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Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes

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Abstract

The new type blue light (BL) receptor aureochrome (AUREO) was recently discovered in a stramenopile alga, Vaucheria (Takahashi et al. Proc Natl Acad Sci USA 104(49):19625–19630, 2007). AUREO has a bZIP (basic region/leucine zipper) and BL-sensing light-oxygen-voltage (LOV) domain and functions as a BL-activated transcription factor. It mediates BL-induced branching and regulates the development of the sex organ in V. frigida. Although AUREO sequences have previously been found in Fucus and some diatoms, here we report that AUREO orthologs are commonly conserved in photosynthetic stramenopiles. Five AUREO orthologs were isolated from three stramenopile genera (Fucus, Ochromonas, and Chattonella). By BLAST search, several AUREO sequences were also detected in genomes in Aureococcus anophagefferens (Pelagophyceae). However, AUREO was not found in heterotrophic stramenopiles or in closely related phyla, such as haptophytes and cryptophytes, or in green plants. Stramenopiles do not possess phototropin, the well-known BL receptor for phototropism of green plants. From comparative analysis of LOV domains, together with kinship analysis of AUREO bZIP domains, AUREO can be regarded as the BL receptor specific to phototrophic stramenopiles. The evolution of AUREO and the phylogeny of LOV domains in stramenopiles and green plants are discussed.

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Abbreviations

AUREO:

Aureochrome

BL:

Blue light

bZIP:

Basic region/leucine zipper

LOV:

Light-oxygen-voltage

NPH:

Nonphototropic hypocotyl

PAS:

Per-ARNT-Sim

PHOT:

Phototropin

VVD:

Vivid

WC-1:

White collar-1

References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Abe M (1970) A method of inducing egg liberation in Fucus evanescens. Bot Mag Tokyo 83:254–255

    Google Scholar 

  • Adachi J, Waddell PJ, Martin W, Hasegawa M (2000) Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J Mol Evol 50:348–358

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bouget F-Y, Berger F, Brownlee C (1998) Position dependent control of cell fate in the Fucus embryo: role of intercellular communication. Development 125:1999–2008

    PubMed  CAS  Google Scholar 

  • Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  PubMed  CAS  Google Scholar 

  • Briggs WR, Beck CF, Cashmore AR et al (2001) The phototropin family of photoreceptors. Plant Cell 13:993–997

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182

    Article  PubMed  CAS  Google Scholar 

  • Crosson S, Moffat K (2001) Structure of flavin-binding plant photoreceptor domain: insights into light-mediated signal transduction. Proc Natl Acad Sci USA 98:2995–3000

    Article  PubMed  CAS  Google Scholar 

  • Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2–10

    Article  PubMed  CAS  Google Scholar 

  • Fischer-Arnold G (1963) Untersuchungen über die Chloroplastenbewegung bei Vaucheria sessilis. Protoplasma 56:495–520

    Article  CAS  Google Scholar 

  • Froehlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297:815–819

    Article  PubMed  CAS  Google Scholar 

  • Grinberg A, Heath IB (1997) Direct evidence for Ca2+ regulation of hyphal branch induction. Fungal Genet Biol 22:127–139

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hadley R, Hable WE, Kropf DL (2006) Polarization of the endomembrane system is an early event in fucoid zygote development. BMC Plant Biol 6:5

    Article  PubMed  Google Scholar 

  • Haupt W, Schönfeld I (1962) Über das Wirkungsspektrum der “negativen Phototaxis” der Vaucheria-Chloroplasten. Ber Dtsch Bot Ges 75:14–23

    Google Scholar 

  • He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y (2002) White collar-1, a DNA binding transcription factor and light sensor. Science 297:840–843

    Article  PubMed  CAS  Google Scholar 

  • Hegemann P (2008) Algal sensory photoreceptors. Annu Rev Plant Biol 59:167–189

    Article  PubMed  CAS  Google Scholar 

  • 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 104:453–464

    Article  PubMed  CAS  Google Scholar 

  • Huala E, Oeller PW, Liscum E, Han I-S, Larsen E, Briggs WR (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278:2120–2123

    Article  PubMed  CAS  Google Scholar 

  • Imaizumi T, Kanegae T, Wada M (2000) Cryptochrome nucleocytoplasmic distribution and gene expression are regulated by light quality in the fern Adiantum capillus-veneris. Plant Cell 12:81–95

    Article  PubMed  CAS  Google Scholar 

  • Inoue S, Kinoshita T, Takemiya A, Doi M, Shimazaki K (2008) Leaf positioning of Arabidopsis in response to blue light. Mol Plant 1:15–26

