The production of recombinant cationic α-helical antimicrobial peptides in plant cells induces the formation of protein bodies derived from the endoplasmic reticulum

Plant Biotechnology Journal

Volumn 12, Issue 1, 2014, Pages 81-92

  Company, Nuri ^a   Nadal, Anna ^a   La Paz, José Luis ^b   Martínez, Sílvia ^b   Rasche, Stefan ^c   Schillberg, Stefan ^c   Montesinos, Emilio ^a   Pla, Maria ^a  

^a UNIVERSITY OF GIRONA   (Spain)

^b CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^c FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

Author keywords

Antimicrobial peptide; BP100; Cationic peptide; Molecular farming; Protein body; Transgenic plant

Indexed keywords

ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA;

ANTIMICROBIAL CATIONIC PEPTIDE; BP100; CATIONIC PEPTIDE; POLYPEPTIDE ANTIBIOTIC AGENT; VEGETABLE PROTEIN;

ARTICLE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR FARMING; PLANT CELL; PROTEIN BODY; RICE; TOBACCO; TRANSGENIC PLANT;

ANTIMICROBIAL PEPTIDE; BP100; CATIONIC PEPTIDE; MOLECULAR FARMING; PROTEIN BODY; TRANSGENIC PLANT;

ANTIMICROBIAL CATIONIC PEPTIDES; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT CELLS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TOBACCO;

EID: 84891148781     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12119     Document Type: Article

References (73)

