Tuber-specific cphA expression to enhance cyanophycin production in potatoes

Plant Biotechnology Journal

Volumn 7, Issue 9, 2009, Pages 883-898

  Hühns, Maja ^a   Neumann, Katrin ^a,i   Hausmann, Tina ^a   Klemke, Friederike ^b   Lockau, Wolfgang ^b   Kahmann, Uwe ^c,d   Kopertekh, Lilya ^e   Staiger, Dorothee ^c   Pistorius, Elfriede K ^c   Reuther, Jens ^f   Waldvogel, Eva ^f   Wohlleben, Wolfgang ^f   Effmert, Martin ^g   Junghans, Holger ^g   Neubauer, Katja ^a   Kragl, Udo ^a   Schmidt, Kerstin ^h   Schmidtke, Jörg ^h   Broer, Inge ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d Zentrum für Ultrastrukturelle Diagnostik im IIT   (Germany)

^e INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^f UNIVERSITY OF TÜBINGEN   (Germany)

^g NORIKA GmbH   (Germany)

^h BIOMATH GMBH   (Germany)

ⁱ Life Print GmbH DNA Analysis   (Germany)

Author keywords

Biodegradable polymer; Cyanophycin; Plastid; Polyaspartate; Solanum tuberosum; Tuber specific

Indexed keywords

BACTERIAL PROTEIN; CYANOPHYCIN; CYANOPHYCIN SYNTHASE, BACTERIA; PEPTIDE SYNTHASE; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; CYTOSOL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT TUBER; PLASTID; POTATO; PROMOTER REGION; TRANSGENIC PLANT;

BACTERIAL PROTEINS; CYTOSOL; GENE EXPRESSION REGULATION, PLANT; PEPTIDE SYNTHASES; PLANT PROTEINS; PLANT TUBERS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROMOTER REGIONS, GENETIC; SOLANUM TUBEROSUM;

SOLANUM TUBEROSUM; THERMOSYNECHOCOCCUS ELONGATUS BP-1; TUBER (TRUFFLE);

EID: 70449344259     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2009.00451.x     Document Type: Article

References (71)

