Antimicrobial Peptides - Small but Mighty Weapons for Plants to Fight Phytopathogens

Author(s): Kaushik Das, Karabi Datta, Subhasis Karmakar, Swapan K. Datta*

Journal Name: Protein & Peptide Letters

Volume 26 , Issue 10 , 2019

Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Antimicrobial Peptides (AMPs) have diverse structures, varied modes of actions, and can inhibit the growth of a wide range of pathogens at low concentrations. Plants are constantly under attack by a wide range of phytopathogens causing massive yield losses worldwide. To combat these pathogens, nature has armed plants with a battery of defense responses including Antimicrobial Peptides (AMPs). These peptides form a vital component of the two-tier plant defense system. They are constitutively expressed as part of the pre-existing first line of defense against pathogen entry. When a pathogen overcomes this barrier, it faces the inducible defense system, which responds to specific molecular or effector patterns by launching an arsenal of defense responses including the production of AMPs. This review emphasizes the structural and functional aspects of different plant-derived AMPs, their homology with AMPs from other organisms, and how their biotechnological potential could generate durable resistance in a wide range of crops against different classes of phytopathogens in an environmentally friendly way without phenotypic cost.

Keywords: Antibacterial, antifungal, antimicrobial peptides, disease resistance, plant biotechnology, transgenic plants.

Gibson, D.M.; King, B.C.; Hayes, M.L.; Bergstrom, G.C. Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr. Opin. Microbiol., 2011, 14(3), 264-270.
[] [PMID: 21536481]
Benali, S.; Mohamed, B.; Eddine, H.J. Virulence strategies of phytopathogenic bacteria and their role in plant disease pathogenesis. Afr. J. Microbiol. Res., 2014, 8(30), 2809-2815.
Ma, K.W.; Ma, W. Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol. Biol., 2016, 91(6), 713-725.
[] [PMID: 26879412]
Jones, J.D.; Dangl, J.L. The plant immune system. Nature, 2006, 444(7117), 323-329.
[] [PMID: 17108957]
Künstler, A.; Bacsó, R.; Hafez, Y.M.; Király, L. Reactive oxygen species and plant disease resistance.In: Reactive Oxygen Species and Oxidative Damage in Plants Under Stress; Gupta, D.K.; Palma, J.M.; Corpas, F.J., Eds.; Springer: Switzerland, 2015, pp. 269-303.
Ahuja, I.; Kissen, R.; Bones, A.M. Phytoalexins in defense against pathogens. Trends Plant Sci., 2012, 17(2), 73-90.
[] [PMID: 22209038]
Künstler, A.; Bacsó, R.; Gullner, G.; Hafez, Y.M.; Király, L. Staying alive is cell death dispensable for plant disease resistance during the hypersensitive response? Physiol. Mol. Plant Pathol., 2016, 93, 75-84.
Dixon, R.A.; Harrison, M.J. Activation, structure, and organization of genes involved in microbial defense in plants. Adv. Genet., 1990, 28, 165-234.
[] [PMID: 2239449]
Aktar, M.W.; Sengupta, D.; Chowdhury, A. Impact of pesticides use in agriculture: Their benefits and hazards. Interdiscip. Toxicol., 2009, 2(1), 1-12.
[] [PMID: 21217838]
de Souza Cândido, E.; Silva Cardoso, M.H.; Sousa, D.A.; Viana, J.C.; de Oliveira-Júnior, N.G.; Miranda, V.; Franco, O.L. The use of versatile plant antimicrobial peptides in agribusiness and human health. Peptides, 2014, 55, 65-78.
[] [PMID: 24548568]
Tam, J.P.; Wang, S.; Wong, K.H.; Tan, W.L. Antimicrobial peptides from plants. Pharmaceuticals (Basel), 2015, 8(4), 711-757.
[] [PMID: 26580629]
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415(6870), 389-395.
[] [PMID: 11807545]
Hammami, R.; Ben Hamida, J.; Vergoten, G.; Fliss, I. PhytAMP: A database dedicated to antimicrobial plant peptides. Nucleic Acids Res., 2009, 37(Database issue)(Suppl. 1), D963-D968.
[] [PMID: 18836196]
Waghu, F.H.; Gopi, L.; Barai, R.S.; Ramteke, P.; Nizami, B.; Idicula-Thomas, S. CAMP: collection of sequences and structures of antimicrobial peptides. Nucleic Acids Res., 2014, 42(Database issue), D1154-D1158.
[] [PMID: 24265220]
Wang, G.; Li, X.; Wang, Z. APD3: The antimicrobial peptide database as a tool for research and education. Nucleic Acids Res., 2015.
[] [PMID: 26602694]
Zhao, X.; Wu, H.; Lu, H.; Li, G.; Huang, Q. LAMP: A database linking antimicrobial peptides. PLoS One, 2013, 8(6)e66557
[] [PMID: 23825543]
Seshadri Sundararajan, V.; Gabere, M.N.; Pretorius, A.; Adam, S.; Christoffels, A.; Lehväslaiho, M.; Archer, J.A.; Bajic, V.B. DAMPD: A manually curated antimicrobial peptide database. Nucleic Acids Res., 2012, 40(Database issue), D1108-D1112.
[] [PMID: 22110032]
Li, Y.; Chen, Z. RAPD: a database of recombinantly-produced antimicrobial peptides. FEMS Microbiol. Lett., 2008, 289(2), 126-129.
[] [PMID: 19054102]
Fan, L.; Sun, J.; Zhou, M.; Zhou, J.; Lao, X.; Zheng, H.; Xu, H. DRAMP: a comprehensive data repository of antimicrobial peptides. Sci. Rep., 2016, 6, 24482.
[] [PMID: 27075512]
Seebah, S.; Suresh, A.; Zhuo, S.; Choong, Y. H.; Chua, H.; Chuon, D.; Beuerman, R.; Verma, C. Defensins knowledgebase: A manually curated database and information source focused on the defensins family of antimicrobial peptides., Nucleic Acids Res. 2006, 35(suppl_1), D265-D268.,
Piotto, S.P.; Sessa, L.; Concilio, S.; Iannelli, P. YADAMP: Yet another database of antimicrobial peptides. Int. J. Antimicrob. Agents, 2012, 39(4), 346-351.
[] [PMID: 22325123]
Pirtskhalava, M.; Gabrielian, A.; Cruz, P.; Griggs, H.L.; Squires, R.B.; Hurt, D.E.; Grigolava, M.; Chubinidze, M.; Gogoladze, G.; Vishnepolsky, B.; Alekseev, V. DBAASP v. 2: an enhanced database of structure and antimicrobial/cytotoxic activity of natural and synthetic peptides. Nucleic Acids Res., 2016, 44(D1), D1104-D1112.
[] [PMID: 26578581]
Bahar, A.A.; Ren, D. Antimicrobial peptides. Pharmaceuticals (Basel), 2013, 6(12), 1543-1575.
[] [PMID: 24287494]
Koo, J.C.; Lee, B.; Young, M.E.; Koo, S.C.; Cooper, J.A.; Baek, D.; Lim, C.O.; Lee, S.Y.; Yun, D.J.; Cho, M.J. Pn-AMP1, a plant defense protein, induces actin depolarization in yeasts. Plant Cell Physiol., 2004, 45(11), 1669-1680.
[] [PMID: 15574843]
Fujimura, M.; Ideguchi, M.; Minami, Y.; Watanabe, K.; Tadera, K. Amino acid sequence and antimicrobial activity of chitin-binding peptides, Pp-AMP 1 and Pp-AMP 2, from Japanese bamboo shoots (Phyllostachys pubescens). Biosci. Biotechnol. Biochem., 2005, 69(3), 642-645.
[] [PMID: 15784998]
Hwang, B.; Hwang, J.S.; Lee, J.; Lee, D.G. The antimicrobial peptide, psacotheasin induces reactive oxygen species and triggers apoptosis in Candida albicans. Biochem. Biophys. Res. Commun., 2011, 405(2), 267-271.
