A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis

PLoS ONE

Volumn 3, Issue 1, 2008, Pages

  Kroth, Peter G ^a   Chiovitti, Anthony ^b   Gruber, Ansgar ^a   Martin Jezeque, Veronique ^c   Mock, Thomas ^d   Parker, Micaela Schnitzler ^d   Stanley, Michele S ^e   Kaplan, Aaron ^f   Caron, Lise ^c   Weber, Till ^a   Maheswari, Uma ^g,h   Armbrust, E Virginia ^d   Bowler, Chris ^g,h  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITÉ DE NANTES   (France)

^d UNIVERSITY OF WASHINGTON   (United States)

^e SCOTTISH MARINE INSTITUTE   (United Kingdom)

^f HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^g ECOLE NORMALE SUPÉRIEURE   (France)

^h Cell Signalling Laboratory   (France)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; BETA 1,3 GLUCAN; BETA GLUCAN HYDROLASE; CARBOHYDRATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE; CHRYSOLAMINARAN; FRUCTOSE BISPHOSPHATASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCAN SYNTHASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCERATE KINASE; GLYOXYLIC ACID; ISOENZYME; LIPID; MALATE DEHYDROGENASE; PENTOSE PHOSPHATE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOSPHOGLUCOMUTASE; PHOSPHOGLYCERATE KINASE; PHOSPHORIBULOKINASE; PHOSPHOTRANSFERASE; PYRUVATE CARBOXYLASE; PYRUVATE KINASE; PYRUVATE PHOSPHATE DIKINASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOHYDRATE METABOLISM; CARBON METABOLISM; CARBOXY TERMINAL SEQUENCE; COMPARATIVE GENE MAPPING; CONTROLLED STUDY; CYTOSOL; DIATOM; ENZYME DEGRADATION; ENZYME SYNTHESIS; EUKARYOTE; EXPRESSED SEQUENCE TAG; GENE IDENTIFICATION; GENOME; GLYCOLYSIS; MEMBRANE BINDING; MITOCHONDRION; NONHUMAN; PHOTORESPIRATION; PHOTOSYNTHESIS; PLASTID; PREDICTION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CARBOHYDRATE METABOLISM; CARBON DIOXIDE; DIATOMS; GENOME; MODELS, BIOLOGICAL;

ALGAE; BACILLARIOPHYTA; EUKARYOTA; PHAEODACTYLUM TRICORNUTUM; THALASSIOSIRA PSEUDONANA;

EID: 38949120916     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001426     Document Type: Article

References (134)

1. Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281: 200-205.
2. Brzezinski MA, Pride CJ, Franck VM (2002) A switch from Si(OH)4 to NO3-depletion in the glacial Southern Ocean. Geophys. Res Let 29: 5-1 to 5-5.
3. Granum E, Raven JA, Leegood RC (2005) How do marine diatoms fix 10 billion tonnes of anorganic carbon per year. Can J Bot 83: 898-908.
4. 4 Pathways of Photosynthetic Carbon Assimilation in Marine Diatoms Are under Genetic, Not Environmental, Control. Plant Physiol 145: 230-235.
5. 2-concentrating mechanisms in algae. Can J Bot 76: 1052-1071.
6. Riebesell U, Wolf-Gladrow, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361: 249-251.
7. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131.
8. Wilhelm C, Büchel 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.
9. Michels AK, Wedel N, Kroth PG (2005) Diatom Plastids Possess a Phosphoribulokinase with an Altered Regulation and No Oxidative Pentose Phosphate Pathway. Plant Physiol 137: 911-920.
10. 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.
11. Maheswari U, Montsant A, Goll J, Krishnasamy S, Rajyashri KR, et al. (2005) The Diatom EST Database. Nucleic Acids Res 33 Database Issue: D344-D347.
12. 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.
13. Fischer H, Robl I, Sumper M, Kröger N (1999) Targeting and covalent modification of cell wall and membrane proteins heterologously expressed in the diatom Cylindrotheca fusiformis. J Phycol 35: 113-120.
14. Poulsen N, Kröger N (2005) A new molecular tool for transgenic diatoms: control of mRNA and protein biosynthesis by an inducible promoter-terminator cassette. FEBS J 272: 3413-3423.
15. 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.
16. Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41: 175-83.
17. Gruber A, Vugrinec S, Hempel F, Gould SB, Maier U-G, et al. (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol Biol 64: 519-530.
18. Gibbs SP (1981) The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int Rev Cytol 72: 49-99.
19. Behrenfeld MJ, Bale AJ, Kolber ZS, Aiken, J, Falkowski PG (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383: 508-511.
20. Gervais F, Riebesell U, Gorbunov MY (2002) Changes in primary productivity and chlorophyll a in response to iron fertilization in the Southern Polar Frontal Zone. Limnol Oceanogr 47: 1324-1335.
21. Reinfelder JR, Kraepiel AML, Morel FMM (2000) Unicellular C-4 photosynthesis in a marine diatom. Nature 407: 996-999.
22. Reinfelder JR, Milligan AJ, Morel FM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135: 2106-2111.
23. Cabello-Passini A, Swift H, Smith GJ, Alberte RS (2001) Phosphoenolpyruvate carboxykinase from the marine diatom Skeletonema costatum and the phaeophyte Laminaria setchellii. II. Immunological characterization and subcellular localization. Bot Marina 44: 199-207.
24. Wittpoth C, Kroth PG, Weyrauch K, Kowallik KV, Strotmann H (1998) Functional characterization of isolated plastids from two marine diatoms. Planta 206: 79-85.
25. Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single-cell C(4) photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55: 173-196.
26. Long JJ, Wang JL, Berry JO (1994) Cloning and analysis of the C4 photosynthetic NAD-depedent malic enzyme of Amaranth mitochondria. J Biol Chem 269: 2827-2833.
27. Burnell JN, Hatch MD (1988) Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: pathways of C4 acid decarboxylation in bundle sheath cells of Urochloa panicoides. Arch Biochem Biophys 260: 187-199.
28. Kanai R, Edwards GE (1999) The biochemistry of C4 plants. In: Sage RF, Monson RK, eds (1999) C4 plant biology. London, UK: Academic Press. pp 49-87.
29. 2 pump. Photosynth Res 77: 191-207.
30. 2 concentrations. Protist 149: 341-345.
31. 2-concentrating mechanism of photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539-570.
32. Ogawa T, Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynthesis Res 77: 105-115.
33. 2 concentrating mechanism. J Exp Bot 57: 249-65.
34. Drechsler Z, Sharkia R, Cabantchik ZI, Beer S (1993) Bicarbonate uptake in the marine macroalga Ulva sp. is inhibited by classical probes of anion exchange by red blood cells. Planta 191: 34-40.
35. Park H, Song B, Morel FM (2007) Diversity of the cadmium-containing carbonic anhydrase in marine diatoms and natural waters. Environ Microb 9: 403-413.
36. 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.
37. Tanaka Y, Nakatsuma D, Harada H, Ishida M, Matsuda Y (2005) Localization of soluble beta-carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Sorting to the chloroplast and cluster formation on the girdle lamellae. Plant Physiol 138: 207-17.
38. Szabo E, Colman B (2007) Isolation and characterization of carbonic anhydrases from the marine diatom Phaeodactylum tricornutum. Physiol Plantarum 129: 484-492.