1. Ajesh, K. and Sreejith, K. (2009) Peptide antibiotics: an alternative and effective antimicrobial strategy to circumvent fungal infections. Peptides, 30, 999-1006.
2. Alves, C.S., Melo, M.N., Franquelim, H.G., Ferré, R., Planas, M., Feliu, L., Bardají, E., Kowalczyk, W., Andreu, D., Santos, N.C., Fernandes, M.X. and Castanho, M.A. (2010) Escherichia coli cell surface perturbation and disruption induced by antimicrobial peptides BP100 and pepR. J. Biol. Chem. 285, 27536-27544.
3. Badosa, E., Ferré, R., Planas, M., Feliu, L., Besalú, E., Cabrefiga, J., Bardají, E. and Montesinos, E. (2007) A library of linear undecapeptides with bactericidal activity against phytopathogenic bacteria. Peptides, 28, 2276-2285.
4. Badosa, E., Ferre, R., Frances, J., Bardaji, E., Feliu, L., Planas, M. and Montesinos, E. (2009) Sporicidal activity of synthetic antifungal undecapeptides and control of Penicillium rot of apples. Appl. Environ. Microbiol. 75, 5563-5569.
5. Bardají, E. Antimicrobial linear peptides. (Patent WO/2007/125142 A1). (2006).
6. Bechinger, B. (2004) Structure and function of membrane-lytic peptides. Crit. Rev. Plant Sci. 23, 271-292.
7. Boman, H.G. (2003) Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med. 254, 197-215.
8. Broekaert, W., Cammue, B., De Bolle, M., Thevissen, K., De Samblanx, G. and Osborn, R. (1997) Antimicrobial peptides from plants. Crit. Rev. Plant Sci. 16, 297-323.
9. Brogden, K.A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250.
10. Brogden, K.A., Ackermann, M., McCray, P.B. Jr and Tack, B.F. (2003) Antimicrobial peptides in animals and their role in host defences. Int. J. Antimicrob. Agents, 22, 465-478.
11. Bulet, P. and Stocklin, R. (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12, 3-11.
12. Bulet, P., Stocklin, R. and Menin, L. (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 198, 169-184.
13. Cavallarín, L., Andreu, D. and San Segundo, B. (1998) Cecropin A-derived peptides are potent inhibitors of fungal plant pathogens. Mol. Plant Microbe Interact. 11, 218-227.
14. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Coca, M., Peñas, G., Gómez, J., Campo, S., Bortolotti, C., Messeguer, J. and San Segundo, B. (2006) Enhanced resistance to the rice blast fungus Magnaporthe grisea conferred by expression of a cecropin A gene in transgenic rice. Planta, 223, 392-406.
16. Coll, A., Nadal, A., Palaudelmàs, M., Messeguer, J., Melé, E., Puigdomènech, P. and Pla, M. (2008) Lack of repeatable differential expression patterns between MON810 and comparable commercial varieties of maize. Plant Mol. Biol. 68, 105-117.
17. Conley, A.J., Joensuu, J.J., Menassa, R. and Brandle, J.E. (2009) Induction of protein body formation in plant leaves by elastin-like polypeptide fusions. BMC Biol. 7, 48.
18. Conley, A.J., Joensuu, J.J., Richman, A. and Menassa, R. (2011) Protein body-inducing fusions for high-level production and purification of recombinant proteins in plants. Plant Biotechnol. J. 9, 419-433.
19. Cooter, P.D., Hill, C. and Ross, P. (2010) Bacterial lantibiotics: strategies to improve therapeutic potential. Curr. Prot. Pept. Sci. 6, 61-75.
20. Degenkolb, T., Berg, A., Gams, W., Schlegel, B. and Grafe, U. (2003) The occurrence of peptaibols and structurally related peptaibiotics in fungi and their mass spectrometric identification via diagnostic fragment ions. J. Pept. Sci. 9, 666-678.
21. Eggenberger, K., Mink, C., Wadhwani, P., Ulrich, A.S. and Nick, P. (2011) Using the peptide Bp100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells. ChemBioChem, 12, 132-137.
22. 2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J. Plant Physiol. 168, 1157-1167.
23. Ferré, R., Melo, M.N., Correira, A.D., Feliu, L., Bardají, E., Planas, M. and Castanho, M. (2009) Synergistic effects of the membrane actions of cecropin-melittin antimicrobial hybrid peptide BP100. Biophys. J. 96, 1815-1827.
24. Fischer, R., Stoger, E., Schillberg, S., Christou, P. and Twyman, R.M. (2004) Plant-based production of biopharmaceuticals. Curr. Opin. Plant Biol. 7, 152-158.
25. Ganz, T. (2003) Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-720.
