Evolutionary origins and functions of the carotenoid biosynthetic pathway in marine diatoms

PLoS ONE

Volumn 3, Issue 8, 2008, Pages

  Coesel, Sacha ^a,e   Oborník, Miroslav ^b   Varela, Joao ^c   Falciatore, Angela ^a   Bowler, Chris ^a,d  

^a STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c UNIVERSITY OF ALGARVE   (Portugal)

^d ECOLE NORMALE SUPÉRIEURE   (France)

^e INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VIOLAXANTHIN DEEPOXIDASE; XANTHOPHYLL; ZEAXANTHIN EPOXIDASE; OXIDOREDUCTASE; SEA WATER; VIOLAXANTHIN DE EPOXIDASE; VIOLAXANTHIN DE-EPOXIDASE;

ARTICLE; CILIATE; CONTROLLED STUDY; DIATOM; ENDOSYMBIOSIS; ENZYME ACTIVITY; ENZYME ANALYSIS; EUKARYOTE; GENE EXPRESSION PROFILING; GENE TRANSFER; GENOME ANALYSIS; GREEN ALGA; HIGHER PLANT; LIGHT HARVESTING SYSTEM; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TETRAHYMENA THERMOPHILA; AMINO ACID SEQUENCE; BIOSYNTHESIS; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

ALGAE; BACILLARIOPHYTA; CHLOROPHYTA; CHROMALVEOLATA; CHROMISTA; CILIOPHORA; EMBRYOPHYTA; EUKARYOTA; NITZSCHIA ALBA; PHAEODACTYLUM TRICORNUTUM; PLANTAE; TETRAHYMENA THERMOPHILA;

AMINO ACID SEQUENCE; CAROTENOIDS; CONSERVED SEQUENCE; DIATOMS; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; SEAWATER; SEQUENCE ALIGNMENT;

EID: 51649110735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002896     Document Type: Article

References (73)