39. 2 and light in the marine diatom Phaeodactylum tricornutum. Plant Physiol 139: 1041-1050.
40. Mitra M, Lato SM, Ynalvez RA, Xiao Y, Moroney JV (2004) Identification of a new chloroplast carbonic anhydrase in Chlanydomonas reinhardtii. Plant Physiol 135: 173-182.
41. 2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiol 142: 1318-1328.
42. Harada, H, Matsuda Y (2005) Identification and characterization of a new carbonic anhydrase in the marine diatom Phaeodactylum tricornutum. Can J Bot 83: 909-16.
43. Tortell PD, Reinfelder JR, Morel FM (1997) Active uptake of bicarbonate by diatoms. Nature (London) 390: 243-244.
44. Igamberdiev AU, Bykova NV, Lea PJ, Gardenstrom P (2001) The role of photorespiration in redox and energy balanc of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol Plantarum 111: 427-438.
45. Park YI, Chow WS, Osmond CB, Anderson JM (1996) Electron transport to oxygen mitigates against photoinactivation of Photosystem II in vivo. Photosynthesis Res 50: 23-32.
46. Wu J, Neimanis S, Heber U (1991) Photorespiration is more effective than the Mehler reaction in protecting the photosynthetic apparatus against photoinhibition. Bot Acta 104: 283-291.
47. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Phil Trans R Soc Lond B 355: 1517-1529.
48. Yamaguchi K, Nishimura M (2000) Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant Cell Physiol 41: 1397-1406.
49. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384: 557-560.
50. Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45: 744-750.
51. Paul JS, Volcani BE (1976) Photorespiration in diatoms. 4. 2 pathways of glycolate metabolism in synchronized cultures of Cylindrotheca fusiformis. Arch Microbiol 110: 247-252.
52. Colman B, Rotatore C (1988) Uptake and accumulation of inorganic carbon by a freshwater diatom. J Exp Bot 39: 1025-1032.
53. Beardall J (1989) Photosynthesis and photorespiration in marine phytoplankton. Aquat Bot 34: 105-130.
54. Beardall J, Raven JA (1990) Pathways and mechanism of respiration in microalgae. Mar Microb Food Webs 4: 7-30.
55. 2 cycle. CRC Crit Rev Plant Sci 5: 45-100.
56. Norman EG, Colman B (1991) Purification and characterization of phosphoglycolate phosphatase from the cyanobacterium Coccochloris peniocystis. Plant Physiol 95: 693-698.
57. Tolbert NE (1997) The C-2 oxidative photosynthetic carbon cycle. Ann Rev Plant Physiol Plant Mol Biol 48: 123.
58. Tolbert NE (1980) Photorespiration. In: Stumpf P, Conn E, eds (1980) The Biochemistry of Plants Academic NY. pp 2, 488-525.
59. Merrett MJ, Lord JM (1973) Glycolate formation and metabolism by algae. New Phytol 72: 751-767.
60. Leboulanger C, Martin-Jézéquel V, Descolas-Gros C, Sciandra A, Jupin HJ (1998) Photorespiration in continuous culture of Dunaliella tertiolecta (Chlorophyta): relationships between serine, glycine, and extracellular glycolate. J Phycol 34: 651-654.
61. 2 net exchange ratio during photosynthesis in Chlamydomonas reinhardtii. Plant Physiol 67: 229-232.
62. Fogg GE (1983) The ecological significance of extracellular products of phytoplankton photosynthesis. Botanica Marina 26: 3-14.
63. Parker MS, Armbrust EV, Piovia-Scott J, Keil RG (2004) Induction of photorespiration by light in the centric diatom Thalassiosira weissflogii (Bacillariophyceae): Molecular characterization and physiological consequences. J Phycol 40: 557-567.
64. Leboulanger C, Oriol Jupin H, Descolas-Gros C (1997) Diel variability of glycolate in the eastern tropical Atlantic Ocean. Deep Sea Res 44: 2131-2139.
65. Eisenhut M, Hasse D, Kahlon S, Lieman-Hurwitz J, Ogawa T, et al. (2006) The plant-type C2 glycolate pathway and the bacterial-like glycerate cycle cooperate in the metabolism of phosphoglycolate in cyanobacteria. Plant Physiol 142: 333-342.
66. Parker MS, Armbrust EV (2005) Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 41: 1142-1153.
67. Winkler U, Stabenau H (1995) Isolation and characterization of peroxisomes from diatoms. Planta 195: 403-407.
68. Suzuki K, Iwamoto K, Yokoyama S, Ikawa T (1991) Glycolate-oxidizing enzymes in algae. J Phycol 27: 492-498.
69. Noctor G, Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol 49: 249-279.
70. Raven JA, Beardall J (1981) Respiration and photorespiration. In: Platt, ed (1981) Physiological Bases of Phytoplankton Ecology. Can Bull Fish Aquat Sci 210: 55-82.
71. Martin W, Scheibe R, Schnarrenberger C (2000) The Calvin cycle and its regulation. In: Leegood RC, Sharkey TD, von Caemmerer S, eds (2000) Photosynthesis: Physiology and Metabolism. Dordrecht: Kluwer Academic Publishers. pp 9-51.
72. Sun N, Ma L, Pan D, Zhao H, Deng XW (2003) Evaluation of light regulatory potential of Calvin cycle steps based on large-scale gene expression profiling data. Plant Mol Biol 53: 467-478.
