Antimicrobial peptides from fruits and their potential use as biotechnological Tools-A review and outlook

Frontiers in Microbiology

Volumn 7, Issue JAN, 2017, Pages

  Meneguetti, Beatriz T ^a   Machado, Leandro dos Santos ^a   Oshiro, Karen G N ^a   Nogueira, Micaella L ^a   Carvalho, Cristiano M E ^a   Franco, Octávio L ^a,b  

^a UNIVERSIDADE CATÓLICA DOM BOSCO   (Brazil)

^b UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

Antimicrobial peptides; Biotechnological potential; Fruits; Infections; Microorganisms

Indexed keywords

DEFENSIN; ETHYLENE; GLYCINE RICH PROTEIN; JASMONIC ACID METHYL ESTER; LIPID TRANSFER PROTEIN; NAPIN; POLYPEPTIDE ANTIBIOTIC AGENT; SALICYLIC ACID; SNAKIN; TENASCIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BIOTECHNOLOGICAL PROCEDURES; CELLULAR STRESS RESPONSE; DISK DIFFUSION; ENVIRONMENTAL STRESS; FRUIT; HYDROPHOBICITY; IC50; INNATE IMMUNITY; NONHUMAN; NORTHERN BLOTTING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; WESTERN BLOTTING;

EID: 85011948999     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.02136     Document Type: Review

References (167)

1. Abdallah, N. A., Shah, D., Abbas, D., and Madkour, M. (2010). Stable integration and expression of a plant defensin in tomato confers resistance to fusarium wilt. GM Crops 1, 344-350. doi: 10.4161/gmcr.1.5.15091
2. Abreu, A. C., Borges, A., Simoes, L. C., Saavedra, M. J., and Simões, M. (2013). Antibacterial activity of phenyl isothiocyanate on Escherichia coli and Staphylococcus aureus. Med. Chem. 9, 756-761. doi: 10.2174/1573406411309050016
3. Agizzio, A. P., Carvalho, A. O., Ribeiros, S. de. F. F., Machado, O. L., Alves, E. W., Okorokov, L. A., et al. (2003). A 2S albumin-homologous protein from passion fruit seeds inhibits the fungal growth and acidification of the medium by Fusarium oxysporum. Arch. Biochem. Biophys. 416, 188-195. doi: 10.1016/S0003-9861(03)00313-8
4. Almeida, M. S., Cabral, K. M., Zingali, R. B., and Kurtenbach, E. (2000). Characterization of two novel defense peptides from pea (Pisum sativum) seeds. Arch. Biochem. Biophys. 378, 278-286. doi: 10.1006/abbi.2000.1824
5. Amien, S., Kliwer, I., Márton, M. L., Debener, T., Geiger, D., Becker, D., et al. (2010). Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS. Biol. 8:e1000388. doi: 10.1371/journal.pbio.1000388
6. Artlip, T. S., and Wisniewski, M. E. (2001). "Induction of proteins in reponse to biotic and abiotic stresses, " in Handbook of Plant and Crop Physiology, 2nd Edn, ed M. Pessarakli (New York, NY: Marcel Dekker), 657-679.
7. Asthana, N., Yadav, S. P., and Ghosh, J. K. (2004). Dissection of antibacterial and toxic activity of melittin: a leucine zipper motif plays a crucial role in determining its hemolytic activity but not antibacterial activity. J. Biol. Chem. 279, 55042-55050. doi: 10.1074/jbc.M408881200
8. Banemann, A., Deppisch, H., and Gross, R. (1998). The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect. Immun. 66, 5607-5612.
9. Baxter, A. A., Richter, V., Lay, F. T., Poon, I. K., Adda, C. G., Veneer, P. K., et al. (2015). The tomato defensin TPP3 binds phosphatidylinositol (4, 5)-bisphosphate via a conserved dimeric cationic grip conformation to mediate cell lysis. Mol. Cell. Biol. 35, 1964-1978. doi: 10.1128/MCB.00282-15
10. Berecz, B., Mills, E. N., Tamás, L., Láng, F., Shewry, P. R., and Mackie, A. R. (2010). Structural stability and surface activity of sunflower 2S albumins and nonspecific lipid transfer protein. J. Agric. Food Chem. 58, 6490-6497. doi: 10.1021/jf100554d
11. α1. Similarity to scorpion toxins. Proteins 32, 334-349.