1. Nelson DM, Tréguer P, Brzezinski MA, Leynaert B, Quéguiner B (1995) Production and dissolution of biogenic silica in the ocean-Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cycles 9: 359-372.
2. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237-240.
3. Mann DG (1999) The species concept in diatoms. Phycologia 38: 437-495.
4. Kooistra WH, De Stefano M, Mann DG, Medlin LK (2003) The phylogeny of the diatoms. Prog Mol Subcell Biol 33: 59-97.
5. Kooistra WH, Gersonde R, Medlin LK, Mann DG (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence; Falkowski PG, Knoll AH, eds. Amsterdam: Academic Press-Elsevier. 480 p.
6. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, et al. (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79-86.
7. Allen AE, Vardi A, Bowler C (2006) An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms. Curr Opin Plant Biol 9: 264-273.
8. Montsant A, Allen AE, Coesel S, De Martino A, Falciatore A, et al. (2007) Identification and comparative genomic analysis of signaling and regulatory components in the diatom Thalassiosira pseudonana. J Phycol 43: 585-604.
9. Siaut M, Heijde M, Mangogna M, Montsant A, Coesel S, et al. (2007) Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene 406: 23-35.
10. Falciatore A, Bowler C (2002) Revealing the molecular secrets of marine diatoms. Annu Rev Plant Biol 53: 109-130.
11. Maheswari U, Montsant A, Goll J, Krishnasamy S, Rajyashri KR, et al. (2005) The Diatom EST Database. Nucleic Acids Res 33: D344-347.
12. Montsant A, Jabbari K, Maheswari U, Bowler C (2005) Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Physiol 137: 500-513.
13. Li S, Nosenko T, Hackett JD, Bhattacharya D (2006) Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates. Mol Biol Evol 23: 663-674.
14. Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3: 1169-1175.
15. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21: 809-818.
16. Cavalier-Smith T (1981) Eukaryote kingdomes seven or nine? Biosystems 14: 461-481.
17. MacIntyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5: 12-17.
18. Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431: 689-692.
19. Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169: 95-108.
20. Ruban A, Lavand J, Rousseau B, Guglielmi G, Horton P, et al. (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82: 165-175.
21. Lavaud J, Rousseau B, Etienne AL (2003) Enrichment of the light-harvesting complex in diadinoxanthin and implications For the nonphotochemical fluorescence quenching in diatoms. Biochemistry 42: 5802-5808.
22. Falkowski PG, Laroche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27: 8-14.
23. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566.
24. Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43: 8281-8289.
25. Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56: 375-382.
26. Hager A (1969) Lichtbedingte pH-erniedrigung in einem chloroplastem-kompatiment als ursache der enzymatische violaxanthin- zu zeaxanthin-umwandlung; Beziehungen zur photophosphorylierung. Planta 89: 224-243.
27. Yamamoto HY, Kamite L, Wang YY (1972) An ascorbate-induced absorbance change in chloroplasts from violaxanthin de-epoxidation. Plant Physiol 49: 224-228.
28. Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci U S A 93: 6320-6325.
29. Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, et al. (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. Embo J 15: 2331-2342.
30. Lavaud J, Rousseau B, Etienne AL (2002) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523: 163-166.
31. Lavaud J, Rousseau B, van Gorkom HJ, Etienne AL (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129: 1398-1406.
32. Olaizola M, La Roche J, Kolber Z, Falkowski P (1994) Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res 41: 357-370.
33. Stransky H, Hager A (1970) Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyllcyclus in verschiedenen Algenklassen. Arch Microbiol 73: 315-323.
34. Emanuelsson O, Brunak S, voa Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
35. Plundel EE, Renganathan M, Gilmore AM, Yamamoto HY, Dilley RA (1994) Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin de-epoxidation. Plant Physiol 106: 1647-1658.
36. Hieber AD, Bugos RC, Verhoeven AS, Yamamoto HY (2002) Overexpression of violaxanthin de-epoxidase: properties of C-terminal deletions on activity and pH-dependent lipid binding. Planta 214: 476-483.
37. Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134.
38. Bugos RC, Hieber AD, Yamamoto HY (1998) Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Chem 273: 15321-15324.
39. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318 (Pt I): 1-14.
40. Hager A, Holocher K (1994) Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 192: 581-589.
41. Grouneva I, Jakob T, Wilhelm C, Goss R (2006) Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol Plant 126: 205-211.
42. Jakob T, Goss R, Wilhelm C (2001) Unusual pH-dependence of diadinoxanthin de-epoxidase activation causes chlororespiratory induced accumulation of diatoxanthin in the diatom Phaeodactylum tricornutum. J Plant Physiol 158: 383-390.
43. Goss R (2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217: 801-812.
44. Hieber AD, Bugos RC, Yamamoto HY (2000) Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. Biochim Biophys Acta 1482: 84-91.
45. Charron JB, Ouellet F, Pelletier M, Danyluk J, Chauve C, et al. (2005) Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol 139: 2017-2028.
46. Ganfornina MD, Gutierrez G, Bastiani M, Sanchez D (2000) A phytogenetic analysis of the lipocalin protein family. Mol Biol Evol 17; 114-126.
47. Salier JP (2000) Chromosomal location, exon/intron organization and evolution of lipocalin genes. Biochim Biophys Acta 1482: 25-34.
48. Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, et al. (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 181-201.
49. Joshua S, Bailey S, Mann NH, Mullineaux CW (2005) Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiol 138: 1577-1585.
50. Marquardt J, Hanelt D (2004) Carotenoid composition of Delesseria lancifolia and other marine red algae from polar and temperate habitats. Eur J Phycol 39: 285-292.
51. Schubert N, Garcia-Mendoza E, Pacheco-Ruiz I (2006) Carotenoid composition of marine red algae. J Phycol 42: 1208-1216.
52. Bouvier F, d'Harlingue A, Hugueney P, Marin E, Marion-Poll A, et al. (1996) Xanthophyll biosynthesis. Cloning, expression, functional reconstitution, and regulation of beta-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). J Biol Chem 271: 28861-28867.
53. Goss R, Ann Pinto E, Wilhelm C, Richter M (2006) The importance of a highly active and DeltapH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163: 1008-1021.
54. Mewes H, Richter M (2002) Supplementary ultraviolet-B radiation induces a rapid reversal of the diadinoxanthin cycle in the strong light-exposed diatom Pnaeodactylum tricornutum. Plant Physiol 130: 1527-1535.
55. Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci U S A 96: 8784-8789.
56. Lohr M, Wilhelm C (2001) Xanthophyll synthesis in diatoms: quantification of putative intermediates and comparison of pigment conversion kinetics with rate constants derived from a model. Planta 212: 382-391.
57. Wilhelm C, Bachel C, Fisahn J, Goss R, Jakob T, et al. (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157: 91-124.
58. Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110: 689-696.
59. Green RM, Geider RJ, Falkowski PG (1991) Effect of iron limitation on photosynthesis in a marine diatom. Limnol Oceanogr 36: 1772-1782.
60. Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54: 539-547.
61. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739-759.
62. Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand A (2007) Genomewide gene expression analysis reveals a critical role for cryptochromel in the response of Arabidopsis to high irradiance. Plant Physiol 141: 1391-1406.
63. Leblanc C, Falciatore A, Watanabe M, Bowler C (1999) Semi-quantitative RT-PCR analysis of photoregulated gene expression in marine diatoms. Plant Mol Biol 40: 1031-1044.
64. Bohne F, Linden H (2002) Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinbardtii. Biochim Biophys Acta 1579: 26-34.
65. Im CS, Eberhard S, Huang K, Beck CF, Grossman AR (2006) Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J 48: 1-16.
66. von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, et al. (1997) Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis, thaliana seedlings. Plant J 12: 625-634.
67. Falciatore A, Bowler C (2005) The evolution and function of blue and red light photoreceptors. Curr Top Dev Biol 68: 317-350.
68. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
69. Lassmann T, Sonnhammer EL (2005) Kalign-an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6: 298.
70. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithim to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
71. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
72. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates; Smith WL, Chanley MH, eds, New York: Plenum Press.
73. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta G(T)) method. Methods 25: 402-408.