73. Fey V, Wagner R, Bräutigam K, Pfannschmidt T (2005) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56: 1491-1498.
74. Ruelland E, Miginiac MM (1999) Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition? Trends Plant Science 4: 136-141.
75. Jacquot J-P, Lancelin J-M, Meyer Y (1997) Thioredoxins: structure and function in plant cells. New Phytol 136: 543-570.
76. Oudot-Le Secq M-P, Grimwood J, Shapiro H, Armbrust EV, Bowler C, et al. (2007). Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Gen Genomics 277: 427-439.
77. Tamoi M, Ishikawa T, Takeda T, Shigeoka S (1996) Molecular characterization and resistance to hydrogen peroxide of two fructose-1,6-bisphosphatases from Synechococcus PCC 7942. Arch Biochem Biophys 334: 27-36.
78. Kroth PG, Schroers Y, Kilian O (2005) The peculiar distribution of class I and class II aldolases in diatoms and in red algae. Curr Genet 48: 389-400.
79. Michelet L, Zaffagnini M, Marchand C, Collin V, Decottignies P, et al. (2005) Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc Natl Acad Sci USA 102: 16478-16483.
80. Liaud MF, Lichtle C, Apt K, Martin W, Cerff R (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: Evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 17: 213-223.
81. Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56: 1481-1489.
82. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56: 1469-1479.
83. Zhang N, Portis AR (1999) Mechanism of light regulation of Rubisco: A specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96: 9438-9443.
84. Wedel N, Soll J (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/ glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proc Natl Acad Sci USA 93: 9694-9704.
85. Graciet E, Lebreton S, Camadro JM, Gontero B (2002) Thermodynamic analysis of the emergence of new regulatory properties in a phosphoribulokinase-glyceraldehyde 3-phosphate dehydrogenase complex. J Biol Chem 277: 12697-12702.
86. Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDR) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20: 1730-1735.
87. Grauvogel C, Brinkmann H, Petersen J (2007) Evolution of the glucose-6-phosphate isomerase: the plasticity of primary metabolism in photosynthetic eukaryotes. Mol Biol Evol 24: 1611-1621.
88. Huppe HC, Turpin DH (1994) Integration of Carbon and Nitrogen Metabolism in Plant and Algal Cells. Ann Rev Plant Physiol Plant Mol Biol 45: 577-607.
89. Cárdenas ML, Cornish-Brown A, Ureta T (1998) Evolution and regulatory role of the hexokinases. Biochim Biophys Acta 140: 242-264.
90. Handa N (1969) Carbohydrate metabolism in the marine diatom Skeletonema costatum. Mar Biol 4: 208-14.
91. Hama J, Handa N (1992) Diel variation of water-extractable carbohydrate composition of natural phytoplankton populations in Kinu-ura Bay. J Exp Mar Biol Ecol 162: 159-176.
92. Van Oijen T, Van Leuwe MA, Gieskes WWC, De Baar HJW (2004) Effects of iron limitation on photosynthesis and carbohydrate metabolism in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). Eur J Phycol 39: 161-171.
93. Vårum KM, Myklestad S (1984) Effects of light, salinity and nutrient limitation on the production of β-1,3-D-Glucan and Exo-D-Glunanase activity in Skeletonema costatum (Grev) Cleve. J Exp Mar Biol Ecol 83: 13-25.
94. Vårum KM, Øtgaard K, Grimsrud K (1986) Diurnal rhythm in carbohydrate metabolism of the marine diatom Skeletonema costatum (Grev.) Cleve. J Exp Mar Biol Ecol 102: 249-256.
95. Granum E, Kirkvold S, Myklestad SM (2002) Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar Ecol Prog Ser 242: 83-94.
96. Ford CW, Percival E (1965) The carbohydrates of Phaeodactylum tricornutum. Part I. Preliminary examination of the organism, and characterization of low molecular weight material and of a glucan. J Chem Soc. pp 7035-7041.
97. Smestad Paulsen B, Myklestad H (1978) Structural studies of the reserve glucan produced by the marine diatom Skeletonema costatum (Grev.) Cleve. Carbohydr Res 62: 386-388.
98. McConville MJ, Bacic A, Clarke AE (1986) Structural studies of chrysolaminaran from the ice diatom Stauroneis amphioxys (Gregory). Carbohydr Res 153: 330-333.
99. Chiovitti A, Molino P, Crawford SA, Teng R, Spurck T, et al. (2004) The glucans extracted with warm water from diatoms are mainly derived from intracellular chrysolaminaran and not extracellular polysaccharides. Eur J Phycol 39: 117-128.
100. Alexseeva SA, Shevchenko NM, Kusaykin MI, Ponomorenko LP, Isakov VV, et al. (2005) Polysaccharides of diatoms occurring in Lake Baikal. Appl Biochem Microbiol 41: 185-191.
101. Størseth TR, Hansen K, Reitan KI, Skjermo J (2005) Structural characterization of β-D-(1→3)-glucans from different growth phases of the marine diatoms Chaetoceros mülleri and Thalassiosira weissflogii. Carbohydr Res 340: 1159-1164.