1. Allen, M.M. (1984) Cyanobacterial cell inclusions. Annu. Rev. Microbiol. 38, 1 25.
2. Amber, I.J., Hibbs, J.B., Taintor, R.R. Vavrin, Z. (1988) The L-arginine dependent effector mechanism is induced in murine adenocarcinoma cells by culture supernatant from cyto-toxic activated macrophages. J. Leukoc. Biol. 43, 187 192.
3. Arai, T. Kino, K. (2008) A cyanophycin synthetase from Thermosynechococcus elongatus BP-1 catalyzes primer-independent cyanophycin synthesis. Appl. Microbiol. Biotechnol. 81, 69 78.
4. Berg, H., Ziegler, K., Piotukh, K., Baier, K., Lockau, W. Volkmer-Engert, R. (2000) Biosynthesis of the cyanobacterial reserve polymer multi-L-arginyl-poly-L-aspartic acid (cyanophycin) - mechanism of the cyanophycin synthetase reaction studied with synthetic primers. Eur. J. Biochem. 267, 5561 5570.
5. Bevan, M., Barker, R., Goldsbrough, A., Jarvis, M., Kavanagh, T. Iturriaga, G. (1986) The structure and transcription start site of a major potato-tuber protein gene. Nucleic Acids Res. 14, 4625 4638.
6. Bohmert, K., Balbo, I., Kopka, J., Mittendorf, V., Nawrath, C., Poirier, Y., Tischendorf, G., Trethewey, R.N. Willmitzer, L. (2000) Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta, 211, 841 845.
7. Bohmert, K., Balbo, I., Steinbuchel, A., Tischendorf, G. Willmitzer, L. (2002) Constitutive expression of the beta-ketothiolase gene in transgenic plants. A major obstacle for obtaining polyhydroxybutyrate-producing plants. Plant Physiol. 128, 1282 1290.
8. Börnke, F., Hajirezaei, M. Sonnewald, U. (2002) Potato tubers as bioreactors for palatinose production. J. Biotechnol. 96, 119 124.
9. Caso, G., McNurlan, M.A., McMillan, N.D., Eremin, O. Garlick, P.J. (2004) Tumour cell growth in culture: dependence on arginine. Clin. Sci. 107, 371 379.
10. Castanon, S., Martin-Alonso, J.M., Marin, M.S., Boga, J.A., Alonso, P., Parra, F. Ordas, R.J. (2002) The effect of the promoter on expression of VP60 gene from rabbit hemorrhagic disease virus in potato plants. Plant Sci. 162, 87 95.
11. Cen, Y., Luo, X. Liu, X. (1999) Effect of arginine on deep partial thickness burn in rats. Hua Xi Yi Ke Da Xue Xue Bao, 30, 198 201. Ref Type: Generic
12. Chang, C.J. Swift, G. (1999) Poly(aspartic acid) hydrogel. J. Macromol. Sci. Pure Appl. Chem. 36, 963 970.
13. Diniz, S.C., Voss, I. Steinbuchel, A. (2006) Optimization of cyanophycin production in recombinant strains of Pseudomonas putida and Ralstonia eutropha employing elementary mode analysis and statistical experimental design. Biotechnol. Bioeng. 93, 698 717.
14. Düring, K., Porsch, P., Fladung, M. Lörz, H. (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia-Carotovora. Plant J. 3, 587 598.
15. Elbahloul, Y., Krehenbrink, M., Reichelt, R. Steinbuchel, A. (2005) Physiological conditions conducive to high cyanophycin content in biomass of Acinetobacter calcoaceticus strain ADP1. Appl. Environ. Microbiol. 71, 858 866.
16. Farran, I., Sanchez-Serrano, J.J., Medina, J.F., Prieto, J. Mingo-Castel, A.M. (2002) Targeted expression of human serum albumin to potato tubers. Transgenic Res. 11, 337 346.
17. Fiedler, H.P. Plaga, A. (1987) Separation of amino acids and antibiotics by narrow-bore and normal-bore high-performance liquid-chromatography with precolumn derivatization. J. Chromatogr. 386, 229 241.
18. Flynn, N.E., Meininger, C.J., Haynes, T.E. Wu, G. (2002) Dossier: free amino acids in human health and pathologies - the metabolic basis of arginine nutrition and pharmacotherapy. Biomed. Pharmacother. 56, 427 438.
19. Gau, A.E., Thole, H.H., Sokolenko, A., Altschmied, L., Herrmann, R.G. Pistorius, E.K. (1998) PsbY, a novel manganese-binding, low-molecular-mass protein associated with photosystem II. Mol. Gen. Genet. 260, 56 68.
20. Goo, Y.M., Chun, H.J., Kim, T.W., Lee, C.H., Ahn, M.J., Bae, S.C., Cho, K.J., Chun, J.A., Chung, C.H. Lee, S.W. (2008) Expressional characterization of dehydroascorbate reductase cDNA in transgenic potato plants. J. Plant Biol. 51, 35 41.
21. Herrera-Estrella, L., Deblock, M., Messens, E., Hernalsteens, J.P., Vanmontagu, M. Schell, J. (1983) Chimeric genes as dominant selectable markers in plant-cells. EMBO J. 2, 987 995.
22. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J. Schilperoort, R.A. (1983) A binary plant vector strategy based on separation of vir-region and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature, 303, 179 180.
