Production of polyhydroxybutyrate by polycistronic expression of bacterial genes in tobacco plastid

Plant and Cell Physiology

Volumn 45, Issue 9, 2004, Pages 1176-1184

  Arai, Yuko ^a,c   Shikanai, Toshiharu ^b,d   Doi, Yoshiharu ^a   Yoshida, Shigeo ^a   Yamaguchi, Isamu ^a,e   Nakashita, Hideo ^a  

^a RIKEN   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e RIKEN Center for Sustainable Resource Science   (Japan)

Author keywords

Biodegradable polyester; Metabolic engineering; Plastid transformation; Polycistron; Polyhydroxybutyrate

Indexed keywords

BACTERIA (MICROORGANISMS); INSERTION SEQUENCES; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 7944233429     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pch139     Document Type: Article

References (45)

1. Arai, Y., Nakashita, H., Doi, Y. and Yamaguchi, I. (2001) The plastid targeting of polyhydroxybutyrate biosynthetic pathway in tobacco. Plant Biotechnol. 18: 289-293.
2. Arai, Y., Nakashita, H., Suzuki, Y., Kobayash, Y., Shimizu, T., Yasuda, M., Doi, Y. and Yamaguchi, I. (2002) Synthesis of a novel class of polyhydroxyalkanoates in Arabidopsis peroxisomes, and their use in monitoring short-chain-length intermediates of β-oxidation. Plant Cell Physiol. 43: 555-562.
3. Bohmert, K., Balbo, I., Kopka, J., Mittendorf, V., Nawrath, C., Poirier, Y., Tischendorf, G., Trethewey, N. and Willmitzer, L. (2000) Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta 211: 841-845.
4. Cosa, B.D., Moar, W., Lee, S.B., Miller, M. and Daniell, H. (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat. Biotechnol. 19: 71-74.
5. Denis, J.M. (1999) Production of novel oils in plants. Curr. Opin. Biotechnol. 10: 175-180.
6. Dawson, W.O. (1996) Gene silencing and virus resistance: a common mechanism. Trends Plant Sci. 1: 107-108.
7. Doi, Y. (1990) Microbial Polyesters. VCH Publishers, New York.
8. Fukui, T. and Doi, Y. (1997) Cloning and analysis of poly(3- hydroxybutyrate-co-3-hydroxyhexanoate) biosynthesis genes of Aeromonas caviae. J. Bacteriol. 179: 4821-4830.
9. Gallardo, F., Miginiac-Maslow, M., Sangwan, R.S., Decottignies, P., Keryer, E., Dubois, F., Bismuth, E., Galvez, S., Sangwan-Norreel, B., Gadal, P. and Cretin, C. (1995) Monocotyledonous C-4 NADP+-malate dehydrogenase is efficiently synthesized, targeted to chloroplasts and processed to an active form in transgenic plants of the C-3 dicotyledon tobacco. Planta 197: 324-332.
10. Gerngross, T.U. (1999) Can biotechnology move us toward a sustainable society? Nat. Biotechnol. 17: 541-544.
11. Gray, M.W. and Doolittle, W.F. (1982) Has the endo symbiont hypothesis been proven? Microbiol. Rev. 46: 1-42.
12. Hahn, J.J., Eschenlauer, A.C., Narrol, M.H., Somers, D.A. and Srienc F. (1997) Growth kinetics, nutrient uptake, and expression of the Alcaligenes eutrophus poly(beta-hydroxybutyrate) synthesis pathway in transgenic maize cell suspension cultures. Biotechnol. Progress 13: 347-354.
13. Hahn, J.J., Eschenlauer, A.C., Sleytr, U.B., Somers, D.A. and Srienc, F. (1999) Peroxisomes as sites for synthesis of polyhydroxyalkanoates in transgenic plants. Biotechnol. Progress 15: 1053-1057.
14. Houmiel, K.L., Slater, S., Broyles, D., Casagrande, L., Colburn, S., Gonzalez, K., Mitsky, T.A., Reiser, S.E., Shah, D., Taylor, N.B., Tran, M., Valentin, H.E. and Gruys, K. (1999) Poly(β-hydroxybutyrate) production in oilseed leukoplasts of Brassica napus. Planta 209: 547-550.
15. Huisman, G.W., Wonink, E., Medima, R., Kazemier, B., Terpstr, P. and Witholt, B. (1991) Metabolism of poly(3-hydroxyalkanoates) (PHAs) by Pseudomonas oleovorans. Identification and sequences of genes and function of the encoded proteins in the synthesis and degradation of PHA. J. Biol. Chem. 226: 2191-2198.
16. John, M.E. and Keller, G. (1996) Metabolic pathway engineering in cotton: Biosynthesis of polyhydroxybutyrate in fiber cells. Proc. Natl Acad. Sci. USA 93: 12768-12773.
17. Kota, M., Daniell, H., Varma, S., Garczynski, S.F., Gould, F. and Moar, W. (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistance insects. Proc. Natl Acad. Sci. USA 96: 1840-1845.
18. Lilly, J.W., Havey, M.J., Jackson, S.A. and Jiang, J. (2001) Cytogenomic analyses reveal the structural plasticity of the chloroplast genome in higher plants. Plant Cell 13: 245-254.
19. Maliga, P. and Nixon, P.J. (1998) Judging the homoplastomic state of plastid transformants. Trends Plant Sci. 3: 376-377.
20. McBride, K.E., Schaaf, D.J., Daley, M. and Stalker, D.M. (1994) Controlled expression of plastid transgene inplants based on a nuclear DNA-encoded and plastid-targeted T7 RNA polymerase. Proc. Natl Acad. Sci. USA 91: 7301-7305.
