Genomic and biochemical analysis of lipid biosynthesis in the unicellular rhodophyte Cyanidioschyzon merolae: Lack of a plastidic desaturation pathway results in the coupled pathway of galactolipid synthesis

Eukaryotic Cell

Volumn 6, Issue 6, 2007, Pages 1006-1017

  Sato, Naoki ^a   Moriyama, Takashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; ALGAL PROTEIN; FATTY ACID; GALACTOLIPID; HYBRID PROTEIN; LIPID;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; CYTOLOGY; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLASTID; RED ALGA; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

ALGAE, RED; ALGAL PROTEINS; AMINO ACID SEQUENCE; FATTY ACID DESATURASES; FATTY ACIDS; GALACTOLIPIDS; INTRACELLULAR MEMBRANES; LIPIDS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASTIDS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

ALGAE; CHLOROPHYTA; CYANIDIOSCHYZON MEROLAE; CYANOBACTERIA; EUKARYOTA; PROKARYOTA; RHODOPHYTA;

EID: 34250834380     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00393-06     Document Type: Article

References (56)

1. Adachi, J., and M. Hasegawa. 1992. Amino acid substitution of proteins coded for in mitochondrial DNA during mammalian evolution. Jpn. J. Genet. 67:187-197.
2. Allen, M. B. 1959. Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch. Microbiol. 32:270-277.
3. Altschul, S. F., T. L. Madden, A. A. Schäfer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Araki, S., T. Sakurai, T. Omata, A. Kawaguchi, and N. Murata. 1986. Lipid and fatty acid composition in the red alga Porphyra yezoensis. Jpn. J. Phycol. 34:94-100.
5. Armbrust, E. V., J. A. Berges, C. Bowler, B. R. Green, D. Martinez, N. H. Putnam, S. Zhou, A. E. Allen, K. E. Apt, M. Bechner, M. A. Brzezinski, B. K. Chaal, A. Chiovitti, A. K. Davis, M. S. Demarest, J. C. Detter, T. Glavina, D. Goodstein, M. Z. Hadi, U. Hellsten, M. Hildebrand, B. D. Jenkins, J. Jurka, V. V. Kapitonov, N. Kroger, W. W. Lau, T. W. Lane, F. W. Larimer, J. C. Lippmeier, S. Lucas, M. Medina, A. Montsant, M. Obornik, M. S. Parker, B. Palenik, G. J. Pazour, P. M. Richardson, T. A. Rynearson, M. A. Saito, D. C. Schwartz, K. Thamatrakoln, K. Valentin, A. Vardi, F. P. Wilkerson, and D. S. Rokhsar. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79-86.
6. Awai, K., T. Kakimoto, C. Awai, T. Kaneko, Y. Nakamura, K. Takamiya, H. Wada, and H. Ohta. 2006. Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria. Plant Physiol. 141:1120-1127.
7. Beisson, F., A. J. K. Koo, S. Ruuska, J. Schwender, M. Pollard, J. J. Thelen, T. Paddock, J. J. Salas, L. Savage, A. Milcamps, V. B. Mhaske, Y. Cho, and J. B. Ohlrogge. 2003. Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol. 132:681-697.
8. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
9. Botte, C., C. Jeanneau, L. Snajdrova, O. Bastien, A. Imberty, C. Breton, and E. Maréchal. 2005. Molecular modeling and site-directed mutagenesis of plant chloroplast monogalactosyldiacylglycerol synthase reveal critical residues for activity. J. Biol. Chem. 280:34691-34701.
10. Browse, J., and C. Somerville. 1991. Glycerolipid synthesis: biochemistry and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:467-506.
11. Cavalier-Smith, T. 2003. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos. Trans. R. Soc. Lond. B 358:109-134.
12. Chenna, R., H. Sugawara, T. Koik, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
13. Chiu, W.-I., Y. Niwa, W. Zeng, T. Hirose, H. Kobayashi, and J. Sheen. 1996. Engineered GFP as vital reporter in plants. Curr. Biol. 6:325-330.
14. Domergue, F., P. Spiekermann, J. Lerchl, C. Beckmann, O. Kilian, P. G. Kroth, W. Boland, U. Zähringer, and E. Heinz. 2003. New insight into Phaeodactylum tricornutum fatty acid metabolism. Cloning and functional characterization of plastidial and microsomal delta12-fatty acid desaturases. Plant Physiol. 131:1648-1660.