23. 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. Gruys, K.J. (1999) Poly(beta-hydroxybutyrate) production in oilseed leukoplasts of Brassica napus. Planta, 209, 547 550.
24. Hühns, M., Neumann, K., Hausmann, T., Ziegler, K., Klemke, F., Kahmann, U., Staiger, D., Lockau, W., Pistorius, E.K. Broer, I. (2008) Plastid targeting strategies for cyanophycin synthetase to achieve high-level polymer accumulation in Nicotiana tabacum. Plant Biotechnol. J. 6, 321 336.
25. Joentgen, W., Groth, T.S.A., Hai, T. Oppermann, F.B. (2001) Polyasparaginic acid homopolymers and copolymers, biotechnical production and use thereof. US Patent 61807572.
26. de Jonge, W.J., Kwikkers, K.L., te Velde, A.A., van Deventer, S.J.H., Nolte, M.A., Mebius, R.E., Ruijter, J.M., Lamers, M.C. Lamers, W.H. (2002) Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice. J. Clin. Invest. 110, 1539 1548.
27. Kjeldahl, J. (1883) Neue methode zur bestimmung des stickstoffs in organischen Körpern. Z. Anal. Chem. 22, 366 382.
28. Krehenbrink, M., Oppermann-Sanio, F.B. Steinbuchel, A. (2002) Evaluation of non-cyanobacterial genome sequences for occurrence of genes encoding proteins homologous to cyanophycin synthetase and cloning of an active cyanophycin synthetase from Acinetobacter sp strain DSM 587. Arch. Microbiol. 177, 371 380.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227 : 680 685.
30. Lenis, N.P., van Diepen, H.T.M., Bikker, P., Jongbloed, A.G. van der Meulen, J. (1999) Effect of the ratio between essential and nonessential amino acids in the diet on utilization of nitrogen and amino acids by growing pigs. J. Anim. Sci. 77, 1777 1787.
31. Li, P., Yin, Y.L., Li, D., Kim, S.W. Wu, G.Y. (2007) Amino acids and immune function. Br. J. Nutr. 98, 237 252.
32. Lössl, A., Eibl, C., Harloff, H.J., Jung, C. Koop, H.U. (2003) Polyester synthesis in transplastomic tobacco (Nicotiana tabacum L.): significant contents of polyhydroxybutyrate are associated with growth reduction. Plant Cell Rep. 21, 891 899.
33. Lunden, A.P. (1956) cited by: Adler, G. (1971 Kartoffeln und Kartoffelerzeugnisse. Paul Parey 1971.
34. Maheswaran, M., Ziegler, K., Lockau, W., Hagemann, M. Forchhammer, K. (2006) P-II-regulated arginine synthesis controls accumulation of cyanophycin in Synechocystis sp strain PCC 6803. J. Bacteriol. 188, 2730 2734.
35. Menzel, G., Harloff, H.J. Jung, C. (2003) Expression of bacterial poly (3-hydroxybutyrate) synthesis genes in hairy roots of sugar beet (Beta vulgaris L.). Appl. Microbiol. Biotechnol. 60, 571 576.
36. Murashige, T. Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473 497.
37. Nawrath, C., Poirier, Y. 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.
38. Neumann, K., Stephan, D.P., Ziegler, K., Hühns, M., Broer, I., Lockau, W. Pistorius, E.K. (2005) Production of cyanophycin, a suitable source for the biodegradable polymer polyaspartate, in transgenic plants. Plant Biotechnol. J. 3, 249 258.
39. Nguyen, T.T., Nugent, G., Cardi, T. Dix, P.J. (2005) Generation of homoplasmic plastid transformants of a commercial cultivar of potato (Solanum tuberosum L.). Plant Sci. 168, 1495 1500.
40. Nieves Jr., C. Langkamp-Henken, B. (2002) Arginine and immunity: a unique perspective. Biomed. Pharmacother. 56, 471 482.
41. Oppermann-Sanio, F.B. Steinbuchel, A. (2002) Occurrence, functions and biosynthesis of polyamides in microorganisms and biotechnological production. Naturwissenschaften, 89, 11 22.
42. Oppermann-Sanio, F.B., Hai, T., Aboulmagd, E., Hezayen, F.F., Jossek, S. Steinbüchel, A. (1999) Biochemistry of polyamide metabolism. Biochemical Principles and Mechanisms of Biosynthesis and Biodegradation of Polymers: Proceedings of the International Symposium (Steinbüchel, A., ed.) 185 193.
43. Peoples, O.P. Sinskey, A.J. (1989a) Poly-beta-hydroxybutyrate (Phb) biosynthesis in Alcaligenes eutrophus H16 - identification and characterization of the Phb polymerase gene (Phbc). J. Biol. Chem. 264, 15298 15303.
44. Peoples, O.P. Sinskey, A.J. (1989b) 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.
45. Petrasovits, L.A., Purnell, M.P., Nielsen, L.K. Brumbley, S.M. (2007) Production of polyhydroxybutyrate in sugarcane. Plant Biotechnol. J. 5, 162 172.
46. Poirier, Y. Güys, K.J. (2001) Production of PHAs in transgenic plants. In Biopolymers (Doi, Y. Steinbüchel, A., eds.) Weinheim : Wiley-VCH, 401 435.
47. Poirier, Y., Dennis, D.E., Klomparens, K. Somerville, C. (1992) Polyhydroxybutyrate, a biodegradable thermoplastic, produced in transgenic plants. Science, 256, 520 523.
