Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii

Eukaryotic Cell

Volumn 4, Issue 2, 2005, Pages 253-261

  Borza, Tudor ^a   Popescu, Cristina E ^a   Lee, Robert W ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL PROTEIN; PEPTIDE; PURINE DERIVATIVE; TERPENE; TETRAPYRROLE DERIVATIVE;

ANIMAL; ARTICLE; CHLORELLA; CYTOLOGY; EXPRESSED SEQUENCE TAG; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLASTID; SIGNAL TRANSDUCTION;

ALGAL PROTEINS; ANIMALS; EXPRESSED SEQUENCE TAGS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PEPTIDES; PLASTIDS; PROTOTHECA; PURINES; SIGNAL TRANSDUCTION; TERPENES; TETRAPYRROLES;

ALGAE; APICOMPLEXA; CHLOROPHYTA; EUKARYOTA; HELICOSPORIDIUM; PLASMODIUM FALCIPARUM; PROTOTHECA WICKERHAMII;

EID: 13844322290     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.4.2.253-261.2005     Document Type: Article

References (64)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Archibald, J. M., and P. J. Keeling. 2002. Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet. 18:577-584.
3. Awai, K., E. Marechal, M. A. Block, D. Brun, T. Masuda, H. Shimada, K. Takamiya, H. Ohta, and J. Joyard. 2001. Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98:10960-10965.
4. Bannai, H., Y. Tamada, O. Maruyama, K. Nakai, and S. Miyano. 2002. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298-305.
5. Boucias, D. G., J. J. Becnel, S. E. White, and M. Bott. 2001. In vivo and in vitro development of the protist Helicosporidium sp. J. Eukaryot. Microbiol. 4:460-470.
6. Bruce, B. D. 2001. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim. Biophys. Acta 1541:2-21.
7. Cai, X., A. L. Fuller, L. R. McDougald, and G. Zhu. 2003. Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39-46.
8. Coggins, J. R., C. Abell, L. B. Evans, M. Frederickson, D. A. Robinson, A. W. Roszak, and A. P. Lapthorn. 2003. Experiences with the shikimate-pathway enzymes as targets for rational drug design. Biochem. Soc. Trans. 31:548-552.
9. Cornah, J. E., M. J. Terry, and A. G. Smith. 2003. Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci. 8:224-230.
10. Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16:10881-10890.
11. de Koning, A. P., and P. J. Keeling. 2004. Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga. Eukaryot. Cell 3:1198-1205.
12. el Kouni, M. H. 2003. Potential chemotherapeutic targets in the purine metabolism of parasites. Pharmacol. Ther. 99:283-309.
13. Emanuelsson, O., H. Nielsen, and G. von Heijne. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8:978-984.
14. Emanuelsson, O., H. Nielsen, S. Brunak, and G. von Heijne. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:1005-1016.
15. Fichera, M. E., and D. S. Roos. 1997. A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407-409.
16. Gockel, G., and W. Hachtel. 2000. Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347-351.
17. Goggin, D. E., R. Lipscombe, E. Fedorova, A. H. Millar, A. Mann, C. A. Atkins, and P. M. Smith. 2003. Dual intracellular localization and targeting of aminoimidazole ribonucleotide synthetase in cowpea. Plant Physiol. 131:1033-1041.
18. Gray, J. C. 2003. Chloroplast-to-nucleus signalling: a role for Mg-protoporphyrin. Trends Genet. 19:526-529.
19. Hanessian, S., P. P. Lu, J. Y. Sanceau, P. Chemla, K. Gohda, R. Fonne-Pfister, L. Prade, S. W. Cowan-Jacob. 1999. An enzyme-bound bisubstrate hybrid inhibitor of adenylosuccinate synthetase. Angew. Chem. Int. Ed. Engl. 38:3159-3162.
20. Hollingsworth, S. R. 2000. Canine protothecosis. Vet. Clin. North Am. Small Anim. Pract. 30:1091-1101.
21. Huss, V. A., and M. L. Sogin. 1990. Phylogenetic position of some Chlorella species within the chlorococcales based upon complete small-subunit ribosomal RNA sequences. J. Mol. Evol. 31:432-442.