26. Goytia, E., Fernández-Calvino, L., Martínez-García, B., López-Abella, D. and López-Moya, J.J. (2006) Production of plum pox virus HC-Pro functionally active for aphid transmission in a transient-expression system. J. Gen. Virol. 87, 3413-3423.
27. Hancock, R.E. (2001) Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1, 156-164.
28. Hoja, U. and Sonnewald, U. (2013) Molecular Farming in Plants, Encyclopedia of Life Sciences. Chichester: John Wiley & Sons Ltd.
29. Huang, H.W. (2000) Action of antimicrobial peptides: two-state model. Biochemistry, 39, 8347-8352.
30. Huang, H.W. (2006) Molecular mechanism of antimicrobial peptides: the origin of cooperativity. Biochim. Biophys. Acta, 1758, 1292-1302.
31. Jack, R.W. and Jung, G. (2000) Lantibiotics and microcins: polypeptides with unusual chemical diversity. Curr. Opin. Chem. Biol. 4, 310-317.
32. Jenssen, H., Hamill, P. and Hancock, R.E. (2006) Peptide antimicrobial agents. Clin. Microbiol. Rev. 19, 491-511.
33. Jiang, W. and Liu, D. (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol. 10, 40.
34. Joensuu, J.J., Conley, A.J., Lienemann, M., Brandle, J.E., Linder, M.B. and Menassa, R. (2010) Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol. 152, 622-633.
35. Joseph, M., Ludevid, M.D., Torrent, M., Rofidal, V., Tauzin, M., Rossignol, M. and Peltier, J.B. (2012) Proteomic characterisation of endoplasmic reticulum-derived protein bodies in tobacco leaves. BMC Plant Biol. 12, 36.
36. Khan, I., Twyman, R.M., Arcalis, E. and Stoger, E. (2012) Using storage organelles for the accumulation and encapsulation of recombinant proteins. Biotechnol. J. 7, 1099-1108.
37. Lay, F.T. and Anderson, M.A. (2005) Defensins-components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85-101.
38. Liu, D., Jiang, W., Meng, Q., Zou, J., Gu, J. and Zeng, M. (2009) Cytogenetical and ultrastructural effects of copper on root meristem cells of Allium sativum L. Biocell, 33, 25-32.
39. Llop-Tous, I., Madurga, S., Giralt, E., Marzabal, P., Torrent, M. and Ludevid, M.D. (2010) Relevant elements of a maize gamma-zein domain involved in protein body biogenesis. J. Biol. Chem. 285, 35633-35644.
40. López-García, B., Pérez-Paya, E. and Marcos, J.F. (2002) Identification of novel hexapeptides bioactive against phytopathogenic fungi through screening of a synthetic peptide combinatorial library. Appl. Environ. Microbiol. 68, 2453-2460.
41. Marcos, J.F. and Gandía, M. (2009) Antimicrobial peptides: to membranes and beyond. Expert Opin. Drug Discov. 4, 659-671.
42. Marcos, J.F., Muñoz, A., Pérez-Paya, E., Misra, S. and López-García, B. (2008) Identification and rational design of novel antimicrobial peptides for plant protection. Annu. Rev. Phytopathol. 46, 273-301.
43. Matz, M.V., Fradkov, A.F., Labas, Y.A., Savitsky, A.P., Zaraisky, A.G., Markelov, M.L. and Lukyanov, S.A. (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17, 969-973.
44. Mitsuhara, I., Matsufuru, H., Ohshima, M., Kaku, H., Nakajima, Y., Murai, N., Natori, S. and Ohashi, Y. (2000) Induced expression of sarcotoxin IA enhanced host resistance against both bacterial and fungal pathogens in transgenic tobacco. Mol. Plant Microbe Interact. 13, 860-868.
45. Monroc, S., Badosa, E., Besalú, E., Planas, M., Bardají, E., Montesinos, E. and Feliu, L. (2006) Improvement of cyclic decapeptides against plant pathogenic bacteria using a combinatorial chemistry approach. Peptides, 27, 2575-2584.
46. Montero, M., Coll, A., Nadal, A., Messeguer, J. and Pla, M. (2011) Only half the transcriptomic differences between resistant genetically modified and conventional rice are associated with the transgene. Plant Biotechnol. J. 9, 693-702.
47. Montesinos, E. (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol. Lett. 270, 1-11.
48. Montesinos, E. and Bardají, E. (2008) Synthetic antimicrobial peptides as agricultural pesticides for plant-disease control. Chem. Biodivers. 5, 1225-1237.