12. Broekaert, W. F., Cammue, B. P. A., de Bolle, M. F. C., Thevissen, K., de Samblanx, G. W., and Osborn, R. W. (1997). Antimicrobial peptides from plants. Crit. Rev. Plant Sci. 16, 297-323. doi: 10.1080/07352689709701952
13. Broekaert, W. F., Terras, F. R., Cammue, B. P., and Osborn, R. W. (1995). Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108, 1353-1358. doi: 10.1104/pp.108.4.1353
14. Brogden, K. A. (2005). Antimicrobial peptide spore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250. doi: 10.1038/nrmicro1098
15. Brogden, N. K., and Brogden, K. A. (2011). Will new generations of modified antimicrobial peptides improve their potential as pharmaceuticals? Int. J. Antimicrob. Agents 38, 217-225. doi: 10.1016/j.ijantimicag.2011.05.004
16. Bruix, M., González, C., Santoro, J., Soriano, F., Rocher, A., Méndez, E., et al. (1995). 1H NMR studies on the structure of a new thionin from barley endosperm. Biopolymers 36, 751-763. doi: 10.1002/bip.360360608
17. Bruix, M., Jimenez, M. A., Santoro, J., González, C., Colilla, F. J., Mendez, E., et al. (1993). Solution structure of gamma 1-H and gamma 1-P thionins from barley and wheat endosperm determined by 1H-NMR: a structural motif common to toxic arthropod proteins. Biochemistry 32, 715-724. doi: 10.1021/bi00053a041
18. Byczynska, A., and Barciszewsk, J. (1999). The biosynthesis, structure and properties of napin-the storage protein from rape seeds. J. Plant Physiol. 154, 417-425. doi: 10.1016/S0176-1617(99)80277-6
19. Campos, M. A., Vargas, M. A., Regueiro, V., Llompart, C. M., Albertí, S., and Bengoechea, J. A. (2004). Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect. Immun. 72, 7107-7114. doi: 10.1128/IAI.72.12.7107-7114.2004
20. Carvalho, A. de. O., and Gomes, V. M. (2001). Plant defensins and defensin-like peptides-biological activities and biotechnological applications. Curr. Pharm. Des. 17, 4270-4293. doi: 10.2174/138161211798999447
21. Carvalho, A. de. O., and Gomes, V. M. (2007). Role of plant lipid transfer proteins in plant cell physiology-a concise review. Peptides 28, 1144-1153. doi: 10.1016/j.peptides.2007.03.004
22. Chan, C., Burrows, L. L., and Deber, C. M. (2004). Helix induction in antimicrobial peptides by alginate in biofilms. J. Biol. Chem. 279, 38749-38754. doi: 10.1074/jbc.M406044200
23. Chen, S. C., Liu, A. R., and Zou, Z. R. (2006). Overexpression of glucanase gene and defensin gene in transgenic tomato enhances resistance to Ralstonia solanacearum. Russ. J. Plant Phys. 53, 671-677. doi: 10.1134/S1021443706050116
24. Chen, S. C., Liu, A. R., Wang, F. H., and Ahammed, G. J. (2009). Combined overexpression of chitinase and defensin genesin transgenic tomato enhances resistance to Botrytis cinerea. Afr. J. Biotech. 8, 5182-5188. doi: 10.5897/AJB09.704
25. Clark, A. M. (1996). Natural products as a resource for new drugs. Pharm. Res. 13, 1133-1144.
26. Corvec, S., Tafin, U. F., Betrisey, B., Borens, O., and Trampuz, A. (2013). Activities of fosfomycin, tigecycline, colistin, and gentamicin against extended-spectrum-β-lactamase-producing Escherichia coli in a foreign-body infection model. Antimicrob. Agents Chemother. 57, 1421-1427. doi: 10.1128/aac.01718-12
27. Cruz, L. P., Ribeiro, S. F., Carvalho, A. O., Vasconcelos, I. M., Rodrigues, R., Da Cunha, M., et al. (2010). Isolation and partial characterization of a novel lipid transfer protein (LTP) and antifungal activity of peptides from chilli pepper seeds. Protein Pept. Lett. 17, 311-318. doi: 10.2174/092986610790780305
28. da Silva, F. P., and Machado, M. C. C. (2012). Antimicrobial peptides: clinical relevance and therapeutic implications. Peptides 36, 308-314. doi: 10.1016/j.peptides.2012.05.014
29. Daneshmand, F., Zardini, H. Z., and Ebrahimi, L. (2013). Investigation of the antimicrobial activities of Snakin-Z, a new cationic peptide derived from Zizyphus jujube fruits. Nat. Product Res. 27, 2292-2296. doi: 10.1080/14786419.2013.827192
30. Da Silva Dantas, C. C., De Souza, E. L., Cardoso, J. D., De Lima, L. A., de Sousa Oliveira, K., Migliolo, L., et al. (2014). Identification of a napin-like peptide from Eugenia malaccensis L. Seeds with inhibitory activity toward Staphylococcus aureus and Salmonella Enteritidis. Protein J. 33, 549-556. doi: 10.1007/s10930-014-9587-5
31. de Beer, A., and Vivier, M. A. (2011). Four plant defensins from an indigenous South African Brassicaceae species display divergent activities against two test pathogens despite high sequence similarity in the encoding genes. BMC Res. Notes 4:459. doi: 10.1186/1756-0500-4-459
32. de Sousa Cândido, E., e Silva Cardoso, M. H., Sousa, D. A., Viana, J. C., de Oliveria-Júnior, N. G., Miranda, V., et al. (2014). The use of versatile plant antimicrobial peptides in agribusiness and human health. Peptides 55, 65-78. doi: 10.1016/j.peptides.2014.02.003
33. de Sousa Cândido, E., Pinto, M. F., Pelegrini, P. B., Lima, T. B., Silva, O. N., Pogue, R., et al. (2011). Plant storage proteins with antimicrobial activity: novel insights into plant defense mechanisms. FASEB J. 25, 3290-3305. doi: 10.1096/fj.11-184291
34. De Lucca, A. J. (2000). Antifungal peptides: potential candidates for the treatment of fungal infections. Expert Opin. Investig. Drugs 9, 273-299. doi: 10.1517/13543784.9.2.273
35. Diz, M. S. S., Carvalho, A. O., Rodrigues, R., Neves-Ferreira, A. G. C., Da Cunha, M., Alves, E. W., et al. (2006). Antimicrobial peptides from chilli pepper seeds causes yeast plasma membrane permeabilization and inhibits the acidification of the medium by yeast cells. Biochim. Biophys. Acta 1760, 1323-1332. doi: 10.1016/j.bbagen.2006.04.010
36. Diz, M. S., Carvalho, A. O., Ribeiro, S. F., Da Cunha, M., Beltramini, L., Rodrigues, R., et al. (2011). Characterisation, immunolocalisation and antifungal activity of a lipid transfer protein from chili pepper (Capsicum annuum) seeds with novel α-amylase inhibitory properties. Physiol. Plant. 142, 233-246. doi: 10.1111/j.1399-3054.2011.01464.x
37. Dobson, A. J., Purves, J., and Rolff, J. (2014). Increased survival of experimentally evolved antimicrobial peptide-resistant Staphylococcus aureus in an animal host. Evol. Appl. 7, 905-912. doi: 10.1111/eva.12184
38. Douliez, J. P., Michon, T., Elmorjani, K., and Marion, D. (2000). Structure, biological and technological functions of lipid transfer proteins and indolines, the major lipid-binding proteins from cereal kernels. J. Cereal Sci. 32, 1-20. doi: 10.1006/jcrs.2000.0315
39. Dutta, P., and Das, S. (2016). Mammalian antimicrobial peptides: promising therapeutic targets against infection and chronic inflammation. Curr. Top. Med. Chem. 16, 99-129. doi: 10.2174/1568026615666150703121819
40. Edstam, M. M., and Edqvist, J. (2014). Involvement of GPI-anchored lipid transfer proteins in the development of seed coats and pollen in Arabidopsis thaliana. Physiol. Plant. 152, 32-42. doi: 10.1111/ppl.12156
41. Ericson, M. L., Rödin, J., Lenman, M., Glimelius, K., Josefsson, L.-G., and Rask, L. (1986). Structure of the rapeseed 1.7 S storage protein, napin, and its precursor. J. Biol. Chem. 261, 14576-14581.