102. Størseth TR, Kirkvold S, Skjermo J, Reitan KI (2006) A branched β-D-(1→3,1→6)-glucan from the marine diatom Chaetocero mülleri characterized by NMR. Carbohydr Res 341: 2108-2114.
103. Waterkeyn L, Bienfait A (1987) Localisation et role des β-1,3-glucanes (callose et chrysolaminarine) dans le genre Pinnularia (Diatomées). La Cellule 74: 198-226.
104. Roessler PG (1987) UDP-Glucose Pyrophosphorylase activity in the diatom Cyclotella cryptica. Pathway of Chrysolaminarin synthesis. J Phycol 23: 494-498.
105. Rayner JC, Pelham HR (1997) Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J 16: 1832-1841.
106. Wiese A, Gröner F, Sonnewald U, Deppner H, Lerch J, et al. (1999) Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett 461: 13-18.
107. Weber AP, Schneidereit J. Voll LM (2004) Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. J Exp Bot 55: 1231-1244.
108. Roach PJ (2002) Glycogen and its metabolism. Curr Mol Med 2: 101-120.
109. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54: 207-233.
110. Pilkis SJ, Weber IT, Harrison RW, Bell GT (1994) Glucokinase: structural analysis of a protein involved in susceptibility to diabetes. J Biological Chem 269: 21925-21928.
111. Sugiyama J, Boisset C. Hashimoto M, Watanabe T (1999) Molecular directionality of β-chitin biosynthesis. J Mol Biol 286: 247-255.
112. Tsekos I (1999) The sites of cellulose synthesis in algae: diversity and evolution of cellulose-synthesizing enzyme complexes. J Phycol 35: 635-655.
113. Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. In: Jeon KW, ed (2000) International Review of Cytology. a Survey of Cell Biology, Volume 199. San Diego, USA: Academic Press. pp 161-199.
114. Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 317-343.
115. Montijn RC, Vink E, Müller WH, Verkleij AJ, van den Ende H, et al. (1999) Localizzation of synthesis b1,6-glucan in Saccharomyces cervisiae. J Bacteriology 181: 7411-7420.
116. Drew ED (1984) Physiology and metabolism of cyclitols. In: Lewis DH, ed (1984) Storage Carbohydrates in Vascular Plants. Cambridge: Cambridge Unversity Press. pp 133-155.
117. Loewus FA, Loewus MW (1983) Myo-inositol: its biosynthesis and metabolism. Annual Review of Plant Physiology 34: 137-161.
118. Stein R, Schnarre-berger C, Gross W (1997) Myo-Inositol dehydrogenase from acido- and thermophilic-red alga Galdieria sulphuraria. Phytochemistry 46: 17-20.
119. Gross W, Meyer A (2003) Distribution of myo-inositol debydrogenase in algae. Eur J Phycol 38: 191-194.
120. + oxidoreductase in mammalian brain. Biochim Biophys Res Commun 68: 1133-1138.
121. Yoshida KI, Aoyama D, Isho I, Shibayama T, Fujita Y (1997) Organization and transcription of the myo-inositol operon, iol, of Bacillus subtilis. J Bacteriol 179: 4591-4598.
122. Lavaud J (2007) Fast Regulation of Photosynthesis in Diatoms: Mechanisms, Evolution and Ecophysiology. Funct Plant Sci Biotechnol J: 267-287.
123. Merchant SS, Prochnik SE, Vallon O, Harris E, Karpowicz SJ, et al. (2007) The Chlamydomonas genome, reveals the evolution of key animal and plant functions. Science 318: 245-251.
124. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database, search programs. Nucleic Acids Res 25: 3389-3402.
125. Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, et al. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653-657.
126. Weber APM, Oesterhelt C, Gross W, Brautigam A, Imboden LA, et al. (2004) EST-analysis of the thermo-acidophilic red alga Galdieria sulphararia reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55: 17-32.
127. Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, et al. (2005) Comparative Genomics of Two Closely Related Unicellular Thermo-Acidophilic Red Algae, Galdieria sulphurariaand Cyanidioschyzon merolae, Reveals the Molecular Basis of the Metabolic Flexibility of Galdieria sulphuraria and Significant Differences in Carbohydrate Metabolism of Both Algae. Plant Physiol 137: 460-474.
128. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-95.
129. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) A neural network method for identification of prokaryotic: and eukaryotic signal peptides and prediction ot their cleavage sites. Int J Neural Syst 8: 581-99.
130. Nielsen H, Krogh A (1998) Prediction of signal peptides and signal anchors by a hidden Markay model. Proc Int Conf Intell Syst Mol Biol: 122-30.
131. Emanuelsson O, Nilsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-84.
132. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, et al. (2005) CDD: a Conserved Domain Database for protein classification. Nucl Acids Res 33: D192-196.
133. Emanuelsson O, Brunak, S, von Heijne G (2000) Predicting subcellular, localization of proteins based on their N-terminal amino acid sequence. Mol Biol 300: 1005-1016.
134. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2: 953-971.