22. Jacquot, J. P., E. Gelhaye, N. Rouhier, C. Corbier, C. Didierjean, and A. Aubry. 2002. Thioredoxins and related proteins in photosynthetic organisms: molecular basis for thiol dependent regulation. Biochem. Pharmacol. 64:1065-1069.
23. Janosi, S., F. Ratz, G. Szigeti, M. Kulcsar, J. Kerenyi, T. Lauko, F. Katona, and G. Huszenicza. 2001. Review of the microbiological, pathological, and clinical aspects of bovine mastitis caused by the alga Prototheca zopfii. Vet. Q. 23:58-61.
24. Jobling, S. A., G. P. Schwall, R. J. Westcott, C. M. Sidebottom, M. Debet, M. J. Gidley, R. Jeffcoat, and R. Safford. 1999. A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterisation of multiple forms of SBE A. Plant J. 18:163-171.
25. Jomaa, H., J. Wiesner, S. Sanderbrand, B. Altincicek, C. Weidemeyer, M. Hintz, I. Turbachova, M. Eberl, J. Zeidler, H. K. Lichtenthaler, D. Soldati, and E. Beck. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285:1573-1576.
26. Kantrow, S. M., and A. S. Boyd. 2003. Protothecosis. Dermatol. Clin. 21:249-255.
27. Kim, J., and S. P. Mayfield. 2002. The active site of the thioredoxin-like domain of chloroplast protein disulfide isomerase, RB60, catalyzes the redox-regulated binding of chloroplast poly(A)-binding protein, RB47, to the 5′ untranslated region of psbA mRNA. Plant Cell Physiol. 43:1238-1243.
28. Kohler, S., C. F. Delwiche, P. W. Denny, L. G. Tilney, P. Webster, R. J. Wilson, J. D. Palmer, and D. S. Roos. 1997. A plastid of probable green algal origin in Apicomplexan parasites. Science 75:1485-1489.
29. Knauf, U., and W. Hachtel. 2002. The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic alga Prototheca wickerhamii. Mol. Genet. Genomics 267:492-497.
30. Lee, W.-S., M. D Lagios, and R. Leonards. 1975. Wound infection by Prototheca wickerhamii, a saprophytic alga pathogenic for man. J. Clin. Microbiol. 2:62-66.
31. Lemaire, S. D., V. Collin, E. Keryer, A. Quesada, and M. Miginiac-Maslow. 2003. Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett. 543:87-92.
32. MacFadden, G. I., M. Reith, J. Munholland, and N. Lang-Unnasch. 1996. Plastid in human parasites. Nature 381:482.
33. Maul, J. E., J. W. Lilly, L. Cui, C. W. de Pamphilis, W. Miller, E. H. Harris, and D. B. Stern. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659-2679.
34. Miege, C., E. Marechal, M. Shimojima, K. Awai, M. A. Block, H. Ohta, K. Takamiya, R. Douce, and J. Joyard. 1999. Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur. J. Biochem. 265:990-1001.
35. Nadakavukaren, M. J., and D. A. McCracken. 1973. Prototheca: an alga or a fungus? J. Phycol. 9:113-116.
36. Nadakavukaren, M. J., and D. A. McCracken. 1977. An ultrastructural survey of the genus Prototheca with special reference to plastids. Mycopathologia 61:117-119.
37. Neuhaus, H. E., and M. J. Emes. 2000. Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:111-140.
38. Obadou, S., R. Tien, J. Soll, and E. Schleiff. 2003. Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J. Cell Sci. 116:837-846.
39. Ohlrogge, J. B., and J. G. Jaworski. 1997. Regulation of fatty acid synthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:109-136.
40. Qi, Q., K. F. Kleppinger-Sparace, and S. A. Sparace. 1995. The utilization of glycolytic intermediates as precursors for fatty acid biosynthesis by pea root plastids. Plant Physiol. 107:413-419.
41. Ralph, S. A., G. G. van Dooren, R. F. Waller, M. J. Crawford, M. J. Fraunholz, B. J. Foth, C. J. Tonkin, D. S. Roos, and G. I. Mc Fadden. 2004. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2:203-216.
42. Sato, S., and R. J. Wilson. 2002. The genome of Plasmodium falciparum encodes an active delta-aminolevulinic acid dehydratase. Curr. Genet. 40:391-398.
43. Sato, S., B. Clough, L. Coates, and R. J. M. I. Wilson. 2004. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 155:117-125.