[] [PMID: 21219857]
Lobo, D.S.; Pereira, I.B.; Fragel-Madeira, L.; Medeiros, L.N.; Cabral, L.M.; Faria, J.; Bellio, M.; Campos, R.C.; Linden, R.; Kurtenbach, E. Antifungal Pisum sativum defensin 1 interacts with Neurospora crassa cyclin F related to the cell cycle. Biochemistry, 2007, 46(4), 987-996.
[] [PMID: 17240982]
van der Weerden, N.L.; Lay, F.T.; Anderson, M.A. The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J. Biol. Chem., 2008, 283(21), 14445-14452.
[] [PMID: 18339623]
Haney, E.F.; Petersen, A.P.; Lau, C.K.; Jing, W.; Storey, D.G.; Vogel, H.J. Mechanism of action of puroindoline derived tryptophan-rich antimicrobial peptides. Biochim. Biophys. Acta, 2013, 1828(8), 1802-1813.
[] [PMID: 23562406]
Nanni, V.; Schumacher, J.; Giacomelli, L.; Brazzale, D.; Sbolci, L.; Moser, C.; Tudzynski, P.; Baraldi, E. VvAMP2, a grapevine flower-specific defensin capable of inhibiting Botrytis cinerea growth: insights into its mode of action. Plant Pathol., 2014, 63(4), 899-910.
Silverstein, K.A.; Moskal, W.A. Jr.; Wu, H.C.; Underwood, B.A.; Graham, M.A.; Town, C.D.; VandenBosch, K.A. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J., 2007, 51(2), 262-280.
[] [PMID: 17565583]
García-Olmedo, F.; Molina, A.; Alamillo, J.M.; Rodríguez-Palenzuéla, P. Plant defense peptides. Biopolymers, 1998, 47(6), 479-491.
[<479:AID-BIP6>3.0.CO;2-K] [PMID: 10333739]
Odintsova, T.; Egorov, T. Plant antimicrobial peptides; Plant Signaling Peptides, 2012, pp. 107-133.
Rahnamaeian, M. Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signal. Behav., 2011, 6(9), 1325-1332.
[] [PMID: 21847025]
Epple, P.; Apel, K.; Bohlmann, H. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol., 1995, 109(3), 813-820.
[] [PMID: 8552715]
Vignutelli, A.; Wasternack, C.; Apel, K.; Bohlmann, H. Systemic and local induction of an Arabidopsis thionin gene by wounding and pathogens. Plant J., 1998, 14(3), 285-295.
[] [PMID: 9628023]
Penninckx, I.A.; Eggermont, K.; Terras, F.R.; Thomma, B.P.; De Samblanx, G.W.; Buchala, A.; Métraux, J.P.; Manners, J.M.; Broekaert, W.F. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell, 1996, 8(12), 2309-2323.
[] [PMID: 8989885]
Penninckx, I.A.; Thomma, B.P.; Buchala, A.; Métraux, J.P.; Broekaert, W.F. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell, 1998, 10(12), 2103-2113.
[] [PMID: 9836748]
Pervieux, I.; Bourassa, M.; Laurans, F.; Hamelin, R.; Séguin, A.J.P.; Pathology, M.P. A spruce defensin showing strong antifungal activity and increased transcript accumulation after wounding and jasmonate treatments. Physiol. Mol. Plant Pathol., 2004, 64(6), 331-341.
Jung, H.W.; Kim, W.; Hwang, B.K. Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ., 2003, 26(6), 915-928.
[] [PMID: 12803619]
Jung, H.W.; Lim, C.W.; Hwang, B.K. Isolation and functional analysis of a pepper lipid transfer protein III (CALTPIII) gene promoter during signaling to pathogen, abiotic and environmental stresses. Plant Sci., 2006, 170(2), 258-266.
Almasia, N.I.; Narhirñak, V.; Hopp, H.E.; Vazquez-Rovere, C. Isolation and characterization of the tissue and development-specific potato snakin-1 promoter inducible by temperature and wounding. Electron. J. Biotechnol., 2010, 13(5), 8-9.
Berrocal-Lobo, M.; Segura, A.; Moreno, M.; López, G.; García-Olmedo, F.; Molina, A. Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol., 2002, 128(3), 951-961.
[] [PMID: 11891250]
Stec, B. Plant thionins--the structural perspective. Cell. Mol. Life Sci., 2006, 63(12), 1370-1385.
[] [PMID: 16715411]
Tam, J.P.; Wang, S.; Wong, K.H.; Tan, W.L. Antimicrobial peptides from plants. Pharmaceuticals (Basel), 2015, 8(4), 711-757.
[] [PMID: 26580629]
Bohlmann, H.; Apel, K. Thionins. Annu. Rev. Plant Biol., 1991, 42(1), 227-240.
Egorov, T.A.; Odintsova, T.I.; Pukhalsky, V.A.; Grishin, E.V. Diversity of wheat anti-microbial peptides. Peptides, 2005, 26(11), 2064-2073.
[] [PMID: 16269343]
Vernon, L.P. Pyrularia thionin: Physical properties, biological responses and comparison to other thionins and cardiotoxin. J. Toxicol. Toxin Rev., 1992, 11(3), 169-191.
Bohlmann, H.; Clausen, S.; Behnke, S.; Giese, H.; Hiller, C.; Reimann-Philipp, U.; Schrader, G.; Barkholt, V.; Apel, K. Leaf-specific thionins of barley-a novel class of cell wall proteins toxic to plant-pathogenic fungi and possibly involved in the defence mechanism of plants. EMBO J., 1988, 7(6), 1559-1565.
[] [PMID: 16453847]
Mellstrand, S.T.; Samuelsson, G. Phoratoxin, a toxic protein from the mistletoe Phoradendron tomentosum subsp. macrophyllum (Loranthaceae). Improvements in the isolation procedure and further studies on the properties. Eur. J. Biochem., 1973, 32(1), 143-147.
[] [PMID: 4687388]
Samuelsson, G.; Pettersson, B. Separation of viscotoxins from the European mistletoe, Viscum album L. (Loranthaceae) by chromatography on sulfoethyl Sephadex. Acta Chem. Scand., 1970, 24(8), 2751-2756.
[] [PMID: 5507482]
Schrader-Fischer, G.; Apel, K. Organ-specific expression of highly divergent thionin variants that are distinct from the seed-specific crambin in the crucifer Crambe abyssinica. Mol. Gen. Genet., 1994, 245(3), 380-389.
[] [PMID: 7816048]
Castagnaro, A.; Maraña, C.; Carbonero, P.; García-Olmedo, F. cDNA cloning and nucleotide sequences of alpha 1 and alpha 2 thionins from hexaploid wheat endosperm. Plant Physiol., 1994, 106(3), 1221-1222.
[] [PMID: 7824649]
Fernandez de Caleya, R.; Gonzalez-Pascual, B.; García-Olmedo, F.; Carbonero, P. Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro. Appl. Microbiol., 1972, 23(5), 998-1000.
[PMID: 5031563]
Giudici, A.M.; Regente, M.C.; Villalaín, J.; Pfüller, K.; Pfüller, U.; De La Canal, L. Mistletoe viscotoxins induce membrane permeabilization and spore death in phytopathogenic fungi. Physiol. Plant., 2004, 121(1), 2-7.
[] [PMID: 15086811]
Hughes, P.; Dennis, E.; Whitecross, M.; Llewellyn, D.; Gage, P. The cytotoxic plant protein, β-purothionin, forms ion channels in lipid membranes. J. Biol. Chem., 2000, 275(2), 823-827.
[] [PMID: 10625613]
Evans, J.; Wang, Y.D.; Shaw, K.P.; Vernon, L.P. Cellular responses to Pyrularia thionin are mediated by Ca2+ influx and phospholipase A2 activation and are inhibited by thionin tyrosine iodination. Proc. Natl. Acad. Sci. USA, 1989, 86(15), 5849-5853.
[] [PMID: 2503825]
Carmona, M.J.; Molina, A.; Fernández, J.A.; López-Fando, J.J.; García-Olmedo, F. Expression of the α-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens. Plant J., 1993, 3(3), 457-462.
