CO2-cAMP-responsive cis-elements targeted by a transcription factor with CREB/ATF-like basic zipper domain in the marine diatom Phaeodactylum tricornutum

Plant Physiology

Volumn 158, Issue 1, 2012, Pages 499-513

  Ohno, Naoki ^a   Inoue, Takuya ^a   Yamashiki, Ryosuke ^a   Nakajima, Kensuke ^a   Kitahara, Yuhei ^a   Ishibashi, Mikiko ^a   Matsuda, Yusuke ^a  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLARIOPHYTA; NITZSCHIA ALBA; PHAEODACTYLUM TRICORNUTUM;

EID: 84855279835     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.190249     Document Type: Article

References (68)

1. Arnold R, Burcin M, Kaiser B, Muller M, Renkawitz R (1996) DNA bending by the silencer protein NeP1 is modulated by TR and RXR. Nucleic Acids Res 24: 2640-2647.
2. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CO2-concentrating mechanisms in the algae. Can J Bot 76: 1052-1071.
3. -uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46: 1378-1391.
4. Cann MJ, Hammer A, Zhou J, Kanacher T (2003) A defined subset of adenylyl cyclases is regulated by bicarbonate ion. J Biol Chem 278: 35033-35038.
5. Chen X, Qiu CE, Shao JZ (2006) Evidence for K+-dependent HCO3 2 utilization in the marine diatom Phaeodactylum tricornutum. Plant Physiol 141: 731-736.
6. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289: 625-628.
7. Colman B, Huertas E, Bhatti S, Dason JS (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29: 261-270.
8. Colman B, Rotatore C (1995) Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ 18: 919-924.
9. Deutsch PJ, Hoeffler JP, Jameson JL, Lin JC, Habener JF (1988) Structural determinants for transcriptional activation by cAMP-responsive DNA elements. J Biol Chem 263: 18466-18472.
10. Eriksson M, Villand P, Gardeström P, Samuelsson G (1998) Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 116: 637-641.
11. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, et al (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290: 291-296.
12. Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S (1990) Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 9779-9783.
13. Fukuzawa H, Miura K, Ishizaki K, Kucho KI, Saito T, Kohinata T, Ohyama K (2001) Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proc Natl Acad Sci USA 98: 5347-5352.
14. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 8: 229-239.
15. Hai T, Curran T (1991) Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci USA 88: 3720-3724.
16. Hai T, Hartman MG (2001) The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 273: 1-11.
17. Hammer A, Hodgson DRW, Cann MJ (2006) Regulation of prokaryotic adenylyl cyclases by CO2. Biochem J 396: 215-218.
18. Harada H, Matsuda Y (2005) Identification and characterization of a new carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Can J Bot 83: 909-916.
19. Harada H, Nakajima K, Sakaue K, Matsuda Y (2006) CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol 142: 1318-1328.
20. Harada H, Nakatsuma D, Ishida M, Matsuda Y (2005) Regulation of the expression of intracellular b-carbonic anhydrase in response to CO2 and light in the marine diatom Phaeodactylum tricornutum. Plant Physiol 139: 1041-1050.
21. Harrison PJ, Waters RE, Taylor FJR (1980) A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton. J Phycol 16: 28-35.
22. Hashimoto Y, Zhang C, Kawauchi J, Imoto I, Adachi MT, Inazawa J, Amagasa T, Hai T, Kitajima S (2002) An alternatively spliced isoform of transcriptional repressor ATF3 and its induction by stress stimuli. Nucleic Acids Res 30: 2398-2406.
23. Haze K, Yoshida H, Yanagi H, Yura T, Mori K (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787-3799.
24. Hyman SE, Comb M, Pearlberg J, Goodman HM (1989) An AP-2 element acts synergistically with the cyclic AMP- and phorbol ester-inducible enhancer of the human proenkephalin gene. Mol Cell Biol 9: 321-324.
25. Johnston AM, Raven JA (1996) Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. Eur J Phycol 31: 285-290.
26. Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and intracellular inorganic carbon pool in the blue green alga Anabaena variabilis: response to external CO2 concentration. Planta 149: 219-226.
27. Kitao Y, Matsuda Y (2009) Formation of macromolecular complexes of carbonic anhydrases in the chloroplast of a marine diatom by the action of the C-terminal helix. Biochem J 419: 681-688.
28. Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schröppel K, Naglik JR, Eckert SE, Mogensen EG, Haynes K, Tuite MF, et al (2005) Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15: 2021-2026.
29. Kucho K, Yoshioka S, Taniguchi F, Ohyama K, Fukuzawa H (2003) Cisacting elements and DNA-binding proteins involved in CO2-responsive transcriptional activation of Cah1 encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 133: 783-793.
30. Liu H, Deng X, Shyu YJ, Li JJ, Taparowsky EJ, Hu CD (2006) Mutual regulation of c-Jun and ATF2 by transcriptional activation and subcellular localization. EMBO J 25: 1058-1069.
31. Matsuda Y, Colman B (1995) Induction of CO2 and bicarbonate transport in the green alga Chlorella ellipsoidea: time course of induction of the two systems. Plant Physiol 108: 247-252.
32. Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom, Phaeodactylum tricornutum. Plant Cell Environ 24: 611-620.
33. Matsuda Y, Nakajima K, Tachibana M (2011) Recent progresses on the genetic basis of the regulation of CO2 acquisition systems in response to CO2 concentration. Photosynth Res 109: 191-203.