42. Falagas, M. E., and Kasiakou, S. K. (2005). Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin. Infect. Dis. 40, 1333-1341. doi: 10.1086/429323
43. Fant, F., Vranken, W., Broekaert, W., and Borremans, F. (1998). Determination of the three-dimensional solution structure of Raphanus sativus antifungal protein 1 by 1H NMR. J. Mol. Biol. 279, 257-270. doi: 10.1006/jmbi.1998.1767
44. Fant, F., Vranken, W. F., and Borremans, F. A. M. (1999). The three-dimensional solution structure of Aesculus hippocastanum antimicrobial protein 1 determined by 1H nuclear magnetic resonance. Proteins 37, 388-403.
45. Finkina, E. I., Melnikova, D. N., Bogdanov, I. V., and Ovchinnikova, T. V. (2016). Lipid transfer proteins as components of the plant innate immune system: structure, functions, and applications. Acta Naturae 8, 47-61.
46. Finkina, E. I., Shramova, E. I., Tagaev, A. A., and Ovchinnikova, T. V. (2008). A novel defesin from the lentil lens culinaris seeds. Biochem. Biophys. Res. Commun. 371, 860-865. doi: 10.1016/j.bbrc.2008.04.161
47. Fox, J. L. (2013). Antimicrobial peptides stage a comeback. Nat. Biotechnol. 31, 379-382. doi: 10.1038/nbt.2572
48. Franco, O. L. (2011). Peptide promiscuity: an evolutionary concept for plant defense. FEBS Lett. 585, 995-1000. doi: 10.1016/j.febslet.2011.03.008
49. Friedrich, C., Scott, M. G., Karunaratne, N., Yan, H., and Hancock, R. E. (1999). Salt-resistant alpha-helical cationic antimicrobial peptides. Antimicrob. Agents Chemother. 43, 1542-1548.
50. Ghag, S. B., Shekhawat, U. K. S., and Ganapathi, T. R. (2012). Petunia floral defensins with unique prodomains as novel candidates for development of Fusarium wilt resistance in transgenic banana plants. PLoS ONE 7:39557. doi: 10.1371/journal.pone.0039557
51. Ghag, S. B., Shekhawat, U. K. S., and Ganapathi, T. R. (2014). Transgenic banana plants expressing a Stellaria media defensin gene (Sm-AMP-D1) demonstrate improved resistance to Fusarium oxysporum. Plant Cell Tissue Organ Culture 119, 247-255. doi: 10.1007/s11240-014-0529-x
52. Giacomelli, L., Nanni, V., Lenzi, L., Zhuang, J., Serra, M. D., Banfield, M. J., et al. (2012). Identification and characterization of the defensin-like gene family of grapevine. Mol. Plant Microbe Interact. 25, 1118-1131. doi: 10.1094/MPMI-12-11-0323
53. Gordon, N. C., Png, K., and Wareham, D. W. (2010). Potent synergy and sustained bactericidal activity of a vancomycin-colistin combination versus multidrug-resistant strains of Acinetobacter baumannii. Antimicrob. Agents Chemother. 54, 5316-5322. doi: 10.1128/AAC.00922-10
54. Guani-Guerra, E., Garcia-Cruz, M. L., Zavala-Molina, D. M., Reyna-Guerra, J. M., Jimenez-Chobillon, M. A., and Teran, L. M. (2009). Natural history and clinical presentation of aspirin-exacerbated respiratory disease: effect of gender, atopy, and family history. Annu. Allerg. Asthma Immunol. 103:A71.
55. Guzmán-Rodríguez, J. J., López-Gómez, R., Suárez-Rodríguez, L. M., Salgado-Garciglia, R., Rodríguez-Zapata, L. C., Ochoa-Zarzosa, A., et al. (2013). Antibacterial activity of defensin PaDef from Avocado Fruit (Persea americana var. drymifolia) expressed in endothelial cells against Escherichia coli and Staphylococcus aureus. BioMed. Res. Int. 2013:986273. doi: 10.1155/2013/986273
56. Hancock, R. E. W. (2000). Cationic antimicrobial peptides: towards clinical applications. Expert Opin. Investig. Drugs 9, 1723-1729. doi: 10.1517/13543784.9.8.1723
57. Hanks, J. N., Snyder, A. K., Graham, M. A., Shah, R. K., Blaylock, L. A., Harrison, M. J., et al. (2005). Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol. Biol. 58, 385-399. doi: 10.1007/s11103-005-5567-7
58. Harris, F., Dennison, S. R., and Phoenix, D. A. (2009). Anionic antimicrobial peptides from eukaryotic organisms. Curr. Protein Pept. Sci. 10, 585-606. doi: 10.2174/138920309789630589
59. Hayek, S. A., Gyawali, R., and Ibrahim, S. A. (2013). "Antimicrobial natural products, " in Microbial Pathogens and Strategies for Combating Them: Science, Technology and Education, Vol. 2, ed A. Méndez-Vílas (Greensboro, NC: Formatex Research Center), 910-921.