[] [PMID: 8220454]
Epple, P.; Apel, K.; Bohlmann, H. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell, 1997, 9(4), 509-520.
[] [PMID: 9144959]
Holtorf, S.; Ludwig-Müller, J.; Apel, K.; Bohlmann, H. High-level expression of a viscotoxin in Arabidopsis thaliana gives enhanced resistance against Plasmodiophora brassicae. Plant Mol. Biol., 1998, 36(5), 673-680.
[] [PMID: 9526499]
Iwai, T.; Kaku, H.; Honkura, R.; Nakamura, S.; Ochiai, H.; Sasaki, T.; Ohashi, Y. Enhanced resistance to seed-transmitted bacterial diseases in transgenic rice plants overproducing an oat cell-wall-bound thionin. Mol. Plant Microbe Interact., 2002, 15(6), 515-521.
[] [PMID: 12059099]
Chan, Y.L.; Prasad, V. Sanjaya, Chen, K.H.; Liu, P.C.; Chan, M.T.; Cheng, C.P. Transgenic tomato plants expressing an Arabidopsis thionin (Thi2.1) driven by fruit-inactive promoter battle against phytopathogenic attack. Planta, 2005, 221(3), 386-393.
[] [PMID: 15657715]
Charity, J.A.; Hughes, P.; Anderson, M.A.; Bittisnich, D.J.; Whitecross, M.; Higgins, T. Pest and disease protection conferred by expression of barley β–hordothionin and Nicotiana alata proteinase inhibitor genes in transgenic tobacco. Funct. Plant Biol., 2005, 32(1), 35-44.
Oard, S.V.; Enright, F.M. Expression of the antimicrobial peptides in plants to control phytopathogenic bacteria and fungi. Plant Cell Rep., 2006, 25(6), 561-572.
[] [PMID: 16456649]
Krens, F.A.; Schaart, J.G.; Groenwold, R.; Walraven, A.E.J.; Hesselink, T.; Thissen, J.T. Performance and long-term stability of the barley hordothionin gene in multiple transgenic apple lines. Transgenic Res., 2011, 20(5), 1113-1123.
[] [PMID: 21243525]
Hoshikawa, K.; Ishihara, G.; Takahashi, H.; Nakamura, I. Enhanced resistance to gray mold (Botrytis cinerea) in transgenic potato plants expressing thionin genes isolated from Brassicaceae species. Plant Biotechnol., 2012, 29(1), 87-93.
Muramoto, N.; Tanaka, T.; Shimamura, T.; Mitsukawa, N.; Hori, E.; Koda, K.; Otani, M.; Hirai, M.; Nakamura, K.; Imaeda, T. Transgenic sweet potato expressing thionin from barley gives resistance to black rot disease caused by Ceratocystis fimbriata in leaves and storage roots. Plant Cell Rep., 2012, 31(6), 987-997.
[] [PMID: 22212462]
Bruix, M.; Jiménez, M.A.; Santoro, J.; González, C.; Colilla, F.J.; Méndez, E.; Rico, M. 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, 1993, 32(2), 715-724.
[] [PMID: 8380707]
Thomma, B.P.; Cammue, B.P.; Thevissen, K. Plant defensins. Planta, 2002, 216(2), 193-202.
[] [PMID: 12447532]
Cornet, B.; Bonmatin, J.M.; Hetru, C.; Hoffmann, J.A.; Ptak, M.; Vovelle, F. Refined three-dimensional solution structure of insect defensin A. Structure, 1995, 3(5), 435-448.
[] [PMID: 7663941]
Lacerda, A.F.; Vasconcelos, É.A.R.; Pelegrini, P.B.; Grossi de Sa, M.F. Antifungal defensins and their role in plant defense. Front. Microbiol., 2014, 5, 116.
[] [PMID: 24765086]
Lay, F.T.; Anderson, M.A. Defensins--components of the innate immune system in plants. Curr. Protein Pept. Sci., 2005, 6(1), 85-101.
[] [PMID: 15638771]
Stotz, H.U.; Thomson, J.G.; Wang, Y. Plant defensins: defense, development and application. Plant Signal. Behav., 2009, 4(11), 1010-1012.
[] [PMID: 20009545]
Thevissen, K.; François, I.E.; Takemoto, J.Y.; Ferket, K.K.; Meert, E.M.; Cammue, B.P. DmAMP1, an antifungal plant defensin from dahlia (Dahlia merckii), interacts with sphingolipids from Saccharomyces cerevisiae. FEMS Microbiol. Lett., 2003, 226(1), 169-173.
[] [PMID: 13129623]
Pelegrini, P.B.; Franco, O.L. Plant γ-thionins: novel insights on the mechanism of action of a multi-functional class of defense proteins. Int. J. Biochem. Cell Biol., 2005, 37(11), 2239-2253.
[] [PMID: 16084753]
Broekaert, W.F.; Terras, F.R.; Cammue, B.P.; Osborn, R.W. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol., 1995, 108(4), 1353-1358.
[] [PMID: 7659744]
Terras, F.R.; Schoofs, H.M.; De Bolle, M.F.; Van Leuven, F.; Rees, S.B.; Vanderleyden, J.; Cammue, B.P.; Broekaert, W.F. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem., 1992, 267(22), 15301-15309.
[PMID: 1639777]
Aerts, A.M.; François, I.E.; Meert, E.M.; Li, Q.T.; Cammue, B.P.; Thevissen, K. The antifungal activity of RsAFP2, a plant defensin from Raphanus sativus, involves the induction of reactive oxygen species in Candida albicans. J. Mol. Microbiol. Biotechnol., 2007, 13(4), 243-247.
[] [PMID: 17827975]
Aerts, A.M.; Carmona-Gutierrez, D.; Lefevre, S.; Govaert, G.; François, I.E.; Madeo, F.; Santos, R.; Cammue, B.P.; Thevissen, K. The antifungal plant defensin RsAFP2 from radish induces apoptosis in a metacaspase independent way in Candida albicans. FEBS Lett., 2009, 583(15), 2513-2516.
[] [PMID: 19596007]
Thevissen, K.; de Mello Tavares, P.; Xu, D.; Blankenship, J.; Vandenbosch, D.; Idkowiak-Baldys, J.; Govaert, G.; Bink, A.; Rozental, S.; de Groot, P.W.; Davis, T.R.; Kumamoto, C.A.; Vargas, G.; Nimrichter, L.; Coenye, T.; Mitchell, A.; Roemer, T.; Hannun, Y.A.; Cammue, B.P. The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans. Mol. Microbiol., 2012, 84(1), 166-180.
[] [PMID: 22384976]
Osborn, R.W.; De Samblanx, G.W.; Thevissen, K.; Goderis, I.; Torrekens, S.; Van Leuven, F.; Attenborough, S.; Rees, S.B.; Broekaert, W.F. Isolation and characterisation of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae. FEBS Lett., 1995, 368(2), 257-262.
[] [PMID: 7628617]
Thevissen, K.; Ghazi, A.; De Samblanx, G.W.; Brownlee, C.; Osborn, R.W.; Broekaert, W.F. Fungal membrane responses induced by plant defensins and thionins. J. Biol. Chem., 1996, 271(25), 15018-15025.
[] [PMID: 8663029]
Giacomelli, L.; Nanni, V.; Lenzi, L.; Zhuang, J.; Dalla Serra, M.; Banfield, M.J.; Town, C.D.; Silverstein, K.A.; Baraldi, E.; Moser, C. Identification and characterization of the defensin-like gene family of grapevine. Mol. Plant Microbe Interact., 2012, 25(8), 1118-1131.
[] [PMID: 22550957]
Viret, O.; Keller, M.; Jaudzems, V.G.; Cole, F.M. Botrytis cinerea infection of grape flowers: Light and electron microscopical studies of infection sites. Phytopathology, 2004, 94(8), 850-857.
