Vaucheria terrestris regulated by calcium III. The role of calcium characterized by use of a high-power argon-ion laser as the source of unilateral blue light. Plant Cell Physiol 34:737–744Google Scholar
  58. Kawai H, Müller DG, Fölster E, Häder DP (1990) Phototactic responses in the gametes of the brown alga, Ectocarpus siliculosus. Planta 182:292–297CrossRefPubMedGoogle Scholar
  59. Kawai H, Kubota M, Kondo T, Watanabe M (1991) Action spectra for phototaxis in zoospores of the brown alga Pseudochorda gracilis. Planta 161:17–22Google Scholar
  60. Kerruth S, Ataka K, Frey D, Schlichting I, Heberle J (2014) Aureochrome 1 illuminated: structural changes of a transcription factor probed by molecular spectroscopy. PLoS One 9:e103307PubMedCentralCrossRefPubMedGoogle Scholar
  61. Kicherer R (1985) Endogene und Blaulicht-induzierte Ionenströme bei der Alge Vaucheria sessilis. p. 59. Dissertation to Universität Erlangen-NürnbergGoogle Scholar
  62. Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki KI (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660CrossRefPubMedGoogle Scholar
  63. Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Mol Biol Rev 56:316–339Google Scholar
  64. Mitra D, Yang X, Moffat K (2012) Crystal structures of Aureochrome1 LOV suggest new design strategies for optogenetics. Structure 20:698–706PubMedCentralCrossRefPubMedGoogle Scholar
  65. Mohr H (1980) Interaction between blue light and phytochrome in photomorphogenesis. In: Senger H (ed) “The Blue Light Syndrome”. Springer, New York, pp 97–109CrossRefGoogle Scholar
  66. Mouget J-L, Rosa P, Vachoux C, Tremblin G (2005) Enhancement of marennine production by blue light in the diatom Haslea ostrearia. J Appl Phycol 17:437–445CrossRefGoogle Scholar
  67. Müller S, Clauss H (1976) Aspects of photomorphogenesis in the brown alga Dictyota dichotoma. Z Pflanzenphysiol 78:461–465CrossRefGoogle Scholar
  68. Nagel G, Ollig D, Fuhrmann M et al (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398CrossRefPubMedGoogle Scholar
  69. Nakatani Y, Hisatomi O (2015) Molecular mechanism of photozipper, a light-regulated dimerizing module consisting of the bZIP and LOV domains of Aureochrome-1. Biochemistry 54:3302–3313CrossRefPubMedGoogle Scholar
  70. Nash AI, McNulty R, Shillito ME et al (2011) Structural basis of photosensitivity in a bacterial light-oxygen-voltage/helix-turn-helix (LOV-HTH) DNA-binding protein. Proc Natl Acad Sci USA 108:9449–9454PubMedCentralCrossRefPubMedGoogle Scholar
  71. Oikawa K, Kasahara M, Kiyosue T et al (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815PubMedCentralCrossRefPubMedGoogle Scholar
  72. Olson RJ, Vaulot D, Chisholm SW (1986) Effects of environmental stresses on the cell cycle of two marine phytoplankton species. Plant Physiol 80:918–925PubMedCentralCrossRefPubMedGoogle Scholar
  73. Oltmanns F (1892) Über die photometrischen Bewegungen der Pflanzen. Flora (Jena) 75:183–266Google Scholar
  74. Rosenvinge MLK (1889) Influence des agents extérieurs sur l’organisation polaire et dorsiventrale des plantes. Rev Gen Bot 1:53–62Google Scholar
  75. Sakai T, Kagawa T, Kasahara M et al (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974PubMedCentralCrossRefPubMedGoogle Scholar
  76. Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735PubMedCentralCrossRefPubMedGoogle Scholar
  77. Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen-Chromatophoren. Wilhelm-Engelmann, LeipzigGoogle Scholar
  78. Shikata T, Matsunaga S, Iseki M et al (2013) Blue light regulates the rhythm of diurnal vertical migration in the raphidophyte red-tide alga Chattonella antiqua. J Plankton Res 35:542–552CrossRefGoogle Scholar
  79. Takahashi F, Hishinuma T, Kataoka H (2001) Blue light-induced branching in Vaucheria. requirement of nuclear accumulation in the irradiated region. Plant Cell Physiol 42:274–285CrossRefPubMedGoogle Scholar
  80. Takahashi F, Yamaguchi K, Hishinuma T, Kataoka H (2003) Mitosis and mitotic wave propagation in the coenocytic alga, Vaucheria terrestris sensu Goetz. J Plant Res 116:381–387CrossRefPubMedGoogle Scholar
  81. Takahashi F, Yamagata D, Ishikawa M et al (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci USA 104:19625–19630PubMedCentralCrossRefPubMedGoogle Scholar
  82. Tyler BM, Tripathy S, Zhang X et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266CrossRefPubMedGoogle Scholar
  83. Toyooka T, Hisatomi O, Takahashi F, Kataoka H, Terazima M (2011) Photoreactions of Aureochrome-1. Biophys J 100:2801–2809PubMedCentralCrossRefPubMedGoogle Scholar
  84. Vieler A, Wu G, Tsai C-H et al (2012) Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet 8:e1003064PubMedCentralCrossRefPubMedGoogle Scholar
  85. Wang W, Wang F, Sun X, Liu F, Liang Z (2013) Comparison of transcriptome under red and blue light culture of Saccharina japonica (Phaeophyceae). Planta 237:1123–1133CrossRefPubMedGoogle Scholar
  86. Yoshikawa S, Kamiya M, Ohki K (2014) Photoperiodic regulation of receptacle induction in Sargassum horneri (Phaeophyceae) using clonal thalli. Phycol Res 62:206–213CrossRefGoogle Scholar

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© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.College of Life SciencesRitsumeikan UniversityKusatsuJapan

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