60. Herbel, V., Schäfer, H., and Wink, M. (2015). Recombinant production of snakin-2 (an antimicrobial peptide from tomato) in E. coli and analysis of its bioactivity. Molecules 20, 14889-14901. doi: 10.3390/molecules200814889
61. Holaskova, E., Galuszka, P., Frebort, I., and Oz Tufan, M. (2015). Antimicrobial peptide production and plant-based expression systems for medical and agricultural biotechnology. Biotechnol. Adv. 33, 1005-1023. doi: 10.1016/j.biotechadv.2015.03.007
62. Hsiao, E. S., Lin, L. J., Li, F. Y., Wang, M. M., Liao, M. Y., and Tzen, J. T. (2006). Gene families encoding isoforms of two major sesame seed storage proteins, 11S globulin and 2S albumin. J. Agric. Food Chem. 54, 9544-9550. doi: 10.1021/jf061505x
63. Huang, C., Jin, H., Qian, Y., Qi, S., Luo, H., Luo, Q., et al. (2013). Hybrid melittin cytolytic Peptide-driven ultrasmall lipid nanoparticles block melanoma growth in vivo. ACS Nano 7, 5791-5800. doi: 10.1021/nn400683s
64. Jenssen, H., Hamill, P., and Hancock, R. E. W. (2006). Peptide antimicrobial agents. J. Clin. Microbiol. Rev. 19, 491-511. doi: 10.1128/CMR.00056-05
65. Jeong, Y. J., Kim, I., Cho, J. H., Park, D. W., Kwon, J. E., Jung, M. W., et al. (2015). Anti-osteoarthritic effects of the Litsea japonica fruit in a rat model of osteoarthritis induced by monosodium iodoacetate. PLoS ONE 10:e0134856. doi: 10.1371/journal.pone.0134856
66. Jones, A., Geörg, M., Maudsdotter, L., and Jonsson, A.-B. (2009). Endotoxin, capsule, and bacterial attachment contribute to Neisseria meningitidis resistance to the human antimicrobial peptide LL-37. J. Bacteriol. 191, 3861-3868. doi: 10.1128/JB.01313-08
67. Kader, J.-C. (1996). Lipid-transfer proteins in plants. Annu Rev. Plant. Physiol. Plant Mol. Biol. 47, 627-654. doi: 10.1146/annurev.arplant.47.1.627
68. Kang, S. J., Kim, D. H., Mishig-Ochir, T., and Lee, B. J. (2012). Antimicrobial peptides: their physicochemical properties and therapeutic application. Arch. Pharm. Res. 35, 409-413. doi: 10.1007/s12272-012-0302-9
69. Keo, T., Collins, J., Kunwar, P., Blaser, M. J., and Iovine, N. M. (2011). Campylobacter capsule and lipooligosaccharide confer resistance to serum and cationic antimicrobials. Virulence 2, 30-40. doi: 10.4161/viru.2.1.14752
70. Kobayashi, Y., Sato, A., Takashima, H., Tamaoki, H., Nishimura, S., Kyogoku, Y., et al. (1991). A new α-helical motif in membrane active peptides. Neurochem. Int. 18, 525-534. doi: 10.1016/0197-0186(91)90151-3
71. Kosciuczuk, E. M., Lisowski, P., Jarczak, J., Strzalkowska, N., Józwik, A., Horbanczuk, J., et al. (2012). Cathelicidins: family of antimicrobial peptides. A review. Mol. Biol. Rep. 39, 10957-10970. doi: 10.1007/s11033-012-1997-x
72. Kushmerick, C., de Souza Castro, M., Santos Cruz, J., Bloch, C. Jr., and Beirão, P. S. (1998). Functional and structural features of γ-zeathionins, a new class of sodium channel blockers. FEBS Lett. 440, 302-306. doi: 10.1016/S0014-5793(98)01480-X
73. Lacerda, A. F., Vasconselos, E. A., Pelegrini, P. B., and Grossi de Sa, M. F. (2014). Antifungal defensins and their role in plant defense. Front. Microbiol. 5:116. doi: 10.3389/fmicb.2014.00116
74. Landman, D., Georgescu, C., Martin, D. A., and Quale, J. (2008). Polymyxins revisited. Clin. Microbiol. Rev. 21, 449-465. doi: 10.1128/CMR.00006-08
75. Lay, F. T., and Anderson, M. A. (2005). Defensins-components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85-101. doi: 10.2174/1389203053027575
76. Lay, F. T., Brugliera, F., and Anderson, M. A. (2003). Isolation and properties of floral defenses from ornamental tobacco and petunia. Plant Physiol. 131, 1283-1293. doi: 10.1104/pp.102.016626
77. Lee, J., and Lee, D. G. (2015). Antimicrobial peptides (amps) with dual mechanisms: membrane: disruption and apoptosis. J. Microbiol. Biotechnol. 25, 759-764.doi: 10.4014/jmb.1411.11058
78. Lee, T.-H., Hall, K. N., and Aguilar, M.-I (2016). Antimicrobial peptide structure and mechanism of action: a focus on the role of membrane structure. Curr. Top. Med. Chem. 16, 25-39. doi: 10.2174/1568026615666150703121700
79. Li, Y., Xiang, Q., Zhang, Q., Huang, Y., and Su, Z. (2012). Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37, 207-215. doi: 10.1016/j.peptides.2012.07.001
80. Lindorff-Larsen, K., Lerche, M. H., Poulsen, F. M., Roepstorff, P., and Winther, J. R. (2001). Barley lipid transfer protein, LTP1, contains a new type of lipid-like post-translational modification. J. Biol. Chem. 276, 33547-33553. doi: 10.1007/s002990100333
81. Liu, Y. J., Cheng, C. S., Lai, S. M., Hsu, M. P., Chen, C. S., and Lyu, P. C. (2006). Solution structure of the plant defensin VrD1 from mung bean and its possible role in insecticidal activity against bruchids. Proteins 63, 777-786. doi: 10.1002/prot.20962
82. Liu, Y., Luo, J., Xu, C., Ren, F., Peng, C., Wu, G., et al. (2000). Purification, characterization, and molecular cloning of the gene of a seed-specific antimicrobial protein from pokeweed. Plant Phys. 122, 1015-1024. doi: 10.1104/pp.122.4.1015
83. Llobet, E., Tomás, J. M., and Bengoechea, J. A. (2008). Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154, 3877-3886. doi: 10.1099/mic.0.2008/022301-0
84. López-García, B., González-Candelas, L., Pérez-Payá, E., and Marcos, J. F. (2000). Identification and characterization of a hexapeptide with activity against phytopathogenic fungi that cause postharvest decay in fruits. Mol. Plant Microbe Interact. 13, 837-846. doi: 10.1128/AEM.68.5.2453-2460.2002
85. Maitra, N., and Cushman, J. C. (1998). Characterization of a drought-induced soybean cDNA encoding a plant defensin. Plant Physiol. 118:1536.