[] [PMID: 18943105]
Games, P.D.; Dos Santos, I.S.; Mello, É.O.; Diz, M.S.; Carvalho, A.O.; de Souza-Filho, G.A.; Da Cunha, M.; Vasconcelos, I.M. Ferreira, Bdos.S.; Gomes, V.M. Isolation, characterization and cloning of a cDNA encoding a new antifungal defensin from Phaseolus vulgaris L. seeds. Peptides, 2008, 29(12), 2090-2100.
[] [PMID: 18786582]
Mello, E.O.; Ribeiro, S.F.; Carvalho, A.O.; Santos, I.S.; Da Cunha, M.; Santa-Catarina, C.; Gomes, V.M. Antifungal activity of PvD1 defensin involves plasma membrane permeabilization, inhibition of medium acidification, and induction of ROS in fungi cells. Curr. Microbiol., 2011, 62(4), 1209-1217.
[] [PMID: 21170711]
Soares, J.R.; de Oliveira Carvalho, A.; Dos Santos, I.S.; Machado, O.L.; Nascimento, V.V.; Vasconcelos, I.M.; da Silva Ferreira, A.T.; de Aguilar Perales, J.E.; Gomes, V.M. Antimicrobial peptides from Adenanthera pavonina L. seeds: characterization and antifungal activity. Protein Pept. Lett., 2012, 19(5), 520-529.
[] [PMID: 22486647]
Soares, J.R.; José Tenório de Melo, E.; da Cunha, M.; Fernandes, K.V.S.; Taveira, G.B.; da Silva Pereira, L.; Pimenta, S.; Trindade, F.G.; Regente, M.; Pinedo, M.; de la Canal, L.; Gomes, V.M.; de Oliveira Carvalho, A. Interaction between the plant ApDef1 defensin and Saccharomyces cerevisiae results in yeast death through a cell cycle- and caspase-dependent process occurring via uncontrolled oxidative stress. Biochim. Biophys. Acta, Gen. Subj., 2017, 1861(1 Pt A), 3429-3443.
[] [PMID: 27614033]
Lay, F.T.; Brugliera, F.; Anderson, M.A. Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol., 2003, 131(3), 1283-1293.
[] [PMID: 12644678]
van der Weerden, N.L.; Hancock, R.E.; Anderson, M.A. Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J. Biol. Chem., 2010, 285(48), 37513-37520.
[] [PMID: 20861017]
Payne, J.A.; Bleackley, M.R.; Lee, T.H.; Shafee, T.M.; Poon, I.K.; Hulett, M.D.; Aguilar, M.I.; van der Weerden, N.L.; Anderson, M.A. The plant defensin NaD1 introduces membrane disorder through a specific interaction with the lipid, phosphatidylinositol 4,5 bisphosphate. Biochim. Biophys. Acta, 2016, 1858(6), 1099-1109.
[] [PMID: 26896695]
Hayes, B.M.; Bleackley, M.R.; Wiltshire, J.L.; Anderson, M.A.; Traven, A.; van der Weerden, N.L. Identification and mechanism of action of the plant defensin NaD1 as a new member of the antifungal drug arsenal against Candida albicans. Antimicrob. Agents Chemother., 2013, 57(8), 3667-3675.
[] [PMID: 23689717]
Lay, F.T.; Mills, G.D.; Poon, I.K.; Cowieson, N.P.; Kirby, N.; Baxter, A.A.; van der Weerden, N.L.; Dogovski, C.; Perugini, M.A.; Anderson, M.A.; Kvansakul, M.; Hulett, M.D. Dimerization of plant defensin NaD1 enhances its antifungal activity. J. Biol. Chem., 2012, 287(24), 19961-19972.
[] [PMID: 22511788]
Almeida, M.S.; Cabral, K.M.; Zingali, R.B.; Kurtenbach, E. Characterization of two novel defense peptides from pea (Pisum sativum) seeds. Arch. Biochem. Biophys., 2000, 378(2), 278-286.
[] [PMID: 10860545]
Vriens, K.; Cools, T.L.; Harvey, P.J.; Craik, D.J.; Spincemaille, P.; Cassiman, D.; Braem, A.; Vleugels, J.; Nibbering, P.H.; Drijfhout, J.W.; De Coninck, B.; Cammue, B.P.; Thevissen, K. Synergistic activity of the plant defensin HsAFP1 and caspofungin against Candida albicans biofilms and planktonic cultures. PLoS One, 2015, 10(8)e0132701
[] [PMID: 26248029]
Thevissen, K.; Osborn, R.W.; Acland, D.P.; Broekaert, W.F. Specific, high affinity binding sites for an antifungal plant defensin on Neurospora crassa hyphae and microsomal membranes. J. Biol. Chem., 1997, 272(51), 32176-32181.
[] [PMID: 9405418]
Cools, T.L.; Vriens, K.; Struyfs, C.; Verbandt, S.; Ramada, M.H.S.; Brand, G.D.; Bloch, C., Jr; Koch, B.; Traven, A.; Drijfhout, J.W.; Demuyser, L.; Kucharíková, S.; Van Dijck, P.; Spasic, D.; Lammertyn, J.; Cammue, B.P.A.; Thevissen, K. The antifungal plant defensin HsAFP1 is a phosphatidic acid-interacting peptide inducing membrane permeabilization. Front. Microbiol., 2017, 8, 2295.
[] [PMID: 29209301]
Aerts, A.M.; Bammens, L.; Govaert, G.; Carmona-Gutierrez, D.; Madeo, F.; Cammue, B.P.; Thevissen, K. The antifungal plant defensin HsAFP1 from Heuchera sanguinea induces apoptosis in Candida albicans. Front. Microbiol., 2011, 2, 47.
[] [PMID: 21993350]
Ramamoorthy, V.; Cahoon, E.B.; Li, J.; Thokala, M.; Minto, R.E.; Shah, D.M. Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum. Mol. Microbiol., 2007, 66(3), 771-786.
[] [PMID: 17908205]
El-Mounadi, K.; Islam, K.T.; Hernández-Ortiz, P.; Read, N.D.; Shah, D.M. Antifungal mechanisms of a plant defensin MtDef4 are not conserved between the ascomycete fungi Neurospora crassa and Fusarium graminearum. Mol. Microbiol., 2016, 100(3), 542-559.
[] [PMID: 26801962]
Terras, F.R.; Eggermont, K.; Kovaleva, V.; Raikhel, N.V.; Osborn, R.W.; Kester, A.; Rees, S.B.; Torrekens, S.; Van Leuven, F.; Vanderleyden, J. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell, 1995, 7(5), 573-588.
[] [PMID: 7780308]
Wang, Y.; Nowak, G.; Culley, D.; Hadwiger, L.A.; Fristensky, B.J. Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Mol. Plant Microbe Interact., 1999, 12(5), 410-418.
Gao, A.G.; Hakimi, S.M.; Mittanck, C.A.; Wu, Y.; Woerner, B.M.; Stark, D.M.; Shah, D.M.; Liang, J.; Rommens, C.M. Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat. Biotechnol., 2000, 18(12), 1307-1310.
[] [PMID: 11101813]
Elfstrand, M.; Fossdal, C.G.; Swedjemark, G.; Clapham, D.; Olsson, O.; Sitbon, F.; Sharma, P.; Lönneborg, A.; von Arnold, S.J. Identification of candidate genes for use in molecular breeding-A case study with the Norway spruce defensin-like gene, Spi1. Silvae Genet., 2001, 50(2), 75-81.
Park, H.C.; Kang, Y.H.; Chun, H.J.; Koo, J.C.; Cheong, Y.H.; Kim, C.Y.; Kim, M.C.; Chung, W.S.; Kim, J.C.; Yoo, J.H.; Koo, Y.D.; Koo, S.C.; Lim, C.O.; Lee, S.Y.; Cho, M.J. Characterization of a stamen-specific cDNA encoding a novel plant defensin in Chinese cabbage. Plant Mol. Biol., 2002, 50(1), 59-69.
[] [PMID: 12139009]
Lai, F.M.; DeLong, C.; Mei, K.; Wignes, T.; Fobert, P.R. Analysis of the DRR230 family of pea defensins: gene expression pattern and evidence of broad host-range antifungal activity. Plant Sci., 2002, 163(4), 855-864.
