Abstract
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.
Similar content being viewed by others
Abbreviations
- AUREO:
-
Aureochrome
- BL:
-
Blue light
- bZIP:
-
Basic leucine zipper
- LOV:
-
Light-oxygen-voltage
References
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 52:399–451
Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166
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 287:9901–9909
Blatt MR (1983) The action spectrum for chloroplast movements and evidence for blue-light-photoreceptor cycling in the alga Vaucheria. Planta 159:267–276
Blatt MR, Briggs WR (1980) Blue-light-induced cortical fiber reticulation concomitant with chloroplast aggregation in the alga Vaucheria sessilis. Planta 147:355–362
Blatt MR, Wessells NK, Briggs WR (1980) Actin and cortical fiber reticulation in the siphonaceous alga Vaucheria sessilis. Planta 147:363–375
Buggeln RG (1974) Negative phototropism of the haptera of Alaria esculenta (Laminarieales). J Phycol 10:80–82
Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57:953–994
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 105:20038–20043
Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45
Christie JM, Reymond P, Powell GK et al (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698–1701
Christie JM, Swartz TE, Bongmolni RA, Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32:205–219
Clauss H (1971) Wachstum von Dictyota dichotoma in Rot- und Blaulicht. Naturwissenschaften 58:272
Cock JM, Sterck L, Rouzé P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621
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 64:483–493
Costa BS, Sachse M, Jungandreas A et al (2013b) Aureochrome 1a is involved in the photoacclimation of the diatom Phaeodactylum tricornutum. PLoS One 8:e74451
Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2–10
Dring MJ, Lüning K (1975a) A photoperiodic response mediated by blue light in the brown alga Scytosiphon lomentaria. Planta 125:25–32
Dring MJ, Lüning K (1975b) Induction of two-dimensional growth and hair formation by blue light in the brown alga Scytosiphon lomentaria. Z Pflanzenphysiol 75:107–117
Fischer-Arnold (1963) Untersuchungen über die Chloroplastenbewegung bei Vaucheria sessilis. Protoplasma 56:495–520
Fu G, Nagasato C, Yamagishi T, Oka S, Cock JM, Motomura T (2014) Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 165:662–675
Furukawa T, Watanabe M, Shihira-Ishikawa I (1998) Green- and blue-light-mediated chloroplast migration in the centric diatom Pleurosira laevis. Protoplasma 203:214–220
Furuya M (1993) Phytochromes: their molecular species, gene families, and functions. Annu Rev Plant Physiol 44:617–645
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 124:331–342
Grusch M, Schelch K, Riedler et al (2014) Spatio-temporally precise activation of engineered receptor tyrosine kinases by light. EMBO J 33:1713–1726
Häder DP, Colombetti G, Leuci F, Quaglia M (1981) Phototaxis in flagellates, Euglena gracilis and Ochromonas danica. Arch Microbiol 130:78–82
Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301:1541–1544
Haupt W, Schönfeld I (1962) Über das Wirkungsspektrum der “negative Phototaxis” der Vaucheria-Chloroplasten. Ber Dtsch Bot Ges 75:14–23
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 297:840–843
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 54:1484–1492
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 52:3094–3101
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 54:93–106
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 289:17379–17391
Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–2123
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 36:575–579
Hurd AM (1920) Effect of unilateral monochromatic light and group orientation on the polarity of geminating Fucus spore. Bot Gaz 70:25–50
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:e1003064
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 25:215–228
Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89
Iseki M, Matsunaga S, Murakami A et al (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051
Ishikawa M, kataoka H, Takahashi F (2012) Analysis of light -dependent cell morphology and an accumulation response in Ochromonas danica. Cytologia 77:465–474
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 230:543–552
Jaffe LF (1958) Tropistic responses of zygotes of the Fucaceae to polarized light. Exp Cell Res 15:282–299
Jakoby M, Weisshaar B, Dröge-Laser W et al (2002) bZIP transcription factor Arabidopsis. Trends Plant Sci 7:106–111
Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954
Kadota A, Yamada N, Suetsugu et al (2008) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106:13106–13111
Kagawa T, Sakai T, Suetsugu N et al (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141
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 45:416–426
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 129:762–773
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 285:34765–34772
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:e0124284
Kataoka H (1975a) Phototropism in Vaucheria geminata I. The action spectrum. Plant Cell Physiol 16:427–437
Kataoka H (1975b) Phototropism in Vaucheria geminate II. The mechanism of bending and branching. Plant Cell Physiol 16:439–448
Kataoka H (1977) Second positive- and negative phototropism in Vaucheria geminate. Plant Cell Physiol 18:473–476
Kataoka H (1981) Expansion of Vaucheria cell apex caused by blue or red light. Plant Cell Physiol 22:583–595
Kataoka H (1988) Negative phototropism in Vaucheria terrestris regulated by calcium I. Dependence on background blue light and external calcium concentration. Plant Cell Physiol 29:1323–1330
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 34:737–744
Kawai H, Müller DG, Fölster E, Häder DP (1990) Phototactic responses in the gametes of the brown alga, Ectocarpus siliculosus. Planta 182:292–297
Kawai H, Kubota M, Kondo T, Watanabe M (1991) Action spectra for phototaxis in zoospores of the brown alga Pseudochorda gracilis. Planta 161:17–22
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:e103307
Kicherer R (1985) Endogene und Blaulicht-induzierte Ionenströme bei der Alge Vaucheria sessilis. p. 59. Dissertation to Universität Erlangen-Nürnberg
Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki KI (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660
Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Mol Biol Rev 56:316–339
Mitra D, Yang X, Moffat K (2012) Crystal structures of Aureochrome1 LOV suggest new design strategies for optogenetics. Structure 20:698–706
Mohr H (1980) Interaction between blue light and phytochrome in photomorphogenesis. In: Senger H (ed) “The Blue Light Syndrome”. Springer, New York, pp 97–109
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 17:437–445
Müller S, Clauss H (1976) Aspects of photomorphogenesis in the brown alga Dictyota dichotoma. Z Pflanzenphysiol 78:461–465
Nagel G, Ollig D, Fuhrmann M et al (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398
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 54:3302–3313
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 108:9449–9454
Oikawa K, Kasahara M, Kiyosue T et al (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815
Olson RJ, Vaulot D, Chisholm SW (1986) Effects of environmental stresses on the cell cycle of two marine phytoplankton species. Plant Physiol 80:918–925
Oltmanns F (1892) Über die photometrischen Bewegungen der Pflanzen. Flora (Jena) 75:183–266
Rosenvinge MLK (1889) Influence des agents extérieurs sur l’organisation polaire et dorsiventrale des plantes. Rev Gen Bot 1:53–62
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 98:6969–6974
Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735
Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen-Chromatophoren. Wilhelm-Engelmann, Leipzig
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 35:542–552
Takahashi F, Hishinuma T, Kataoka H (2001) Blue light-induced branching in Vaucheria. requirement of nuclear accumulation in the irradiated region. Plant Cell Physiol 42:274–285
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 116:381–387
Takahashi F, Yamagata D, Ishikawa M et al (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci USA 104:19625–19630
Tyler BM, Tripathy S, Zhang X et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266
Toyooka T, Hisatomi O, Takahashi F, Kataoka H, Terazima M (2011) Photoreactions of Aureochrome-1. Biophys J 100:2801–2809
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:e1003064
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 237:1123–1133
Yoshikawa S, Kamiya M, Ohki K (2014) Photoperiodic regulation of receptacle induction in Sargassum horneri (Phaeophyceae) using clonal thalli. Phycol Res 62:206–213
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Takahashi, F. Blue-light-regulated transcription factor, Aureochrome, in photosynthetic stramenopiles. J Plant Res 129, 189–197 (2016). https://doi.org/10.1007/s10265-016-0784-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-016-0784-5