86. Mandal, S. M., Dey, S., Mandal, M., Sarkar, S., Maria-Neto, S., and Franco, O. L. (2009). Identification and structural insights of three novel antimicrobial peptides isolated from green coconut water. Peptides 30, 633-637. doi: 10.1016/j.peptides.2008.12.001
87. Mandal, S. M., Migliolo, L., Franco, O. L., and Ghosh, A. K. (2011). Identification of an antifungal peptide from Trapa natans fruits with inhibitory effects on Candida tropicalis biofilm formation. Peptides 32, 1741-1747. doi: 10.1007/s10930-011-9337-x
88. Manners, J. (2009). Primitive defence: the MiAMP1 antimicrobial peptide family. Plant Mol. Biol. Rep. 27, 237-242. doi: 10.1007/s11105-008-0083-y
89. Mansour, S. C., Pena, O. M., and Hancock, R. E. (2014). Host defense peptides: front-line immunomodulators. Trends Immunol. 35, 443-450. doi: 10.1016/j.it.2014.07.004
90. Maria-Neto, S., Honorato, R. V., Costa, F. T., Almeida, R. G., Amaro, D. S., and Oliveira, J. T. (2011). Bactericidal activity identified in 2S albumin from sesame seeds and in silico studies of structure-function relations. Protein J. 30, 340-350. doi: 10.1007/s10930-011-9337-x
91. Maróti, G., Kereszt, A., Kondorosi, E., and Mergaert, P. (2011). Natural roles of antimicrobial peptides in microbes, plants and animals. Res. Microbiol. 162, 363-374. doi: 10.1016/j.resmic.2011.02.005
92. Marr, A. K., Gooderham, W. J., and Hancock, R. E. W. (2006). Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr.Opin. Pharmacol. 6, 468-472. doi: 10.1016/j.coph.2006.04.006
93. Matsuzaki, K. (1999). Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462, 1-10. doi: 10.1016/S0005-2736(99)00197-2
94. McPhee, J. B., Bains, M., Winsor, G., Lewenza, S., Kwasnicka, A., Brazas, M. D., et al. (2006). Contribution of the PhoP-PhoQ and PmrA-PmrB two-component regulatory systems to Mg2+-induced gene regulation in Pseudomonas aeruginosa. J. Bacteriol. 188, 3995-4006. doi: 10.1128/JB.00053-06
95. McPhee, J. B., Lewenza, S., and Hancock, R. E. (2003). Cationic antimicrobial peptides activate a twocomponent regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol. Microbiol. 50, 205-217. doi: 10.1046/j.1365-2958.2003.03673.x
96. Memarpoor-Yazdi, M., Mahakia, H., and Zare-Zardini, H. (2013). Antioxidant activity of protein hydrolysates and purified peptides from Zizyphus jujuba fruits. J. Funct. Foods 5, 62-70. doi: 10.1016/j.jff.2012.08.004
97. Meyer, B., Houlné, G., Pozueta-Romero, J., Schantz, M. L., and Schantz, R. (1996). Fruit specific expression of a defensin-type gene family in bell pepper. Upregulation during ripening and upon wounding. Plant Physiol. 112, 615-622. doi: 10.1104/pp.112.2.615
98. Montesinos, E. (2007). Antimicrobial peptides and plant disease control. FEMS Microbiol. Lett. 270, 1-11. doi: 10.1111/j.1574-6968.2007.00683.x
99. Moskowitz, S. M., Ernst, R. K., and Miller, S. I. (2004). PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J. Bacteriol. 186, 575-579. doi: 10.1128/JB.186.2.575-579.2004
100. Mousavi, A., and Hotta, Y. (2005). Glycine-rich proteins: a class of novel proteins. Appl. Biochem. Biotechnol. 120, 169-174. doi: 10.1385/ABAB:120:3:169
101. Muhle, S. A., and Tam, J. P. (2001). Design of Gram-negative selective antimicrobial peptides. Biochemistry 40, 5777-5785. doi: 10.1021/bi0100384
102. Müntz, K. (1998). Deposition of storage proteins. Plant Mol. Biol. 38, 77-99. doi: 10.1023/A:1006020208380
103. Naghmouchi, K., le Lay, C., Baah, J., and Drider, D. (2012). Antibiotic and antimicrobial peptide combinations: synergistic inhibition of Pseudomonas fluorescens and antibiotic-resistant variants. Res. Microbiol. 163, 101-108. doi: 10.1016/j.resmic.2011.11.002
104. Nahirñak, V., Almasia, N. I., Hopp, H. E., and Vazquez-Rovere, C. (2012). Snakin/GASA proteins: involvement in hormone crosstalk and redox homeostasis. Plant Signal. Behav. 7, 1004-1008. doi: 10.4161/psb.20813
105. Nanni, V., Zanetti, M., Bellucci, M., Moser, C., Bertolini, P., Guella, G., et al. (2013). The peach (Prunus persica) defensin PpDFN1 displays antifungal activity through specific interactions with the membrane lipids. Plant Pathol. 62, 393-403. doi: 10.1111/j.1365-3059.2012.02648.x
106. Nasrollahi, S. A., Taghibiglou, C., Azizi, E., and Farboud, E. S. (2012). Cell-penetrating peptides as a novel transdermal drug delivery system. Chem. Biol. Drug Des. 80, 639-646. doi: 10.1111/cbdd.12008
107. Ng, T. B., and Ngai, P. H. K. (2004). The trypsin-inhibitory, immunostimulatory and antiproliferative activities of a napin-like polypeptide from Chinese cabbage seeds. J. Pept. Sci. 10, 103-108. doi: 10.1002/psc.516