Kanzaki, H.; Nirasawa, S.; Saitoh, H.; Ito, M.; Nishihara, M.; Terauchi, R.; Nakamura, I. Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor. Appl. Genet., 2002, 105(6-7), 809-814.
[] [PMID: 12582903]
Turrini, A.; Sbrana, C.; Pitto, L.; Castiglione, M.R.; Giorgetti, L.; Briganti, R.; Bracci, T.; Evangelista, M.; Nuti, M.; Giovannetti, M.J. The antifungal Dm‐AMP1 protein from Dahlia merckii expressed in Solanum melongena is released in root exudates and differentially affects pathogenic fungi and mycorrhizal symbiosis. New Phytol., 2004, 163(2), 393-403.
Zhu, Y.J.; Agbayani, R.; Moore, P.H. Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor. Planta, 2007, 226(1), 87-97.
[] [PMID: 17216480]
Swathi Anuradha, T.; Divya, K.; Jami, S.K.; Kirti, P.B. Transgenic tobacco and peanut plants expressing a mustard defensin show resistance to fungal pathogens. Plant Cell Rep., 2008, 27(11), 1777-1786.
[] [PMID: 18758784]
Choi, Y.; Choi, Y.D.; Lee, J.S. Antimicrobial activity of gamma-thionin-like soybean SE60 in E. coli and tobacco plants. Biochem. Biophys. Res. Commun., 2008, 375(2), 230-234.
[] [PMID: 18700134]
Lee, S.C.; Hwang, I.S.; Choi, H.W.; Hwang, B.K. Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol., 2008, 148(2), 1004-1020.
[] [PMID: 18676663]
Kostov, K.; Christova, P.; Slavov, S.; Batchvarova, R. Constitutive expression of a radish defensin gene Rs-AFP2 in tomato increases the resistance to fungal pathogens. Biotechnol. Biotechnol. Equip., 2009, 23(1), 1121-1125.
Zainal, Z.; Marouf, E.; Ismail, I.; Fei, C. Expression of the Capsicuum annum (chili) defensin gene in transgenic tomatoes confers enhanced resistance to fungal pathogens. Am. J. Plant Physiol., 2009, 4(2), 70-79.
Wu, J.; Wu, L.T.; Liu, Z.B.; Qian, L.; Wang, M.H.; Zhou, L.R.; Yang, Y.; Li, X.F. A plant defensin gene from Orychophragmus violaceus can improve Brassica napus resistance to Sclerotinia sclerotiorum. Afr. J. Biotechnol., 2009, 8(22)
Jha, S.; Tank, H.G.; Prasad, B.D.; Chattoo, B.B. Expression of Dm-AMP1 in rice confers resistance to Magnaporthe oryzae and Rhizoctonia solani. Transgenic Res., 2009, 18(1), 59-69.
[] [PMID: 18618285]
Jha, S.; Chattoo, B.B. Transgene stacking and coordinated expression of plant defensins confer fungal resistance in rice. Rice (N. Y.), 2009, 2(4), 143-154.
Jha, S.; Chattoo, B.B. Expression of a plant defensin in rice confers resistance to fungal phytopathogens. Transgenic Res., 2010, 19(3), 373-384.
[] [PMID: 19690975]
Portieles, R.; Ayra, C.; Gonzalez, E.; Gallo, A.; Rodriguez, R.; Chacón, O.; López, Y.; Rodriguez, M.; Castillo, J.; Pujol, M.; Enriquez, G.; Borroto, C.; Trujillo, L.; Thomma, B.P.; Borrás-Hidalgo, O. NmDef02, a novel antimicrobial gene isolated from Nicotiana megalosiphon confers high-level pathogen resistance under greenhouse and field conditions. Plant Biotechnol. J., 2010, 8(6), 678-690.
[] [PMID: 20626828]
Abdallah, N.A.; Shah, D.; Abbas, D.; Madkour, M. Stable integration and expression of a plant defensin in tomato confers resistance to fusarium wilt. GM Crops, 2010, 1(5), 344-350.
[] [PMID: 21844692]
Li, Z.; Zhou, M.; Zhang, Z.; Ren, L.; Du, L.; Zhang, B.; Xu, H.; Xin, Z. Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct. Integr. Genomics, 2011, 11(1), 63-70.
[] [PMID: 21279533]
Wang, B.; Yu, J.; Zhu, D.; Zhao, Q. Maize defensin ZmDEF1 is involved in plant response to fungal phytopathogens. Afr. J. Biotechnol., 2011, 10(72), 16128-16137.
Ghag, S.B.; Shekhawat, U.K.S.; Ganapathi, T.R. Petunia floral defensins with unique prodomains as novel candidates for development of fusarium wilt resistance in transgenic banana plants. PLoS One, 2012, 7(6)e39557
[] [PMID: 22745785]
Kaur, J.; Thokala, M.; Robert-Seilaniantz, A.; Zhao, P.; Peyret, H.; Berg, H.; Pandey, S.; Jones, J.; Shah, D. Subcellular targeting of an evolutionarily conserved plant defensin MtDef4.2 determines the outcome of plant-pathogen interaction in transgenic Arabidopsis. Mol. Plant Pathol., 2012, 13(9), 1032-1046.
[] [PMID: 22776629]
Vijayan, S.; Singh, N.; Shukla, P.; Kirti, P. Defensin (TvD1) from Tephrosia villosa exhibited strong anti-insect and anti-fungal activities in transgenic tobacco plants. J. Pest Sci., 2013, 86(2), 337-344.
Vasavirama, K.; Kirti, P. Constitutive expression of a fusion gene comprising-defensin (Tfgd2) and antifungal protein (RsAFP2) confers enhanced disease and insect resistance in transgenic tobacco. Plant Cell Tissue Organ Cult., 2013, 3(115), 309-319.
Seo, H.H.; Park, S.; Park, S.; Oh, B.J.; Back, K.; Han, O.; Kim, J.I.; Kim, Y.S. Overexpression of a defensin enhances resistance to a fruit-specific anthracnose fungus in pepper. PLoS One, 2014, 9(5)e97936
[] [PMID: 24848280]
Gaspar, Y.M.; McKenna, J.A.; McGinness, B.S.; Hinch, J.; Poon, S.; Connelly, A.A.; Anderson, M.A.; Heath, R.L. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J. Exp. Bot., 2014, 65(6), 1541-1550.
[] [PMID: 24502957]
Ghag, S.B.; Shekhawat, U.K.S.; Ganapathi, T.R. Transgenic banana plants expressing a Stellaria media defensin gene (Sm-AMP-D1) demonstrate improved resistance to Fusarium oxysporum. Plant Cell Tissue Organ Cult., 2014, 119(2), 247-255.
Kong, K.; Ntui, V.O.; Makabe, S.; Khan, R.S.; Mii, M.; Nakamura, I. Transgenic tobacco and tomato plants expressing wasabi defensin genes driven by root-specific LjNRT2 and AtNRT2.1 promoters confer resistance against Fusarium oxysporum. Plant Biotechnol., 2014, 31(2), 89-96.
Sasaki, K.; Kuwabara, C.; Umeki, N.; Fujioka, M.; Saburi, W.; Matsui, H.; Abe, F.; Imai, R. The cold-induced defensin TAD1 confers resistance against snow mold and Fusarium head blight in transgenic wheat. J. Biotechnol., 2016, 228, 3-7.
[] [PMID: 27080445]
Bala, M.; Radhakrishnan, T.; Kumar, A.; Mishra, G.P.; Dobraia, J.R.; Kirti, P.B. Overexpression of a fusion defensin gene from radish and fenugreek improves resistance against leaf spot diseases caused by Cercospora arachidicola and Phaeoisariopsis personata in peanut. Turk. J. Biol., 2015, 40(1), 139-149.