    Article  CAS  Google Scholar 

  • Jaffe LF (1958) Tropistic responses of zygotes of the Fucaceae to polarized light. Exp Cell Res 15:282–299

    Article  PubMed  CAS  Google Scholar 

  • Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  PubMed  CAS  Google Scholar 

  • Kagawa T (2003) The phototropin family as photoreceptors for blue light-induced chloroplast relocation. J Plant Res 116:77–82

    PubMed  CAS  Google Scholar 

  • Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  PubMed  CAS  Google Scholar 

  • Kataoka H (1975a) Phototropism in Vaucheria geminata I. The action spectrum. Plant Cell Physiol 16:427–437

    Google Scholar 

  • Kataoka H (1975b) Phototropism in Vaucheria geminate II. The mechanism of bending and branching. Plant Cell Physiol 16:439–448

    Google Scholar 

  • Kataoka H (1987) The light growth response of Vaucheria. A conditio sine qua non of the phototropic response? Plant Cell Physiol 28:61–71

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

    Article  PubMed  CAS  Google Scholar 

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  PubMed  CAS  Google Scholar 

  • Lee K, Loros JJ, Dunlap JC (2000) Interconnected feedback loops in the Neurospora circadian system. Science 289:107–110

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka D, Tokutomi S (2005) Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc Natl Acad Sci USA 102:13337–13342

    Article  PubMed  CAS  Google Scholar 

  • Motomura T (1994) Electron and immunofluorescence microscopy on the fertilization of Fucus distichus (Fucales, Phaeophyceae). Protoplasma 178:97–110

    Article  Google Scholar 

  • Nozaki H, Ito M, Watanabe MM, Takano H, Kuroiwa T (1997) Phylogenetic analysis of morphological species of Carteria (Volvocales, Chlorophyta) based on rbcL gene sequences. J Phycol 33:864–867

    Article  Google Scholar 

  • Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh KC, Lagarias JC, Wada M (1998) A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci USA 95:15826–15830

    Article  PubMed  CAS  Google Scholar 

  • Oltmanns F (1892) Über die photometrischen Bewegungen der Pflanzen. Flora (Jena) 75:183–266

    Google Scholar 

  • Pearson G, Serrāo EA, Cancela ML (2001) Suppression subtractive hybridization for studying gene expression during aerial exposure and desiccation in fucoid algae. Eur J Phycol 36:359–366

    Article  Google Scholar 

  • Rosenvinge MLK (1889) Influence des agents extérieurs sur l’organisation polaire et dorsiventrale des plantes. Rev Gen Bot 1:53–62

    Google Scholar 

  • Saitou N, Nei M (1998) The Neighbor-joining method: a new method for reconstracting phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735

    Article  PubMed  CAS  Google Scholar 

  • Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39:9401–9410

    Article  PubMed  CAS  Google Scholar 

  • Schindler U, Menkens AE, Beckmamm H, Ecker JR, Cashmore AR (1992) Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. EMBO J 11:1261–1273

    PubMed  CAS  Google Scholar 

  • Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen-Chromatophoren. Wilhelm-Engelmann, Leipzig

    Google Scholar 

  • Suetsugu N, Mittmann F, Wagner G, Hughes J, Wada M (2005) A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc Natl Acad Sci USA 38:13705–13709

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10 (Alvitec). Sinauer Associates, Sunderland

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, Kasahara M, Kiyosue T, Kikuyama M, Wada M, Kataoka H (2007) AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci USA 104(49):19625–19630

    Article  PubMed  CAS  Google Scholar 

  • Teyler BM, Tripathy S, Zhang X et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Nature 313:1261–1266

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Yanovsky MJ, Kay SA (2003) Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4:265–275

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastid. Proc Natl Acad Sci USA 99:15507–15512

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Akiko Yokoyama (Yamagata University, Yamagata, Japan) for helpful advice in construction of phylogenetic trees. We are also grateful to Dr. Ian Gleadall (Tohoku Bunka Gakuen University, Sendai, Japan) for his critical comments on the manuscript. This work was partially supported by Ministry of Education, Sports, Science, and Technology of Japan Grant #17084001 (to H.K.), and by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists (to M.I.).

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Correspondence to Mié Ishikawa.

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Ishikawa, M., Takahashi, F., Nozaki, H. et al. Distribution and phylogeny of the blue light receptors aureochromes in eukaryotes. Planta 230, 543–552 (2009). https://doi.org/10.1007/s00425-009-0967-6

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