108. Ngai, P. H., and Ng, T. B. (2004). A napin-like polypeptide from dwarf Chinese white cabbage seeds with translation-inhibitory, trypsin-inhibitory, and antibacterial activities. Peptides 25, 171-176. doi: 10.1016/j.peptides.2003.12.012
109. Ngai, T. H., and Ng, T. B. (2003). Isolation of a napin-like polypeptide with potent translation-inhibitory activity from Chinese cabbage (Brassica parachinensis cv green-stalked) seeds. J. Pept. Sci. 9, 442-449. doi: 10.1002/psc.460
110. Nguyen, L. T., Haney, E. F., and Vogel, H. J. (2011). The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29, 464-472. doi: 10.1016/j.tibtech.2011.05.001
111. Pálffy, R., Gardlík, R., Behuliak, M., Kadasi, L., Turna, J., and Celec, P. (2009). On the physiology and pathophysiology of antimicrobial peptides. Mol. Med. 15, 51-59. doi: 10.2119/molmed.2008.00087
112. Parachin, N. S., and Franco, O. L. (2014). New edge of antibiotic development: antimicrobial peptides and corresponding resistance. Front. Microbiol. 5:147. doi: 10.3389/fmicb.2014.00147
113. Pawlowska, A. M., Camangi, F., Bader, A., and Braca, A. (2009). Flavonoids of Zizyphus jujuba L. and Zizyphus spina-christi (L.) Willd (Rhamnaceae) fruits. Food Chem. 112, 858-862. doi: 10.1016/j.foodchem.2008.06.053
114. Pelegrini, P. B., and Franco, O. L. (2005). Plant gamma-thionins: novel insights on the mechanism of action of amulti-functional class of defense proteins. Int. J. Biochem. Cell Biol. 37, 2239-2253. doi: 10.1016/j.biocel.2005.06.011
115. Pelegrini, P. B., Murad, A. M., Silva, L. P., dos Santos, R. C. P., Costa, F. T., Tagliari, P. D., et al. (2008). Identification of a novel storage glycine-rich peptide from guava (Psidium guajava) seeds with activity against Gram-negative bacteria. Peptides 29, 1271-1279. doi: 10.1016/j.peptides.2008.03.013
116. Pelegrini, P. B., Noronha, E. F., Muniz, M. A., Vasconcelos, I. M., Chiarello, M. D., and Oliveira, J. T. (2006). An antifungal peptide from passion fruit (Passiflora edulis) seeds with similarities to 2S albumin proteins. Biochim. Biophys. Acta 1764, 1141-1146. doi: 10.1016/j.bbapap.2006.04.010
117. Peng, C., Dong, C., Hou, Q., Xu, C., and Zhao, J. (2005). The hydrophobic surface of PaAMP from pokeweed seeds is essential to its interaction with fungal membrane lipids and the antifungal activity. FEBS Lett. 579, 2445-2450. doi: 10.1016/j.febslet.2005.03.046
118. Perron, G. G., Zasloff, M., and Bell, G. (2006). Experimental evolution of resistance to an antimicrobial peptide. Proc. Biol. Sci. 273, 251-256. doi: 10.1098/rspb.2005.3301
119. Podschun, R., and Ullmann, U. (1998). Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 11, 589-603. doi: 10.1128/AEM.67.7.3325-3327.2001
120. Ribeiro, S. F., Carvalho, A. O., Da Cunha, M., Rodrigues, R., Cruz, L. P., Melo, V. M., et al. (2007). Isolation and characterization of novel peptides from chilli pepper seeds: antimicrobial activities against pathogenic yeasts. Toxicon 50, 600-611. doi: 10.1016/j.toxicon.2007.05.005
121. Ribeiro, S. M., Almeida, R. G., Pereira, C. A., Moreira, J. S., Pinto, M. F., and Oliveira, A. C. (2011). Identification of a Passiflora alata Curtis dimeric peptide showing identity with 2S albumins. Peptides 32, 868-874. doi: 10.1016/j.peptides.2010.10.011
122. Rotem, S., and Mor, A. (2009). Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta 1788, 1582-1592. doi: 10.1016/j.bbamem.2008.10.020
123. Salminen, T. A., Blomqvist, K., and Edqvist, J. (2016). Lipid transfer proteins: classification, nomenclature, structure, and function. Rev. Plant. 244, 971-997. doi: 10.1007/s00425-016-2585-4
124. Santana, M. J., de Oliveira, A. L., Queiroz Júnior, L. H., Mandal, S. M., Matos, C. O., Dias, R. de. O., et al. (2015). Structural insights into Cn-AMP1, a short disulfide-free multifunctional peptide from green coconut water. FEBS Lett. 589, 639-644. doi: 10.1016/j.febslet.2015.01.029
125. Selitrennikoff, C. P. (2001). Antifungal proteins. Appl. Environ. Microbiol. 67, 2883-2894. doi: 10.1128/AEM.67.7.2883-2894.2001
126. Seo, H.-H, Park, S., Park, S., Oh, B.-J, Back, K., Han, O., et al. (2014). Overexpression of a defensin enhances resistance to a fruit-specific anthracnose fungus in pepper. PLoS ONE 9:e97936. doi: 10.1371/journal.pone.0097936
127. Seo, M. D., Won, H. S., Kim, J. H., Mishig-Ochir, T., and Lee, B. J. (2012). Antimicrobial peptides for therapeutic applications: a review. Molecules 17, 12276-12286. doi: 10.3390/molecules171012276
128. Shewry, P. R., Napier, J. A., and Tatham, A. S. (1995). Seed storage proteins: structures and biosynthesis. Plant Cell 7, 945-956.