Kaur, J.; Fellers, J.; Adholeya, A.; Velivelli, S.L.; El-Mounadi, K.; Nersesian, N.; Clemente, T.; Shah, D. Expression of apoplast-targeted plant defensin MtDef4.2 confers resistance to leaf rust pathogen Puccinia triticina but does not affect mycorrhizal symbiosis in transgenic wheat. Transgenic Res., 2017, 26(1), 37-49.
[] [PMID: 27582300]
Pérez-Bernal, M.; Delgado, M.; Cruz, A.; Abreu, D.; Valdivia, O.; Armas, R. Marker-free transgenic rice lines with a defensin gene are potentially active against phytopathogenic fungus Sarocladium oryzae. Acta Phytopathol. Entomol. Hung., 2017, 52(2), 1-10.
Hsiao, P.Y.; Cheng, C.P.; Koh, K.W.; Chan, M.T. The Arabidopsis defensin gene, AtPDF1.1, mediates defence against Pectobacterium carotovorum subsp. carotovorum via an iron-withholding defence system. Sci. Rep., 2017, 7(1), 9175.
[] [PMID: 28835670]
Lee, H.H.; Kim, J.S.; Hoang, Q.T.; Kim, J.I.; Kim, Y.S. Root-specific expression of defensin in transgenic tobacco results in enhanced resistance against Phytophthora parasitica var. nicotianae. Eur. J. Plant Pathol., 2018, 151(3), 811-823.
Badrhadad, A.; Nazarian-Firouzabadi, F. Ismaili, A Fusion of a chitin-binding domain to an antibacterial peptide to enhance resistance to Fusarium solani in tobacco (Nicotiana tabacum).3 Biotech, 2018, 8(9), 391.
[[http://10.1007/s13205-018-1416-7]] [PMID: 30175028]
Kader, J.C. Proteins and the intracellular exchange of lipids. I. Stimulation of phospholipid exchange between mitochondria and microsomal fractions by proteins isolated from potato tuber. Biochim. Biophys. Acta, 1975, 380(1), 31-44.
[] [PMID: 804327]
Boutrot, F.; Chantret, N.; Gautier, M.F. Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics, 2008, 9(1), 86.
[] [PMID: 18291034]
Lei, L.; Chen, L.; Shi, X.; Li, Y.; Wang, J.; Chen, D.; Xie, F.; Li, Y. A nodule-specific lipid transfer protein AsE246 participates in transport of plant-synthesized lipids to symbiosome membrane and is essential for nodule organogenesis in Chinese milk vetch. Plant Physiol., 2014, 164(2), 1045-1058.
[] [PMID: 24367021]
Wei, K.; Zhong, X. Non-specific lipid transfer proteins in maize. BMC Plant Biol., 2014, 14, 281.
[] [PMID: 25348423]
Carvalho, Ade. O.; Gomes, V.M. Role of plant lipid transfer proteins in plant cell physiology-a concise review. Peptides, 2007, 28(5), 1144-1153.
[] [PMID: 17418913]
Kader, J.C. Lipid-transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, 47, 627-654.
[] [PMID: 15012303]
Selitrennikoff, C.P. Antifungal proteins. Appl. Environ. Microbiol., 2001, 67(7), 2883-2894.
[] [PMID: 11425698]
Molina, A.; García-Olmedo, F. Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J., 1997, 12(3), 669-675.
[] [PMID: 9351251]
Bi, Y.M.; Cammue, B.; Goodwin, P. KrishnaRaj, S.; Saxena, P. Resistance to Botrytis cinerea in scented geranium transformed with a gene encoding the antimicrobial protein Ace-AMP1. Plant Cell Rep., 1999, 18(10), 835-840.
Li, X.; Gasic, K.; Cammue, B.; Broekaert, W.; Korban, S.S. Transgenic rose lines harboring an antimicrobial protein gene, Ace-AMP1, demonstrate enhanced resistance to powdery mildew (Sphaerotheca pannosa). Planta, 2003, 218(2), 226-232.
[] [PMID: 14508687]
Jung, H.W.; Kim, K.D.; Hwang, B.K. Identification of pathogen-responsive regions in the promoter of a pepper lipid transfer protein gene (CALTPI) and the enhanced resistance of the CALTPI transgenic Arabidopsis against pathogen and environmental stresses. Planta, 2005, 221(3), 361-373.
[] [PMID: 15654638]
Patkar, R.N.; Chattoo, B.B. Transgenic indica rice expressing ns-LTP-like protein shows enhanced resistance to both fungal and bacterial pathogens. Mol. Breed., 2006, 17(2), 159-171.
Roy-Barman, S.; Sautter, C.; Chattoo, B.B. Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses. Transgenic Res., 2006, 15(4), 435-446.
[] [PMID: 16906444]
Yang, X.; Xiao, Y.; Wang, X.; Pei, Y. Expression of a novel small antimicrobial protein from the seeds of motherwort (Leonurus japonicus) confers disease resistance in tobacco. Appl. Environ. Microbiol., 2007, 73(3), 939-946.
[] [PMID: 17158620]
Sarowar, S.; Kim, Y.J.; Kim, K.D.; Hwang, B.K.; Ok, S.H.; Shin, J.S. Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep., 2009, 28(3), 419-427.
[] [PMID: 19089429]
Jia, Z.; Gou, J.; Sun, Y.; Yuan, L.; Tang, Q.; Yang, X.; Pei, Y.; Luo, K. Enhanced resistance to fungal pathogens in transgenic Populus tomentosa Carr. by overexpression of an nsLTP-like antimicrobial protein gene from motherwort (Leonurus japonicus). Tree Physiol., 2010, 30(12), 1599-1605.
[] [PMID: 21084346]
Zhu, X.; Li, Z.; Xu, H.; Zhou, M.; Du, L.; Zhang, Z. Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistances to Cochliobolus sativus and Fusarium graminearum in transgenic wheat. Funct. Integr. Genomics, 2012, 12(3), 481-488.
[] [PMID: 22689341]
Jiang, Y.; Fu, X.; Wen, M.; Wang, F.; Tang, Q.; Tian, Q.; Luo, K. Overexpression of an nsLTPs-like antimicrobial protein gene (LJAMP2) from motherwort (Leonurus japonicus) enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Physiol. Mol. Plant Pathol., 2013, 82, 81-87.
Mohandas, S.; Sowmya, H.; Saxena, A.; Meenakshi, S.; Rani, R.T.; Mahmood, R. Transgenic banana cv. Rasthali (AAB, Silk gp) harboring Ace-AMP1 gene imparts enhanced resistance to Fusarium oxysporum f. sp. cubense race 1. Sci. Hortic. (Amsterdam), 2013, 164, 392-399.
Safi, H.; Saibi, W.; Alaoui, M.M.; Hmyene, A.; Masmoudi, K.; Hanin, M.; Brini, F. A wheat lipid transfer protein (TdLTP4) promotes tolerance to abiotic and biotic stress in Arabidopsis thaliana. Plant Physiol. Biochem., 2015, 89, 64-75.
[] [PMID: 25703105]
Giroux, M.J.; Sripo, T.; Gerhardt, S.; Sherwood, J. Puroindolines: Their role in grain hardness and plant defence. Biotechnol. Genet. Eng. Rev., 2003, 20(1), 277-290.
[] [PMID: 14997856]
Xia, L.; Geng, H.; Chen, X.; He, Z.; Lillemo, M.; Morris, C.F. Silencing of puroindoline a alters the kernel texture in transgenic bread wheat. J. Cereal Sci., 2008, 47(2), 331-338.
Dhatwalia, V.K.; Sati, O.; Tripathi, M.; Kumar, A. Isolation, characterization and antimicrobial activity at diverse dilution of wheat puroindoline protein. WJAS, 2009, 5(3), 297-300.
Dubreil, L.; Gaborit, T.; Bouchet, B.; Gallant, D.J.; Broekaert, W.F.; Quillien, L.; Marion, D. Spatial and temporal distribution of the major isoforms of puroindolines (puroindoline-a and puroindoline-b) and nonspecific lipid transfer protein (ns-LTP1e 1) of Triticum aestivum seeds. Relationships with their in vitro antifungal properties. Plant Sci., 1998, 138(2), 121-135.