44. Schmitzer, P. R., P. R. Graupner, E. L. Chapin, S. C. Fields, J. R. Gilbert, J. A. Gray, C. L. Peacock, and B. C. Gerwick. 2000. Ribofuranosyl triazolone: a natural product herbicide with activity on adenylosuccinate synthetase following phosphorylation J. Nat. Prod. 63:777-781.
45. Sekiguchi, H., M. Moriya, T. Nakayama, I. Inouye. 2002. Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 153:157-167.
46. Shanklin, J., and E. B. Cahoon. 1998. Desaturation and related modifications of fatty acids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:611-641.
47. Siehl, D. L., M. V. Subramanian, E. W. Walters, S. F. Lee, R. J. Anderson, and A. G. Toschi. 1996. Adenylosuccinate synthetase: site of action of hydantocidin, a microbial phytotoxin. Plant Physiol. 110:753-758.
48. Spalton, D. E. 1985. Bovine mastitis caused by Prototheca zopfii: a case study. Vet. Rec. 116:347.
49. Strand, A., T. Asami, J. Alonso, J. R. Ecker, and J. Chory. 2003. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421:79-83.
50. Tartar, A., D. G. Boucias, B. J. Adams, and J. J. Becnel. 2002. Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). Int. J. Syst. Evol. Microbiol. 52:273-279.
51. Tartar, A., and D. G. Boucias. 2004. The non-photosynthetic, pathogenic green alga Helicosporidium sp. has retained a modified, functional plastid genome. FEMS Microbiol. Lett. 233:153-157.
52. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
53. Torres, H. A., G. P. Bodey, J. J. Tarrand, and D. P. Kontoyiannis. 2003. Protothecosis in patients with cancer: case series and literature review. Clin. Microbiol. Infect. 9:786-792.
54. Trebitsh, T., E. Meiri, O. Ostersetzer, Z. Adam, and A. Danon. 2001. The protein disulfide isomerase-like RB60 is partitioned between stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J. Biol. Chem. 276:4564-4569.
55. Ueno, R., N. Urano, and M. Suzuki. 2003. Phylogeny of the non-photosynthetic green micro-algal genus Prototheca (Trebouxiophyceae, Chlorophyta) and related taxa inferred from SSU and LSU ribosomal DNA partial sequence data. FEMS Microbiol. Lett. 223:275-280.
56. Vollmer, M., N. Thomsen, S. Wiek, and F. Seeber. 2001. Apicomplexan parasites possess distinct nuclear-encoded, but apicoplast-localized, plant-type ferredoxin-NADP+ reductase and ferredoxin. J. Biol. Chem. 276:5483-5490.
57. Wakabayashi, K., and P. Boger. 2002. Target sites for herbicides: entering the 21st century. Pest Manag. Sci. 58:1149-1154.
58. Wakasugi, T., T. Nagai, M. Kapoor, M. Sugita, M. Ito, S. Ito, J. Tsudzuki, K. Nakashima, T. Tsudzuki, Y. Suzuki, A. Hamada, T. Ohta, A. Inamura, K. Yoshinaga, and M. Sugiura. 1997. Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc. Natl. Acad. Sci. USA 94:5967-5972.
59. Waller, R. F., P. J. Keeling, R. G. Donald, B. Striepen, E. Handman, N. Lang-Unnasch, A. F. Cowman, G. S. Besra, D. S. Roos, and G. I. McFadden. 1998. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95:12352-12357.
60. Weeden, N. F. 1981. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J. Mol. Evol. 17:133-139.
61. Williams, B. A., and P. J. Keeling. 2003. Cryptic organelles in parasitic protists and fungi. Adv. Parasitol. 54:9-68.
62. Wilson, R. J., P. W. Denny, P. R. Preiser, K. Rangachari, K. Roberts, A. Roy, A. Whyte, M. Strath, D. J. Moore, P. W. Moore, and D. H. Williamson. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261:155-172.
63. Wolfe, K. H., C. W. Morden, and J. D. Palmer. 1992. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. USA 89:10648-10652.
64. Wolfe, A. D., and C. W. dePamphilis. 1998. The effect of relaxed functional constraints on the photosynthetic gene rbcL in photosynthetic and nonphotosynthetic parasitic plants. Mol. Biol. Evol. 15:1243-1258.