15. Erwin, J. A. 1973. Comparative biochemistry of fatty acids in eukaryotic microorganisms, p. 41-143. In J. A. Erwin (ed.), Lipids and biomembranes of eukaryotic microorganisms. Academic Press, New York, NY.
16. Fischer, W., E. Heinz, and M. Zeus. 1973. The suitability of lipase from Rhizopus arrhizus delemar for analysis of fatty acid distribution in dihexosyl diglycerides, phospholipids and plant sulfolipids. Hoppe-Seyler's Z. Physiol. Chem. 354:1115-1123.
17. Harwood, J. L., and A. L. Jones. 1989. Lipid metabolism in algae. Adv. Bot. Res. 16:1-53.
18. Heemskerk, J. W. M., H. Schmidt, U. Hammer, and E. Heinz. 1991. Biosynthesis and desaturation of prokaryotic galactolipids in leaves and isolated chloroplasts from spinach. Plant Physiol. 96:144-152.
19. Heilmann, I., S. Mekhedov, B. King, J. Browse, and J. Shanklin. 2004. Identification of the Arabidopsis palmitoyl-monogalactosyldiacylglycerol 87-desaturase gene FAD5, and effects of plastidial retargeting of Arabidopsis desaturases on the fad5 mutant phenotype. Plant Physiol. 136:4237-4245.
20. Itoh, R., K. Toda, H. Takahashi, H. Takano, and T. Kuroiwa. 1998. Delta-9 fatty acid desaturase gene containing a carboxyl-terminal cytochrome b5 domain from the red alga Cyanidioschyzon merolae. Curr. Genet. 33:165-170.
21. Katayama, K., I. Sakurai, and H. Wada. 2004. Identification of an Arabidopsis thaliana gene for cardiolipin synthase located in mitochondria. FEBS Lett. 577:193-198.
22. Kenyon, C. N., R. Rippka, and R. Y. Stanier. 1972. Fatty acid composition and physiological properties of some filamentous blue-green algae. Arch. Mikrobiol. 83:216-236.
23. Kleinschmidt, M. G., and V. A. McMahon. 1970. Effect of growth temperature on the lipid composition of Cyanidium caldarium. II. Glycolipid and phospholipid components. Plant Physiol. 46:290-293.
24. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
25. Kuroiwa, T. 1998. The primitive red algae Cyanidium caldarium and Cyanidioschyzon merolae as model system for investigating the dividing apparatus of mitochondria and plastids. BioEssays 20:344-354.
26. Marquardt, T. C., and R. F. Wilson. 1998. An improved reversed-phase thin-layer chromatography method for separation of fatty acid methyl esters. J. Am. Oil Chem. Soc. 75:1889-1892.
27. Martin, W., T. Rujan, E. Richly, A. Hansen, S. Cornelsen, T. Lins, D. Leister, B. Stoebe, M. Hasegawa, and D. Penny. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phytogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99:12246-12251.
28. Matsuzaki, M., O. Misumi, T. Shin-i, S. Maruyama, M. Takahara, S. Miyagishima, T. Mori, K. Nishida, F. Yagisawa, K. Nishida, Y. Yoshida, Y. Nishimura, S. Nakao, T. Kobayashi, Y. Momoyama, T. Higashiyama, A. Minoda, M. Sano, H. Nomoto, K. Oishi, H. Hayashi, F. Ohta, S. Nishizaka, S. Haga, S. Miura, T. Morishita, Y. Kabeya, K. Terasawa, Y. Suzuki, Y. Ishii, S. Asakawa, H. Takano, N. Ohta, H. Kuroiwa, K. Tanaka, N. Shimizu, S. Sugano, N. Sato, H. Nozaki, N. Ogasawara, Y. Kohara, and T. Kuroiwa. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653-657.
29. Mitchell, A. G., and C. E. Martin. 1995. A novel cytochrome b5-like domain is linked to the carboxyl terminus of the Saccharomyces cerevisiae Δ9 fatty acid desaturase. J. Biol. Chem. 270:29766- 29772.
30. Moreira, D., H. Le Guyader, and H. Philippe. 2000. The origin of red algae and the evolution of chloroplasts. Nature 405:69-72.
31. Moretti, A., and R. Nazzaro. 1980. Fatty acids in thermoacidophilic algae. Delpinoa 21:3-11.
32. Murakami, Y., M. Tsuyama, Y. Kobayashi, H. Kodama, and K. Iba. 2000. Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476-479.
33. Napier, J. A., O. Sayanova, P. Sperling, and E. Heinz. 1999. A growing family of cytochrome b5-domain fusion proteins. Trends Plant Sci. 4:2-4.