Alfred, R.L.; Palombo, E.A.; Panozzo, J.F.; Bhave, M. The antimicrobial domains of wheat puroindolines are cell-penetrating peptides with possible intracellular mechanisms of action. PLoS One, 2013, 8(10)e75488
[] [PMID: 24098387]
Krishnamurthy, K.; Balconi, C.; Sherwood, J.E.; Giroux, M.J. Wheat puroindolines enhance fungal disease resistance in transgenic rice. Mol. Plant Microbe Interact., 2001, 14(10), 1255-1260.
[] [PMID: 11605965]
Faize, M.; Sourice, S.; Dupuis, F.; Parisi, L.; Gautier, M.F.; Chevreau, E. Expression of wheat puroindoline-b reduces scab susceptibility in transgenic apple (Malus× domestica Borkh.). Plant Sci., 2004, 167(2), 347-354.
Luo, L.; Zhang, J.; Yang, G.; Li, Y.; Li, K.; He, G. Expression of puroindoline a enhances leaf rust resistance in transgenic tetraploid wheat. Mol. Biol. Rep., 2008, 35(2), 195-200.
[] [PMID: 17380426]
Zhang, J.; Martin, J.M.; Balint‐Kurti, P.; Huang, L.; Giroux, M.J. The wheat puroindoline genes confer fungal resistance in transgenic corn. J. Phytopathol., 2011, 159(3), 188-190.
Kim, K.H.; Feiz, L.; Dyer, A.T.; Grey, W.; Hogg, A.C.; Martin, J.M.; Giroux, M.J. Increased resistance to Penicillium seed rot in transgenic wheat overexpressing puroindolines. J. Phytopathol., 2012, 160(5), 243-247.
Archer, B.L. The proteins of Hevea brasiliensis Latex. 4. Isolation and characterization of crystalline hevein. Biochem. J., 1960, 75(2), 236-240.
[] [PMID: 13794068]
Porto, W.F.; Souza, V.A.; Nolasco, D.O.; Franco, O.L. In silico identification of novel hevein-like peptide precursors. Peptides, 2012, 38(1), 127-136.
[] [PMID: 22981805]
Van Parijs, J.; Broekaert, W.F.; Goldstein, I.J.; Peumans, W.J. Hevein: An antifungal protein from rubber-tree (Hevea brasiliensis) latex. Planta, 1991, 183(2), 258-264.
[] [PMID: 24193629]
Slavokhotova, A.A.; Naumann, T.A.; Price, N.P.; Rogozhin, E.A.; Andreev, Y.A.; Vassilevski, A.A.; Odintsova, T.I. Novel mode of action of plant defense peptides - hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases. FEBS J., 2014, 281(20), 4754-4764.
[] [PMID: 25154438]
Liang, H.; Catranis, C.M.; Maynard, C.A.; Powell, W.A. Enhanced resistance to the poplar fungal pathogen, Septoria musiva, in hybrid poplar clones transformed with genes encoding antimicrobial peptides. Biotechnol. Lett., 2002, 24(5), 383-389.
Koo, J.C.; Chun, H.J.; Park, H.C.; Kim, M.C.; Koo, Y.D.; Koo, S.C.; Ok, H.M.; Park, S.J.; Lee, S.H.; Yun, D.J.; Lim, C.O.; Bahk, J.D.; Lee, S.Y.; Cho, M.J. Over-expression of a seed specific hevein-like antimicrobial peptide from Pharbitis nil enhances resistance to a fungal pathogen in transgenic tobacco plants. Plant Mol. Biol., 2002, 50(3), 441-452.
[] [PMID: 12369620]
Lee, O.S.; Lee, B.; Park, N.; Koo, J.C.; Kim, Y.H.; Prasad, D.T.; Karigar, C.; Chun, H.J.; Jeong, B.R.; Kim, D.H.; Nam, J.; Yun, J.G.; Kwak, S.S.; Cho, M.J.; Yun, D.J. Pn-AMPs, the hevein-like proteins from Pharbitis nil confers disease resistance against phytopathogenic fungi in tomato, Lycopersicum esculentum. Phytochemistry, 2003, 62(7), 1073-1079.
[] [PMID: 12591259]
Khan, R.S.; Nishihara, M.; Yamamura, S.; Nakamura, I.; Mii, M. Transgenic potatoes expressing wasabi defensin peptide confer partial resistance to gray mold (Botrytis cinerea). Plant Biotechnol., 2006, 23(2), 179-183.
Sjahril, R.; Chin, D.P.; Khan, R.S.; Yamamura, S.; Nakamura, I.; Amemiya, Y.; Mii, M. Transgenic Phalaenopsis plants with resistance to Erwinia carotovora produced by introducing wasabi defensin gene using Agrobacterium method. Plant Biotechnol. J., 2006, 23(2), 191-194.
Ntui, V.O.; Thirukkumaran, G.; Azadi, P.; Khan, R.S.; Nakamura, I.; Mii, M. Stable integration and expression of wasabi defensin gene in “Egusi” melon (Colocynthis citrullus L.) confers resistance to Fusarium wilt and Alternaria leaf spot. Plant Cell Rep., 2010, 29(9), 943-954.
[] [PMID: 20552202]
R., Shukurov D Voblikova, V.; Nikonorova, A.K.; Komakhin, R.A.; V Komakhina, V.; A Egorov, T.; V Grishin, E.; V Babakov, A. Transformation of tobacco and Arabidopsis plants with Stellaria media genes encoding novel hevein-like peptides increases their resistance to fungal pathogens. Transgenic Res., 2012, 21(2), 313-325.
[] [PMID: 21706181]
Segura, A.; Moreno, M.; Madueño, F.; Molina, A.; García-Olmedo, F. Snakin-1, a peptide from potato that is active against plant pathogens. Mol. Plant Microbe Interact., 1999, 12(1), 16-23.
[] [PMID: 9885189]
Yeung, H.; Squire, C.J.; Yosaatmadja, Y.; Panjikar, S.; López, G.; Molina, A.; Baker, E.N.; Harris, P.W.; Brimble, M.A. Radiation damage and racemic protein crystallography reveal the unique structure of the GASA/snakin protein superfamily. Angew. Chem. Int. Ed. Engl., 2016, 55(28), 7930-7933.
[] [PMID: 27145301]
Almasia, N.I.; Bazzini, A.A.; Hopp, H.E.; Vazquez-Rovere, C. Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants. Mol. Plant Pathol., 2008, 9(3), 329-338.
[] [PMID: 18705874]
Faccio, P.; Vazquez-Rovere, C.; Hopp, E.; Gonzalez, G.; Decima-Oneto, C.; Favret, E.; Paleo, A.D.; Franzone, P.; Braun, H.; Snape, J. Increased tolerance to wheat powdery mildew by heterologous constitutive expression of the Solanum chacoense snakin-1 gene. Czech J. Genet. Plant Breed., 2011, 47, S135-S141.
Rong, W.; Qi, L.; Wang, J.; Du, L.; Xu, H.; Wang, A.; Zhang, Z. Expression of a potato antimicrobial peptide SN1 increases resistance to take-all pathogen Gaeumannomyces graminis var. tritici in transgenic wheat. Funct. Integr. Genomics, 2013, 13(3), 403-409.
[] [PMID: 23839728]
García, A.N.; Ayub, N.D.; Fox, A.R.; Gómez, M.C.; Diéguez, M.J.; Pagano, E.M.; Berini, C.A.; Muschietti, J.P.; Soto, G. Alfalfa snakin-1 prevents fungal colonization and probably coevolved with rhizobia. BMC Plant Biol., 2014, 14(1), 248.
[] [PMID: 25227589]
Balaji, V.; Smart, C.D. Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhances tolerance to Clavibacter michiganensis subsp. michiganensis in transgenic tomato (Solanum lycopersicum). Transgenic Res., 2012, 21(1), 23-37.