48. Popovic, P.J., Zeh, H.J. Ochoa, J.B. (2007) Arginine and immunity. J. Nutr. 137, 1681S 1686S.
49. Purnell, M.P., Petrasovits, L.A., Nielsen, L.K. Brumbley, S.M. (2007) Spatio-temporal characterization of polyhydroxybutyrate accumulation in sugarcane. Plant Biotechnol. J. 5, 173 184.
50. Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J. Willmitzer, L. (1989) Both developmental and metabolic signals activate the promoter of a class-I patatin gene. EMBO J. 8, 23 29.
51. Roth, F.X., Fickler, J. Kirchgessner, M. (1995) Effect of dietary arginine and glutamic-acid supply on the N-balance of piglets. 5. Communication on the importance of nonessential amino-acids for protein retention. J. Anm. Physiol. Nutr. 73, 202 212.
52. Saruul, P., Srienc, F., Somers, D.A. Samac, D.A. (2002) Production of a biodegradable plastic polymer, poly-beta-hydroxybutyrate, in transgenic alfalfa. Crop Sci. 42, 919 927.
53. Schwamborn, M. (1996) Polyasparaginsäuren. Nachr. Chem. Techn. Lab. 44, 1167 1179.
54. Schwamborn, M. (1998) Chemical synthesis of polyaspartates: a biodegradable alternative to currently used polycarboxylate homo- and copolymers. Polym. Degrad. Stab. 59, 39 45. (Pubitemid 128389689)
55. Sidorov, V.A., Kasten, D., Pang, S.Z., Hajdukiewicz, P.T.J., Staub, J.M. Nehra, N.S. (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J. 19, 209 216.
56. Simon, R.D. (1971) Cyanophycin granules from blue-green alga Anabaena cylindrica - reserve material consisting of copolymers of aspartic acid and arginine. Proc. Natl Acad. Sci. USA, 68 : 265 &.
57. Simon, R.D. (1976) Biosynthesis of multi-L-arginyl-poly(L-aspartic acid) in filamentous cyanobacterium Anabaena cylindrica. Biochim. Biophys. Acta, 422, 407 418.
58. Simon, R.D. (1987) Inclusion bodies in the cyanobacteria: cyanophycin, polyphosphate, polyhedral bodies. The Cyanobacteria (Fag, P. van Baalen, C., eds.) Elsevier, Amsterdam, the Netherlands 199 225.
59. Simon, R.D. Weathers, P. (1976) Determination of structure of novel polypeptide containing aspartic acid and arginine which is found in cyanobacteria. Biochim. Biophys. Acta, 420, 165 176.
60. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. Klenk, D.C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76 85.
61. SPSS (1999) SPSS (R) Base 10.0 Benutzerhandbuch. SPSS GmbH Software.
62. Tabata, K., Abe, H. Doi, Y. (2000) Microbial degradation of poly(aspartic acid) by two isolated strains of Pedobacter sp. and Sphingomonas sp. Biomacromolecules, 1, 157 161.
63. Taheri, F., Ochoa, J.B., Faghiri, Z., Culotta, K., Park, H.J., Lan, M.S., Zea, A.H. Ochoa, A.C. (2001) L-arginine regulates the expression of the T-cell receptor zeta chain (CD3 zeta) in Jurkat cells. Clin. Cancer Res. 7, 958S 965S.
64. Tapiero, H., Mathe, G., Couvreur, P. Tew, K.D. (2002) I. Arginine. Biomed. Pharmacother. 56, 439 445.
65. Wegener, C., Bartling, S., Olsen, O., Weber, J. von Wettstein, D. (1996) Pectate lyase in transgenic potatoes confers preactivation of defence against Erwinia carotovora. Physiol. Mol. Plant Pathol. 49, 359 376.
66. Wrobel, M., Zebrowski, J. Szopa, J. (2004) Polyhydroxybutyrate synthesis in transgenic flax. J. Biotechnol. 107, 41 54.
67. Wu, G.Y., Bazer, F.W., Davis, T.A., Jaeger, L.A., Johnson, G.A., Kim, S.W., Knabe, D.A., Meininger, C.J., Spencer, T.E. Yin, Y.L. (2007) Important roles for the arginine family of amino acids in swine nutrition and production. Livestock Sci. 112, 8 22.
68. Yeramian, A., Martin, L., Arpa, L., Bertran, J., Soler, C., McLeod, C., Modolell, M., Palacin, M., Lloberas, J. Celada, A. (2006) Macrophages require distinct arginine catabolism and transport systems for proliferation and for activation. Eur. J. Immunol. 36, 1516 1526.
69. Ziegler, K., Diener, A., Herpin, C., Richter, R., Deutzmann, R. Lockau, W. (1998) Molecular characterization of cyanophycin synthetase, the enzyme catalyzing the biosynthesis of the cyanobacterial reserve material multi-L-arginyl-poly-L-aspartate (cyanophycin). Eur. J. Biochem. 254, 154 159.
70. Ziegler, K., Deutzmann, R. Lockau, W. (2002) Cyanophycin synthetase-like enzymes of non-cyanobacterial eubacteria: characterization of the polymer produced by a recombinant synthetase of Desulfitobacterium hafniense. Z Naturforsch., C, J. Biosci. 57, 522 529.
71. Zotz, R.J., Schenk, S., Kuhn, A., Schlunken, S., Krone, V., Bruns, W., Genth, S. Schuler, G. (2001) Safety and efficacy of LK565 - a new polymer ultrasound contrast agent. Z. Kardiol. 90, 419 426.