34. Nozaki, H., M. Matsuzaki, M. Takahara, O. Misumi, H. Kuroiwa, M. Hasegawa, T. Shin-i, Y. Kohara, N. Ogasawara, and T. Kuroiwa. 2003. PhyLogeny of plastids based on cladistic analysis of gene loss inferred from complete plastid genome sequences. J. Mol. Evol. 56:485-497.
35. Nyberg, H., and K. Koskimies-Soininen. 1984. The glycolipid fatty acids of Porphyridium purpureum cultured in the presence of detergents. Phytochemistry 23:751-757.
36. Riekhof, W. R., B. B. Sears, and C. Benning. 2005. Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot. Cell 4:242-252.
37. Routaboul, J.-M., S. F. Fischer, and J. Browse. 2000. Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol. 124:1697-1705.
38. Sato, N. 1991. Lipids in Cryptomonas CR-1. I. Occurrence of betaine lipids. Plant Cell Physiol. 32:819-825.
39. Sato, N. 1991. Lipids in Cryptomonas CR-1. II. Biosynthesis of betaine lipids and galactolipids. Plant Cell Physiol. 32:845-851.
40. Sato, N. 2000. SISEQ: manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16:180-181.
41. Sato, N. 2001. Was the evolution of plastid genetic machinery discontinuous? Trends Plant Sci. 6:151-156.
42. Sato, N. 2006. Origin and evolution of plastids: genomic view on the unification and diversity of plastids, p. 75-102. In R. R. Wise and J. K. Hoober (ed.), The structure and function of plastids. Springer, Berlin, Germany.
43. Sato, N. 2006. Gclust server: phylogenetic profiling with pre-defined organism sets. Genome Inform. 17:P156.
44. Sato, N., and M. Furuya. 1984. The composition of lipids and fatty acids determined at various stages of haploid and diploid generations in the fern Adiantum capillus-veneris. Physiol. Plant 62:139-147.
45. Sato, N., M. Ishikawa, M. Fujiwara, and K. Sonoike. 2005. Mass identification of chloroplast proteins of endosymbiont origin by phylogenetic profiling based on organism-optimized homologous protein groups. Genome Inform. 16:56-68.
46. Sato, N., and N. Murata. 1980. Temperature shift-induced responses in lipids in the blue-green alga, Anabaena variabilis. The central role of diacylmonogalactosylglycerol in thermo-adaptation. Biochim. Biophys. Acta 619:353-366.
47. Sato, N., and N. Murata. 1982. Lipid biosynthesis in the blue-green alga, Anabaena variabilis. II. Fatty acids and lipid molecular species. Biochim. Biophys. Acta 710:279-289.
48. Sato, N., and N. Murata. 1988. Membrane lipids. Methods Enzymol. 167: 251-259.
49. Sato, N., N. Murata, Y. Miura, and N. Ueta. 1979. Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Anacystis nidulans. Biochim. Biophys. Acta 572:19-28.
50. Sato, N., Y. Nemoto, and M. Furuya. 1988. Lipids of Chattonella antiqua (Raphidophyceae). Plant Physiol. Biochem. 26:93-98.
51. Sato, N., K. Sekine, Y. Kabeya, S. Ehira, M. Onuma, and N. Ohta. 2004. Discontinuous evolution of plastid genomic machinery: radical replacement of major DNA-binding proteins. Endocytobiosis Cell Res. 15:286-293.
52. Sato, N., K. Terasawa, K. Miyajima, and Y. Kabeya. 2003. Organization, developmental dynamics and evolution of the plastid nucleoid. Int. Rev. Cytol. 232:217-262.
53. Shanklin, J., and E. B. Cahoon. 1998. Desaturation and related modification of fatty acids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:611-641.
54. Sperling, P., P. Ternes, T. K. Zank, and E. Heinz. 2003. The evolution of desaturases. Prostaglandins Leukot. Essent. Fatty Acids 68:73-95.
55. Toda, K., H. Takano, S. Miyagishima, H. Kuroiwa, and T. Kuroiwa. 1998. Characterization of a chloroplast isoform of serine acetyltransferase from the thermo-acidiphilic red alga Cyanidioschyzon merolae. Biochim. Biophys. Acta 1403:72-84.
56. Yoon, H. S., J. D. Hackett, G. Pinto, and D. Bhattacharya. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99:15507-15512.