129. Silva, O. N., Porto, W. F., Migliolo, L., Mandal, S. M., Gomes, D. G., Holanda, H. H., et al. (2012). Cn-AMP1: a new promiscuous peptide with potential for microbial infections treatment. Biopolymers 98, 322-331. doi: 10.1002/bip.22071
130. Silva, P. M., Gonçalves, S., and Santos, N. C. (2014). Defensins: antifungal lessons from eukaryotes. Front. Microbiol. 5:97. doi: 10.3389/fmicb.2014.00097
131. Skinner, M., and Hunter, D. (2013). Bioactives in Fruit: Health Benefits and Functional Foods. Oxford: Wiley-Blackwell, 542.
132. Spelbrink, R. G., Dilmac, N., Allen, A., Smith, T. J., Shah, D. M., and Hockerman, G. H. (2004). Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiol. 135, 2055-2067. doi: 10.1104/pp.104.040873
133. Stotz, H. U., Thomson, J. G., and Wang, Y. (2009). Plant defensins defense, development and application. Plant Signal. Behav. 11, 1010-1012. doi: 10.4161/psb.4.11.9755
134. Strandberg, K. L., Richards, S. M., Tamayo, R., Reeves, L. T., and Gunn, J. S. (2012). An altered immune response, but not individual cationic antimicrobial peptides, is associated with the oral attenuation of Ara4N-deficient Salmonella enterica serovar typhimurium in mice. PLoS ONE 7:e49588. doi: 10.1371/journal.pone.0049588
135. Sun, X., Chen, S., Li, S., Yan, H., Fan, Y., and Mi, H. (2005). Deletion of two C-terminal Gln residues of 12-26-residue fragment of melittin improves its antimicrobial activity. Peptides 26, 369-375. doi: 10.1016/j.peptides.2004.10.004
136. Tajkarimi, M., Ibrahim, S., and Cliver, D. (2010). Antimicrobial herb and spice compounds in food. Food Control 21, 1199-1218. doi: 10.1016/j.foodcont.2010.02.003
137. Takayama, S., Shimosato, H., Shiba, H., Funato, M., Che, F. S., Watanabe, M., et al. (2001). Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534-538. doi: 10.1038/35097104
138. Tanaka, K. (2001). P-I3-kinase p85 is a target molecule of proline-rich antimicrobial peptide to suppress proliferation of ras-transformed cells. Jpn. J. Cancer Res. 92, 959-967. doi: 10.1111/j.1349-7006.2001.tb01187.x
139. Taveira, G. B., Carvalho, A. O., Rodrigues, R., Trindade, F. G., Da Cunha, M., and Gomes, V. M. (2016). Thionin-like peptide from Capsicum annuum fruits: mechanism of action and synergism with fluconazole against Candida species. BMC Microbiol. 16:12. doi: 10.1186/s12866-016-0626-6
140. Taveira, G. B., Mathias, L. S., da Motta, O. V., Machado, O. L. T., Rodrigues, R., Carvalho, A. O., et al. (2014). Thionin-like peptides from Capsicum annuum fruits with high activity against human pathogenic bacteria and yeasts. Biopolymers 102, 30-39. doi: 10.1002/bip.22351
141. Terras, F. R., Eggermont, K., Kovaleva, V., Raikhel, N. V., Osborn, R. W, Kester, A., et al. (1995). Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7, 573-588. doi: 10.1105/tpc.7.5.573
142. Terras, F. R., Schoofs, H. M., De Bolle, M. F., Van Leuven, F., Rees, S. B., Vanderleyden, J., et al. (1992). Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267, 15301-15309.
143. Thevissen, K., Terras, F. R. G., and Broekaert, W. F. (1999). Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl. Environ. Microbiol. 65, 5451-5458.