34. Miller AG, Espie GS, Canvin DT (1990) Physiological aspects of CO2 and HCO3 2 transport by cyanobacteria: a review. Can J Bot 68: 1291-1302.
35. Montminy MR, Sevarino KA, Wagner JA, Mandel G, Goodman RH (1986) Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci USA 83: 6682-6686.
36. Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6: 1251-1259.
37. Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S, Omata T (2008) Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Mol Microbiol 68: 98-109.
38. Nitsch D, Boshart M, Schütz G (1993) Activation of the tyrosine aminotransferase gene is dependent on synergy between liver-specific and hormone-responsive elements. Proc Natl Acad Sci USA 90: 5479-5483.
39. Nomura N, Zu YL, Maekawa T, Tabata S, Akiyama T, Ishii S (1993) Isolation and characterization of a novel member of the gene family encoding the cAMP response element-binding protein CRE-BP1. J Biol Chem 268: 4259-4266.
40. Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183: 1891-1898.
41. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461.
42. Rayko E, Maumus F, Maheswari U, Jabbari K, Bowler C (2010) Transcription factor families inferred from genome sequences of photosynthetic stramenopiles. New Phytol 188: 52-66.
43. Rehfuss RP, Walton KM, Loriaux MM, Goodman RH (1991) The cAMPregulated enhancer-binding protein ATF-1 activates transcription in response to cAMP-dependent protein kinase A. J Biol Chem 266: 18431-18434.
44. Reinfelder JR, Milligan AJ, Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135: 2106-2111.
45. Ribeiro A, Brown A, Lee KAW (1994) An in vivo assay for members of the cAMP response element-binding protein family of transcription factors. J Biol Chem 269: 31124-31128.
46. Rikitake Y, Moran E (1992) DNA-binding properties of the E1A-associated 300-kilodalton protein. Mol Cell Biol 12: 2826-2836.
47. Roberts K, Granum E, Leegood RC, Raven JA (2007) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145: 230-235.
48. Roesler WJ, Graham JG, Kolen R, Klemm DJ, McFie PJ (1995) The cAMP response element binding protein synergizes with other transcription factors to mediate cAMP responsiveness. J Biol Chem 270: 8225-8232.
49. Rotatore C, Colman B (1992) Active uptake of CO2 by the diatom Navicula pelliculosa. J Exp Bot 43: 571-576.
50. Satoh D, Hiraoka Y, Colman B, Matsuda Y (2001) Physiological and molecular biological characterization of intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol 126: 1459-1470.
51. Schumacher MA, Goodman RH, Brennan RG (2000) The structure of a CREB bZIP.somatostatin CRE complex reveals the basis for selective dimerization and divalent cation-enhanced DNA binding. J Biol Chem 275: 35242-35247.
52. Spalding MH (2008) Microalgal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters. J Exp Bot 59: 1463-1473.
53. Sültemeyer D (1998) Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot 76: 962-972.
54. Tachibana M, Allen AE, Kikutani S, Endo Y, Bowler C, Matsuda Y (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth Res 109: 205-221.
55. Tanaka Y, Nakatsuma D, Harada H, Ishida M, Matsuda Y (2005) Localization of soluble b-carbonic anhydrase in the marine diatom Phaeodactylum tricornutum: sorting to the chloroplast and cluster formation on the girdle lamellae. Plant Physiol 138: 207-217.
56. Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T, Ishii S (1997) Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc Natl Acad Sci USA 94: 10215-10220.
57. Thoms S, Pahlow M, Gladrow DAW (2001) Model of the carbon concentrating mechanism in chloroplasts of eukaryotic algae. J Theor Biol 208: 295-313.
58. Tréguer P, Nelson DM, Van Bennekom AJ, Demaster DJ, Leynaert A, Quéguiner B (1995) The silica balance in the world ocean: a reestimate. Science 268: 375-379.
59. Trimborn S, Lundholm N, Thoms S, Richter KU, Krock B, Hansen PJ, Rost B (2008) Inorganic carbon acquisition in potentially toxic and nontoxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiol Plant 133: 92-105.
60. Vance P, Spalding MH (2005) Growth, photosynthesis and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states. Can J Bot 83: 796-809.
61. van Dam H, Wilhelm D, Herr I, Steffen A, Herrlich P, Angel P (1995) ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J 14: 1798-1811.
62. Vinson C, Myakishev M, Acharya A, Mir AA, Moll JR, Bonovich M (2002) Classification of human B-ZIP proteins based on dimerization properties. Mol Cell Biol 22: 6321-6335.
63. Walker AK, See R, Batchelder C, Kophengnavong T, Gronniger JT, Shi Y, Blackwell TK (2000) A conserved transcription motif suggesting functional parallels between Caenorhabditis elegans SKN-1 and Cap'n'Collarrelated basic leucine zipper proteins. J Biol Chem 275: 22166-22171.
64. Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279: 5739-5751.
65. Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman RJ, Prywes R (2000) Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem 275: 27013-27020.
66. Yoshioka S, Taniguchi F, Miura K, Inoue T, Yamano T, Fukuzawa H (2004) The novel Myb transcription factor LCR1 regulates the CO2-responsive gene Cah1, encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Cell 16: 1466-1477.
67. Xiang Y, Zhang J, Weeks DP (2001) The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 98: 5341-5346.
68. Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE (2000) Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36: 379-386.