An insect peptide engineered into the tomato prosystemin gene is released in transgenic tobacco plants and exerts biological activity

Plant Molecular Biology

Volumn 53, Issue 6, 2003, Pages 891-902

  Tortiglione, Claudia ^a   Fogliano, Vincenzo ^a   Ferracane, Rosalia ^a   Fanti, Paolo ^a   Pennacchio, Francesco ^a   Monti, Luigi Maria ^a   Rao, Rosa ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Insecticidal peptides; Prohormone processing; Systemin; Transgene expression; Trypsin modulating oostatic factor (TMOF)

Indexed keywords

AMINO ACIDS; HORMONES; INSECT CONTROL; PLANTS (BOTANY); TOXICITY;

INSECT LARVAE; INSECT PEPTIDES;

GENES;

EMBRYOPHYTA; HELIOTHIS; HELIOTHIS VIRESCENS; INSECTA; LYCOPERSICON ESCULENTUM; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

HYBRID PROTEIN; MESSENGER RNA; OLIGOPEPTIDE; OOSTATIC FACTOR, MOSQUITO; PEPTIDE; PEPTIDE HORMONE; PROSYSTEMIN PROTEIN, LYCOPERSICON ESCULENTUM; SYSTEMIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DRUG EFFECT; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LARVA; METABOLISM; MOLECULAR GENETICS; MOTH; PLANT LEAF; SECRETION; TOBACCO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GENE EXPRESSION; LARVA; MOLECULAR SEQUENCE DATA; MOTHS; OLIGOPEPTIDES; PEPTIDE HORMONES; PEPTIDES; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TOBACCO;

EID: 3242736673     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PLAN.0000023667.62501.ef     Document Type: Article

References (43)