[] [PMID: 21479554]
Mohan, S.; Meiyalaghan, S.; Latimer, J.M.; Gatehouse, M.L.; Monaghan, K.S.; Vanga, B.R.; Pitman, A.R.; Jones, E.E.; Conner, A.J.; Jacobs, J.M. GSL2 over-expression confers resistance to Pectobacterium atrosepticum in potato. Theor. Appl. Genet., 2014, 127(3), 677-689.
[] [PMID: 24370960]
He, H.; Yang, X.; Xun, H.; Lou, X.; Li, S.; Zhang, Z.; Jiang, L.; Dong, Y.; Wang, S.; Pang, J.; Liu, B. Over-expression of GmSN1 enhances virus resistance in Arabidopsis and soybean. Plant Cell Rep., 2017, 36(9), 1441-1455.
[] [PMID: 28656325]
Darqui, F.S.; Radonic, L.M.; Trotz, P.M.; López, N.; Vázquez Rovere, C.; Hopp, H.E.; López Bilbao, M. Potato snakin-1 gene enhances tolerance to Rhizoctonia solani and Sclerotinia sclerotiorum in transgenic lettuce plants. J. Biotechnol., 2018, 283, 62-69.
[] [PMID: 30016741]
Le Nguyen, D.; Heitz, A.; Chiche, L.; Castro, B.; Boigegrain, R.A.; Favel, A.; Coletti-Previero, M.A. Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie, 1990, 72(6-7), 431-435.
[] [PMID: 2124146]
Gao, G.H.; Liu, W.; Dai, J.X.; Wang, J.F.; Hu, Z.; Zhang, Y.; Wang, D.C. Solution structure of PAFP-S: A new knottin-type antifungal peptide from the seeds of Phytolacca americana. Biochemistry, 2001, 40(37), 10973-10978.
[] [PMID: 11551192]
Kolmar, H. Biological diversity and therapeutic potential of natural and engineered cystine knot miniproteins. Curr. Opin. Pharmacol., 2009, 9(5), 608-614.
[] [PMID: 19523876]
Hwang, B.; Hwang, J.S.; Lee, J.; Lee, D.G. Antifungal properties and mode of action of psacotheasin, a novel knottin-type peptide derived from Psacothea hilaris. Biochem. Biophys. Res. Commun., 2010, 400(3), 352-357.
[] [PMID: 20735987]
Schaefer, S.C.; Gasic, K.; Cammue, B.; Broekaert, W.; van Damme, E.J.; Peumans, W.J.; Korban, S.S. Enhanced resistance to early blight in transgenic tomato lines expressing heterologous plant defense genes. Planta, 2005, 222(5), 858-866.
[] [PMID: 16047198]
Prasad, B.D.; Jha, S.; Chattoo, B.B. Transgenic indica rice expressing Mirabilis jalapa antimicrobial protein (Mj-AMP2) shows enhanced resistance to the rice blast fungus Magnaporthe oryzae. Plant Sci., 2008, 175(3), 364-371.
Craik, D.J.; Daly, N.L.; Bond, T.; Waine, C. Plant cyclotides: A unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol., 1999, 294(5), 1327-1336.
[] [PMID: 10600388]
Gruber, C.W.; Elliott, A.G.; Ireland, D.C.; Delprete, P.G.; Dessein, S.; Göransson, U.; Trabi, M.; Wang, C.K.; Kinghorn, A.B.; Robbrecht, E.; Craik, D.J. Distribution and evolution of circular miniproteins in flowering plants. Plant Cell, 2008, 20(9), 2471-2483.
[] [PMID: 18827180]
Gruber, C.W. Global cyclotide adventure: A journey dedicated to the discovery of circular peptides from flowering plants. Biopolymers, 2010, 94(5), 565-572.
[] [PMID: 20564015]
Craik, D.J. Discovery and applications of the plant cyclotides. Toxicon, 2010, 56(7), 1092-1102.
[] [PMID: 20219513]
Saska, I.; Gillon, A.D.; Hatsugai, N.; Dietzgen, R.G.; Hara-Nishimura, I.; Anderson, M.A.; Craik, D.J. An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J. Biol. Chem., 2007, 282(40), 29721-29728.
[] [PMID: 17698845]
Gillon, A.D.; Saska, I.; Jennings, C.V.; Guarino, R.F.; Craik, D.J.; Anderson, M.A. Biosynthesis of circular proteins in plants. Plant J., 2008, 53(3), 505-515.
[] [PMID: 18086282]
Strömstedt, A.A.; Park, S.; Burman, R.; Göransson, U. Bactericidal activity of cyclotides where phosphatidylethanolamine-lipid selectivity determines antimicrobial spectra. Biochim. Biophys. Acta Biomembr., 2017, 1859(10), 1986-2000.
[] [PMID: 28669767]
Nawae, W.; Hannongbua, S.; Ruengjitchatchawalya, M. Defining the membrane disruption mechanism of kalata B1 via coarse-grained molecular dynamics simulations. Sci. Rep., 2014, 4, 3933.
[] [PMID: 24492660]
Henriques, S.T.; Huang, Y.H.; Chaousis, S.; Sani, M.A.; Poth, A.G.; Separovic, F.; Craik, D.J. The prototypic cyclotide Kalata B1 has a unique mechanism of entering cells. Chem. Biol., 2015, 22(8), 1087-1097.
[] [PMID: 26278183]
Shafee, T.M.; Lay, F.T.; Hulett, M.D.; Anderson, M.A. The defensins consist of two independent, convergent protein superfamilies. Mol. Biol. Evol., 2016, 33(9), 2345-2356.
[] [PMID: 27297472]
Zhou, W.; Gao, B.; Zhu, S. Did cis- and trans-defensins derive from a common ancestor? Immunogenetics, 2019, 71(1), 61-69.
[] [PMID: 30280251]
Zhu, S. Evidence for myxobacterial origin of eukaryotic defensins. Immunogenetics, 2007, 59(12), 949-954.
[] [PMID: 18058146]
Mygind, P.H.; Fischer, R.L.; Schnorr, K.M.; Hansen, M.T.; Sönksen, C.P.; Ludvigsen, S.; Raventós, D.; Buskov, S.; Christensen, B.; De Maria, L.; Taboureau, O.; Yaver, D.; Elvig-Jørgensen, S.G.; Sørensen, M.V.; Christensen, B.E.; Kjaerulff, S.; Frimodt-Moller, N.; Lehrer, R.I.; Zasloff, M.; Kristensen, H.H. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature, 2005, 437(7061), 975-980.
[] [PMID: 16222292]
Aerts, A.M.; Thevissen, K.; Bresseleers, S.M.; Sels, J.; Wouters, P.; Cammue, B.P.; François, I.E.A.J. Arabidopsis thaliana plants expressing human beta-defensin-2 are more resistant to fungal attack: functional homology between plant and human defensins. Plant Cell Rep., 2007, 26(8), 1391-1398.
[] [PMID: 17340092]
Thevissen, K.; Warnecke, D.C.; François, I.E.; Leipelt, M.; Heinz, E.; Ott, C.; Zähringer, U.; Thomma, B.P.; Ferket, K.K.; Cammue, B.P. Defensins from insects and plants interact with fungal glucosylceramides. J. Biol. Chem., 2004, 279(6), 3900-3905.
[] [PMID: 14604982]
Zhang, B.; Qin, Y.; Han, Y.; Dong, C.; Li, P.; Shang, Q. Comparative proteomic analysis reveals intracellular targets for bacillomycin L to induce Rhizoctonia solani Kühn hyphal cell death. Biochim. Biophys. Acta, 2016, 1864(9), 1152-1159.
[] [PMID: 27267622]
Delgado, J.; Owens, R.A.; Doyle, S.; Asensio, M.A.; Núñez, F. Impact of the antifungal protein PgAFP from Penicillium chrysogenum on the protein profile in Aspergillus flavus. Appl. Microbiol. Biotechnol., 2015, 99(20), 8701-8715.
[] [PMID: 26078108]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Published on: 29 September, 2019
Page: [720 - 742]
Pages: 23
DOI: 10.2174/0929866526666190619112438
Price: $65

Article Metrics

PDF: 26
PRC: 1