21. McFadden, G.I. (1999) Plastids and protein targeting. J. Eukaryot. Microbiol. 46: 339-346.
22. Mittendorf, V., Robertson, E.J., Leech, R.M., Krüger, N., Steinbüchel, A. and Poirier, Y. (1998) Synthesis of medium-chain-length polyhydroxyalkanoates in Arabidopsis thaliana using intermediates of peroxisomal fatty acid β-oxidation. Proc. Natl Acad. Sci. USA 95: 13397-13402.
23. Mittendorf, V., Bongcam, V., Allenbach, L., Clullerez, G., Martini, N. and Poirier, Y. (1999) Polyhydroxyalkanoate synthesis in transgenic plants as a new tool to study carbon flow through β-oxidation. Plant J. 20: 45-55.
24. Mullet, J.E. (1993) Dynamic regulation of chloroplast transcription. Plant Physiol. 103: 309-313.
25. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
26. Nakashita, H., Arai, Y., Yoshioka, K., Fukui, T., Doi, Y., Usami, R., Horikoshi, K. and Yamaguchi, I. (1999) Production of biodegradable polyester by a transgenic tobacco. Biosci. Biotechnol. Biochem. 63: 870-874.
27. Nakashita, H., Arai, Y., Shikanai, T., Doi, Y. and Yamaguchi, I. (2001) Introduction of bacterial metabolism into higher plants by polycistronic transgene expression. Biosci. Biotechnol. Biochem. 65: 1688-1691.
28. Nawrath, C., Poirier, Y., and Somerville, C. (1994) Targeting of the polyhydroxybutyrate biosynthetic pathway to the plastids of Arabidopsis thaliana results in high levels of polymer accumulation. Proc. Natl Acad. Sci. USA 91: 12760-12764.
29. Peoples, O.P. and Sinskey, A.J. (1989a) Poly-beta-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16. Characterization of the genes encoding beta-ketothiolase and acetoacetyl-CoA reductase. J. Biol. Chem. 264: 15293-15297.
30. Peoples, O.P. and Sinskey, A.J. (1989b) Poly-beta-hydroxybutyrate (PHB) biosynthesis in Alcaligenes eutrophus H16. Identification and characterization of the PHB polymerase gene (phbC). J. Biol. Chem. 264: 15298-15303.
31. Poirier, Y. (2001) Production of polyesters in transgenic plants. Adv. Biochem. Eng. Biotechnol. 71: 209-240.
32. Poirier, Y., Dennis, D.E., Klomparens, K. and Somerville, C. (1992) Polyhydroxybutyrate, a biodegradable thermoplastic, produced in transgenic plants. Science 256: 520-523.
33. Possingham, J.V. (1980) Plastid replication and development in the life cycle of higher plants. Annu. Rev. Plant Physiol. 31: 113-130.
34. Reith, M. (1995) Molecular biology of rhodophyte and chromophyte plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 549-575.
35. Ruf, S., Hermann, M., Berger, M.J., Carrer, H. and Bock, R. (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat. Biotechnol. 19: 870-875.
36. Scott, S.E. and Wilkinson, M.J. (1999) Low probability of chloroplast movement from oilseed rape (Brassica napus) into wild Brassica rapa. Nat. Biotechnol. 17: 390-392.
37. Shelton, A.M., Tang, J.D., Roush, R.T., Metz, T.D. and Earle, E.D. (2000) Field tests on managing resistance to Bt-engineered plants. Nat. Biotechnol. 18: 339-342.
38. Shinozaki, K., Ohme M., Tanaka, M., Wakasugi, T., Hayashida, N., Matsubayashi, T., Zaita, N., Chunwongse, J., Obokata, J., Yamaguchi-Shinozaki, K. Ohto, C., Torazawa, K., Meng, B.Y., Sugita, M., Deno, H., Kamogashira, T., Yamada, K., Kusuda, J., Takaiwa, F., Kato, A., Yohdoh, N., Shimada, H. and Sugiura, M. (1986) The complete sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5: 2043-2049.
39. Shikanai, T., Endo, T., Hashimoto, T., Yamada, Y., Asada, K. and Yokota, A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA 95: 9705-9709.
40. Sidorov, V.A., Kasten, D., Pang, S.Z., Hajdukiewicz, P.T.J., Staub, J.M. and Nehra, N.S. (1999) Stable chloroplast transformation in potato: Use of green fluorescent protein as a plastid marker. Plant J. 19: 209-216.
41. Sikdar, S.R., Serino, G., Chaudhuri, S. and Maliga, P. (1998) Plastid transformation of Arabidopsis thaliana. Plant Cell Rep. 18: 20-24.
42. Staub, J.M., Bradley Garcia, B., Graves, J., Hajdukiewicz, P.T.J., Hunter, P., Nehra, N., Paradkar, V., Schlittler, M., Carroll, J.A., Spatola, L., Ward, D., Ye, G. and Russell, D.A. (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat. Biotechnol. 18: 333-338.
43. Svab, Z. and Maliga, P. (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl Acad. Sci. USA 90: 913-917.
44. Voelker, T.A., Worrell, A.C., Anderson, L., Bleibaum, J., Fan, C., Hawkins, D.J., Radke, S.E. and Davies, H.M. (1992) Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. Science 257: 72-74.
45. Ye, G.N., Hajdukiewicz, P.T.J., Broyles, D., Rodriguez, D., Xu, C.W., Nehra, N. and Staub, J.M. (2001) Plastid-expressed 5-enolpyruvylshikimate-3- phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J. 25: 261-270.