1. An, G., Ebert, P.R., Mitra, A. and Ha, S.B. 1988: Binary vectors. In: G.B. Gelvin, R.A. Schilperoort and D.P.S. Verma (Eds.) Plant Molecular Biology Manual, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. A3: 1-19.
2. Baggerman, G., Huybrechts, J., Clynen, E., Hens, K., Harthoorn, L., van der Horst, D., Poulos, C., de Loof, A. and Schoofs, L. 2002. New insights in adipokinetic hormone (AKH) precursor processing in Locusta migratoria obtained by capillary liquid chromatography-tandem mass spectrometry (1). Peptides 23: 635-644.
3. Bergey, D.R., Howe, G.A. and Ryan, C.A. 1996. Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. USA 93: 12053-12058.
4. Bergey, D.R., Orozco-Cardenas, M., de Moura, D.S. and Ryan, C.A. 1999. A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc. Natl. Acad. Sci. USA 96: 1756-1760.
5. Borovsky, D., Carlson, D.A., Griffin, P.R., Shabanowitz, J. and Hunt, D.F. 1990. Mosquito oostatic factor: a novel decapeptide modulating trypsin-like enzymes biosynthesis in the midgut. J. Fed. Am. Soc. Exp. Biol. 4: 3015-3020.
6. Borovsky, D., Carlson, D.A., Griffin, P.R., Shabanowitz, J. and Hunt, D.F. 1993. .Mass spectrometry and characterization of Aedes aegypti trypsin modulating oostatic factor (TMOF) and its analogs. Insect Biochem. Mol. Biol. 23: 703-712.
7. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein dye binding. Anal. Biochem. 72: 248-254.
8. Constabel, C.P., Yip, L. and Ryan C.A. 1998. Prosystemin from potato, black nightshade and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 36: 55-62.
9. Delano, J.P., Dombrowski, J.E. and Ryan, C.A. 1999. The expression of tomato prosystemin in Escherichia coli: a structural challenge. Prot. Expr. Purific. 17: 74-82.
10. Dmochowska, A., Dignard, D., Henning, D., Thomas, D.Y. and Bussey, H. 1987. Yeast KEX1 gene encodes a putative protease with a carboxypeptidase B-like function involved in killer toxin and alpha-factor precursor processing. Cell 14: 573-584.
11. Dombrowski, J.E., Pearce, G. and Ryan, C.A. 1999. Proteinase inhibitor-inducing activity of the prohormone prosystemin resides exclusively in the C-terminal systemin domain. Proc. Natl. Acad. Sci. USA 22: 12947-12952.
12. Doyle, J.J. and Doyle, J.L. 1987. Genomic Plant DNA preparation from fresh tissue. Phytochem. Bull. 19: 11-14.
13. D'Hont, K., Bosch, D., Van Damme, J., Goethals, M., Vandekerckhove, J. and Krebbers, E. 1993. An aspartic endoproteinase present in seed cleaves Arabidopsis 2S albumins in vitro. J. Biol. Chem. 268: 20884-20891.
14. Einarsson, S., Josefsson, B. and Lagerkvist, S. 1983. Determination of amino acids with 9-fluorenylmethyl chloroformate and reversed-phase high-performance liquid chromatography. J. Chromatogr. 282: 609-618.
15. Francois, I.E., De Bolle, M., Dwyer, G., Goderis, I., Woutors, P., F., Verhaert, P., Proost, P., Schaaper, W., M., Cammue, B. and Broekaert, W. 2002. Transgenic expression in Arabidopsis of a polyprotein construct leading to production of two different antimicrobial proteins. Plant Physiol. 128: 1346-1358.
16. Halpin, C., Cooke, S.E., Barakate, A., El Amrani, A. and Ryan, M., D. 1999. Self-processing 2A-polyproteins: a system for coordinate expression of multiple proteins in transgenic plants. Plant J. 17: 453-459.
17. Higo, K., Saito, Y. and Higo, H. 1993. Expression of a chemically synthesised gene for human epidermal growth factor under the control of cauliflower mosaic virus 35S promoter in transgenic tobacco. Biosci. Biotech. Biochem. 57: 1477-1481.
18. Horsh, R.B., Fry, J.E., Hoffmann, N.L., Eicholtz, D., Rogers, S.H. and Fraley, R.T. 1987. A simple and general method for transferring genes in plants. Science 227: 1229-1231.
19. McGurl, B. and Ryan, C.A. 1992. The organization of the prosystemin gene. Plant Mol. Biol. 20: 405-409.
20. McGurl, B., Pearce, G., Orozco-Cardenas, M. and Ryan, C.A. 1992. Structure, expression, and antisense inhibition of the systemin precursor gene. Science 20: 1570-1573.
21. McGurl B, Orozco-Cardenas M, Pearce G, Ryan CA. 1994. Over-expression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 11: 9799-9802.
22. Nauen, R., Sorge, D., Sterner, A. and Borovsky, D. 2001. TMOF-like factor controls the biosynthesis of serine proteases in the larval gut of Heliothis virescens. Arch. Insect Biochem. Physiol. 47: 169-180.
23. Narvaez-Vasquez, J. and Ryan, C.A. 2003. The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 10.1007/s00425-003-1115-3.
24. Okamoto, M., Mitsuhara, I., Ohshima, M., Natori, S. and Ohashi, Y. 1998. Enhanced expression of an antimicrobial peptide sarcotoxin IA by GUS fusion in transgenic tobacco plants. Plant Cell Physiol. 39: 57-63.
25. Pearce, G. and Ryan, C.A. 2003. Systemic signaling in tomato for defense against herbivores: isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J. Biol. Chem. 8: 30044-30050.
26. Pearce, G., Moura, D.S., Stratmann, J. and Ryan, C.A. 2001a. RALF, a 5-KDa ubiquitous polypeptide in plants, arrest root growth and development. Proc. Natl. Acad. Sci. USA 22: 12843-12847.
27. Pearce, G., Moura, D.S., Stratmann, J. and Ryan, C.A. 2001b. Production of multiple plant hormones from a single polyprotein precursor. Nature 14: 817-820.
28. Rao, R., Manzi, A., Filippone, E., Manfredi, P., Spasiano, A., Colucci, G., Monti, L. and Malva, C. 1996. Synthesis and expression of genes encoding putative insect neuropeptide precursor in tobacco. Gene 175: 1-5.
29. Ryan, C.A., Pearce, G., Scheer, J., and Moura, D. 2002. Polypeptide hormone. Plant Cell 14: S251-S264.
30. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
31. Schaller, A. 1998. Action of proteolysis-resistant systemin analogues in wound signalling. Phytochemistry 47: 605-612.
32. Schaller, A. and Ryan, C.A. 1994. Identification of a 50-kDa systemin-binding protein in tomato plasma membranes having Kex2p like properties. Proc. Natl. Acad. Sci. USA 91: 11802-11806.
33. Scheer, J.M. and Ryan C.A. 1999. A 160-kD systemin receptor on the surface of Lycopersicon peruvianum cultured cells. Plant Cell 11: 1525-1535.
34. Seidach, N.G., Chretien, M. and Day, R. 1994. The family of subtilisin/kexin like pro-protein and pro-hormone convertase: divergent or shared functions. Biochimie 76: 197-209.
35. Sokal, R.R. and Rohlf, F.J. 1995. Biometry, 3rd ed. Freeman, New York.
36. Steiner, D.F., Smeekens, S.P., Ohagi, S. and Chan, S.J. 1992. The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267: (AUTHOR: PLEASE FILL IN PAGES).
37. SPSS Inc. 1999. Systat for Windows Statistics I, 660 pp.
38. Tortiglione, C., Malva, C., Pennacchio, F. and Rao, R. 1999. New genes for pest control. In: Scarascia Mugnozza, G.T., Porceddu, E. and Magnotta, E.A. (Eds.) Genetics and Breeding for Crop Quality and Resistance, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 159-163.
39. Tortiglione, C., Fanti, P., Pennacchio, F., Malva, C., Breuer, M., De Loof, A., Monti, L., Tremblay E. and Rao, R. 2002. The expression in tobacco plants of Aedes aegypti Trypsin Modulating Oostatic Factor (Aea-TMOF) alters growth and development of the tobacco budworm, Heliothis virescens. Mol. Breed. 9: 159-169.
40. Verwoerd, T.C., van Paridon, P.A., van Ooyen, A.J.J., van Lent, J.W.M., Hoekema, A. and Pen. J. 1995. Stable accumulation of Aspergillus niger phytase in transgenic tobacco leaves. Plant Physiol. 109: 1199-1205.
41. Vetsch, M., Janzik, I. and Shaller, A. 2000. Characterization of prosystemin expressed in the baculovirus/insect cell system reveals biological activity of the systemin precursor. Planta 211: 91-97.
42. Yang, H., Matsubayashi, Y., Nakamura, K. and Sakagami, Y. 1999. Oryza sativa PSK gene encodes a precursor of phytosulfokine-α, a sulfated peptide growth factor found in plants. Proc. Natl. Acad. Sci. USA 23: 13560-13565.
43. Yang, H., Matsubayashi, Y., Nakamura, K. and Sakagami, Y. 2001. Diversity of Arabidopsis genes encoding precursor for phytosulfokines, a peptide growth factor. Plant Physiol. 127: 842-851.