144. Thomma, B. P., Cammue, B. P., and Thevissen, K. (2002). Plant defensins. Planta 216, 193-202. doi: 10.1007/s00425-002-0902-6
145. Tran, A. X., Whittimore, J. D., Wyrick, P. B., Mcgrath, S. C., Cotter, R. J., and Trent, M. S. (2006). The lipid A 1-phosphatase of Helicobacter pylori is required for resistance to the antimicrobial peptide polymyxin. J. Bacteriol. 188, 4531-4541. doi: 10.1128/JB.00146-06
146. Tran, D., Tran, P. A., Tang, Y.-Q., Yuan, J., Cole, T., and Selsted, M. E. (2002). Homodimeric u-defensins from rhesus macaque leukocytes. J. Biol. Chem. 277, 3079-3084. doi: 10.1074/jbc.M109117200
147. Uhliga, T., Kyprianoua, T., Martinellia, F. G., Oppicia, C. A., Heiligersa, D., Hillsa, D., et al. (2014). The emergence of peptides in the pharmaceutical business: from exploration to exploitation. EuPA Open Proteomics 4, 58-69. doi: 10.1016/j.euprot.2014.05.003
148. Vashishta, A., Sahu, T., Sharma, A., Choudhary, S. K., and Dixit, A. (2006). In vitro refolded napin-like protein of Momordica charantia expressed in Escherichia coli displays properties of native napin. Biochim. Biophys. Acta 1764, 847-855. doi: 10.1016/j.bbapap.2006.03.010
149. Wang, G. (2015). Improved methods for classification, prediction, and design of antimicrobial peptides. Methods Mol. Biol. 1268, 43-66. doi: 10.1007/978-1-4939-2285-7_3
150. Wang, G., Li, X., and Wang, Z. (2016). APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 44, D1087-D1093. doi: 10.1093/nar/gkv1278
151. Wang, H. X., and Ng, T. B. (2005). An antifungal peptide from the coconut. Peptides 26, 2392-2396. doi: 10.1016/j.peptides.2005.05.009
152. Welling, M. M., Paulusma-Annema, A., Balter, H. S., Pauwels, E. K., and And Nibbering, P. H. (2000). Tenehtium-99m labeled antimicrobial peptide discriminate between bacterial infection and sterile inflammations. Eur. J. Nucl. Med. 27, 292-301. doi: 10.1007/s002590050036
153. Wijaya, R., Neumann, G. M., Condron, R., Hughes, A. B., and Polya, G. M. (2000). Defense proteins from seed of Cassia fistula include a lipid transfer protein homologue and a protease inhibitory plant defensin. Plant Sci. 159, 243-255. doi: 10.1016/S0168-9452(00)00348-4
154. Wisniewski, M. E., Bassett, C. L., Artlip, T. S., Webb, R. P., Janisiewicz, W. J., Norelli, J. L., et al. (2003). Characterization of a defensin in bark and fruit tissues of peach and antimicrobial activity of a recombinant defensin in the yeast, Pichia pastoris. Physiol. Plant. 119, 563-572. doi: 10.1046/j.1399-3054.2003.00204.x
155. Won, J., Kim, J., Choi, D. H., Han, M. W., Lee, D.-H., Kang, S. C., et al. (2016). Effects of compounds isolated from a Litsea japonica fruit extract on the TNF-a signaling pathway and cell viability. Mol. Céll. Toxicol. 12, 37-44. doi: 10.1007/s13273-016-0006-1
156. Wong, R. W., Hägg, U., Samaranayake, L., Yuen, M. K., Seneviratne, C. J., and Kao, R. (2010). Antimicrobial activity of Chinese medicine herbs against common bacteria in oral biofilm. A pilot study. Int. J. Oral Maxillofac. Surg. 39, 599-605. doi: 10.1016/j.ijom.2010.02.024
157. Yang, X., Xiao, Y., Wang, X., and Pei, Y. (2007). Expression of a novel small antimicrobial protein from the seeds of motherwort (Leonurus japonicus) confers disease resistance in tobacco. Appl. Environ. Microbiol. 73, 939-946. doi: 10.1128/AEM.02016-06
158. Yazdi, M. M., Mahaki, H., and Zardini, H. Z. (2013). Antioxidant activity of protein hydrolysates and purified peptides from Zizyphus jujuba fruits, J. Funct. Foods 5, 62-70. doi: 10.1016/j.jff.2012.08.00410.1016
159. Yeaman, M. R., and Yount, N. Y. (2003). Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55. doi: 10.1124/pr.55.1.2
160. Youle, R., and Huang, A. H. C. (1981). Occurrence of low molecular weight and high cysteine containing albumin storage protein in oilseeds of diverse species Am. J. Bot. 68, 44-48.
161. Zainal, Z., Marouf, E., Ismail, I., and Fei, C. K. (2009). Expression of the Capsicuum annum (chili) defensin gene in transgenic tomatoes confers enhanced resistance to fungal pathogens. Am. J. Plant Physiol. 4, 70-79. doi: 10.3923/ajpp.2009.70.79
162. Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389-395. doi: 10.1038/415389a
163. Zavascki, A. P., Goldani, L. Z., Li, J., and Nation, R. L. (2007). Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J. Antimicrob. Chemother. 60, 1206-1215. doi: 10.1093/jac/dkm357
164. Zhu, S., Gao, B., and Tytgat, J. (2005). Phylogenetic distribution, functional epitopes and evolution of the CSab superfamily. Cell Mol. Life Sci. 62, 2257-2269. doi: 10.1007/s00018-005-5200-6
165. Zhu, Y. J., Agbayani, R., and Moore, P. H. (2007). Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor. Planta 226, 87-97. doi: 10.1007/s00425-006-0471-1
166. Zottich, U., Da Cunha, M., Carvalho, A. O., Dias, G. B., Casarin, N., and Vasconcelos, I. M. (2013). An antifungal peptide from Coffea canephora seeds with sequence homology to glycine-rich proteins exerts membrane permeabilization and nuclear localization in fungi. Biochim. Biophys. Acta 1830, 3509-3516. doi: 10.1016/j.bbagen.2013.03.007
167. Zottich, U., Da Cunha, M., Carvalho, A. O., Dias, G. B., Silva, N. C., Santos, I. S., et al. (2011). Purification, biochemical characterization and antifungal activity of a new lipid transfer protein (LTP) from Coffea canephora seeds with α-amylase inhibitor properties. Biochim. Biophys. Acta 4, 375-383. doi: 10.1016/j.bbagen.2010.12.002