49. Montesinos, E., Badosa, E., Cabrefiga, J., Planas, M., Feliu, L. and Bardají, E. (2012) Antimicrobial peptides for plant disease control. From discovery to application. In Small Wonders: Peptides for Disease Control (Rajasekaran, K., Cary, J., Jaynes, J. and Montesinos, E., eds.), pp. 235-261. Washington, DC: Oxford University Press.
50. Moreno, A.B., Martínez, D.P. and San Segundo, B. (2006) Biotechnologically relevant enzymes and proteins. Antifungal mechanism of the Aspergillus giganteus AFP against the rice blast fungus Magnaporthe grisea. Appl. Microbiol. Biotechnol. 72, 883-895.
51. Nadal, A., Montero, M., Company, N., Badosa, E., Messeguer, J., Montesinos, L., Montesinos, E. and Pla, M. (2012) Constitutive expression of transgenes encoding derivatives of the synthetic antimicrobial peptide BP100: impact on rice host plant fitness. BMC Plant Biol. 12, 159.
52. Ng, T.B. (2004) Peptides and proteins from fungi. Peptides, 25, 1055-1073.
53. Oh, D., Shin, S.Y., Lee, S., Kang, J.H., Kim, S.D., Ryu, P.D., Hahm, K.S. and Kim, Y. (2000) Role of the hinge region and the tryptophan residue in the synthetic antimicrobial peptides, cecropin A(1-8)-magainin 2(1-12) and its analogues, on their antibiotic activities and structures. Biochemistry, 39, 11855-11864.
54. Otvos, L. Jr. (2000) Antibacterial peptides isolated from insects. J. Pept. Sci. 6, 497-511.
55. Peschel, A. and Sahl, H.G. (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4, 529-536.
56. Piotrzkowski, N., Schillberg, S. and Rasche, S. (2012) Tackling heterogeneity: a leaf disc-based assay for the high-throughput screening of transient gene expression in tobacco. PLoS ONE, 7, e45803.
57. Pons, M.J., Marfà, V., Melé, E. and Messeguer, J. (2000) Regeneration and genetic transformation of Spanish rice cultivars using mature embryos. Euphytica, 114, 117-122.
58. Raaijmakers, J.M., De Bruijn, I. and de Kock, M.J. (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol. Plant Microbe Interact. 19, 699-710.
59. Rajasekaran, K., Cary, J., Jaynes, J. and Montesinos, E. (2012) Small Wonders: Peptides for Disease Control. American Chemical Society: Oxford University Press.
60. Rasche, S., Martin, A., Holzem, A., Fischer, R., Schinkel, H. and Schillberg, S. (2011) One-step protein purification: Use of a novel epitope tag for highly efficient detection and purification of recombinant proteins. Open Biotechnol. J. 5, 1-6.
61. Sambrook, J. and Russell, D. (2001) Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
62. Tincu, J.A. and Taylor, S.W. (2004) Antimicrobial peptides from marine invertebrates. Antimicrob. Agents Chemother. 48, 3645-3654.
63. Toke, O. (2005) Antimicrobial peptides: new candidates in the fight against bacterial infections. Biopolymers, 80, 717-735.
64. Torrent, M., Llompart, B., Lasserre-Ramassamy, S., Llop-Tous, I., Bastida, M., Marzabal, P., Westerholm-Parvinen, A., Saloheimo, M., Heifetz, P.B. and Ludevid, M.D. (2009) Eukaryotic protein production in designed storage organelles. BMC Biol. 7, 5.
65. Torrent, M., Pulido, D., Rivas, L. and Andreu, D. (2012) Antimicrobial peptide action on parasites. Curr. Drug Targets, 13, 1138-1147.
66. Tossi, A., Sandri, L. and Giangaspero, A. (2000) Amphipathic, alpha-helical antimicrobial peptides. Biopolymers, 55, 4-30.
67. Truernit, E. and Haseloff, J. (2008) A simple way to identify non-viable cells within living plant tissue using confocal microscopy. Plant Methods, 4, 15.
68. Twyman, R.M., Stoger, E., Schillberg, S., Christou, P. and Fischer, R. (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 21, 570-578.
69. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome biology, 3, Research 0034.
70. Vaquero, C., Sack, M., Chandler, J., Drossard, J., Schuster, F., Monecke, M., Schillberg, S. and Fischer, R. (1999) Transient expression of a tumor-specific single-chain fragment and a chimeric antibody in tobacco leaves. Proc. Natl Acad. Sci. USA, 96, 11128-11133.
71. Yeaman, M.R. and Yount, N.Y. (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55.
72. Yount, N.Y. and Yeaman, M.R. (2005) Immunocontinuum: perspectives in antimicrobial peptide mechanisms of action and resistance. Protein Pept. Lett. 12, 49-67.
73. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature, 415, 389-395.