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Antimicrobial peptides as effective tools for enhanced disease resistance in plants

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Abstract

Plants being exposed to a variety of pathogenic infections, acquire the natural mechanism of combating the pathogens leading to an increased level of defense. Several pathogenesis-related (PR) proteins are expressed by plants; approximately 17 families have been discovered till now. Most of them confer resistance to fungal pathogens and some of the PR proteins are bactericidal. These PR proteins consist of a short sequence of amino acids thus called antimicrobial peptides (AMPs). These AMPs permeabilize the pathogenic membrane via pore formation leading to cell death. The specific characteristic of these peptides is conserved domain and the disulfide bond pattern. Several types of AMPs such as defensins, thionins, cyclotides, lipid transfer proteins (LTPs) and several others, with a diverse mode of action, have been characterized from different plant species. These AMPs have been playing an important role in the host plant’s defense against the pathogens. In this review we summarized types of AMPs, their structural conformation and mode of action, their expression and co-expression in transgenic plants for conferring elevated resistance against the phytopathogens.

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References

  • Aerts AM, Carmona-Gutierrez D, Lefevre S, Govaert G, François IE, Madeo F, Santos R, Cammue B, Thevissen K (2009) The antifungal plant defensin RsAFP2 from radish induces apoptosis in a metacaspase independent way in Candida albicans. FEBS Lett 583:2513–2516

    Article  CAS  PubMed  Google Scholar 

  • Allen A, Snyder AK, Preuss M, Nielsen EE, Shah DM, Smith TJ (2008) Plant defensins and virally encoded fungal toxin KP4 inhibit plant root growth. Planta 227:331–339

    Article  CAS  PubMed  Google Scholar 

  • Asano T, Miwa A, Maeda K, Kimura M, Nishiuchi T (2013) The secreted antifungal protein thionin 2.4 in Arabidopsis thaliana suppresses the toxicity of a fungal fruit body lectin from Fusarium graminearum. PLoS Pathog 9:e1003581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balls AK, Hale WS, Harris TH (1942) A crystalline protein obtained from a lipoprotein of wheat flour. Ceram Chem 19:279–288

    CAS  Google Scholar 

  • Bard GCV, Zottich U, Souza TAM, Ribeiro SFF, Dias GB, Pireda S, Da Cunha M, Rodrigues R, Pereira LS, Machado OLT, Carvalho AO, Gomes VM (2016) Purification, biochemical characterization, and antimicrobial activity of a new lipid transfer protein from Coffeacanephora seeds. Genet Mol Res. https://doi.org/10.4238/gmr15048859

    Article  PubMed  Google Scholar 

  • Berec B, Mills EN, Tamás L, Láng F, Shewry PR, Mackie AR (2010) Structural stability and surface activity of sunflower 2S albumins and non-specific lipid transfer protein. J Agric Food Chem 58:6490–6497

    Article  CAS  Google Scholar 

  • Blein JP, Coutos-Thévenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7:293–296

    Article  CAS  PubMed  Google Scholar 

  • Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977

    Article  CAS  PubMed  Google Scholar 

  • Bogdanov IV, Shenkarev ZO, Finkina EI, Melnikova DN, Rumynskiy EI, Arseniev AS, Ovchinnikova T (2016) A novel lipid transfer protein from the pea Pisum sativum: isolation, recombinant expression, solution structure, antifungal activity, lipid binding, and allergenic properties. BMC Plant Biol 16:107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohlmann H, Clausen S, Behnke S, Giese H, Hiller C, Reimann-Philipp U, Schrader G, Barkholt V, Apel K (1988) 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 7:1559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boman HG (2000) Innate immunity and the normal microflora. Immunol Rev 173:5–16

    Article  CAS  PubMed  Google Scholar 

  • Broekaert WF, Mariën W, Terras FR, De Bolle MF, Proost P, Van Damme J, Dillen L, Claeys M, Rees SB, Vanderleyden J et al (1992) Antimicrobial peptides from Amaranthus caudatus seeds with sequence homology to the cysteine/glycine-rich domain of chitin-binding proteins. Biochemistry 31:4308–4314

    Article  CAS  PubMed  Google Scholar 

  • Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250

    Article  CAS  PubMed  Google Scholar 

  • Cammue BPA, Thevissen K, Hendriks M, Eggermont K, Goderis IJ, Proost P, Van Damme J, Osborn RW, Guerbette F, Kader JC (1995) A potent antimicrobial protein from onion seeds showing sequence homology to plant lipid transfer proteins. Plant Physiol 109:445–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chagolla-Lopez A, Blanco-Labra A, Patthy A, Sánchez R, Pongor S (1994) A novel-amylase inhibitor from Amaranth (Amaranthus hypocondriacus) seeds. J Biol Chem 269(38):23675–23680

    CAS  PubMed  Google Scholar 

  • Chan YS, Wong JH, Fang EF, Pan WL, Ng TB (2012) An antifungal peptide from Phaseolus vulgaris cv. brown kidney bean. Acta Bioch Biophysica Sinica 44:307–315

    Article  CAS  Google Scholar 

  • Chávez MI, Vila-Perelló M, Cañada FJ, Andreu D, Jiménez-Barbero J (2010) Effect of a serine-to-aspartate replacement on the recognition of chitin oligosaccharides by truncated hevein. A 3D view by using NMR. Carbohydrate Res 345:1461–1468

    Article  CAS  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craik DJ (2010) Discovery and applications of the plant cyclotides. Toxicon 56:1092–1102

    Article  CAS  PubMed  Google Scholar 

  • Craik DJ, Čemazar M, Wang CK, Daly NL (2006) The cyclotide family of circular miniproteins: nature’s combinatorial peptide template. Pep Sci 84:250–266

    Article  CAS  Google Scholar 

  • Cruz LP, Ribeiro SF, Carvalho AO, Vasconcelos IM, Rodrigue R, Da Cunha M (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

    Article  CAS  PubMed  Google Scholar 

  • Daly NL, Clark RJ, Plan MR, Craik DJ (2006) Kalata B8, a novel antiviral circular protein, exhibits conformational flexibility in the cystine knot motif. Biochem J 393:619–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darwish NA, Khan RS, Ntui VO, Nakamura I, Mii M (2014) Generation of selectable marker-free transgenic eggplant resistant to Alternaria solani using the R/RS site-specific recombination system. Plant Cell Rep 33:411–421

    Article  CAS  PubMed  Google Scholar 

  • De Bolle MF, Osborn RW, Goderis IJ, Noe IL, Acland Hart CA, Torrekens S, Van Leuven F, Broekart NF (1996) Antimicrobial properties from Mirablis jalapa and Amaranthus caudatus: expression, processing, localization and biological activity in transgenic tobacco. Plant Mol Biol 31:993–1008

    Article  PubMed  Google Scholar 

  • De Caleya RF, Gonzalez-Pascual B, García-Olmedo F, Carbonero P (1972) Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro. Appl Microbiol 23:998–1000

    PubMed Central  Google Scholar 

  • De Oliveira Carvalho A, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology—a concise review. Peptides 28:1144–1153

    Article  CAS  Google Scholar 

  • Diz MSS, Carvalho AO, Rodrigues R, Neves-Ferreira AGC, Da Cunha M, Alves EW (2006) Antimicrobial peptides from chilli pepper seeds causes yeast plasma membrane permeabilization and inhibits the acidification of the medium by yeast cells. Biochem Biophys Acta 1760:1323–1332

    Article  CAS  PubMed  Google Scholar 

  • Diz MS, Carvalho AO, Ribeiro SF, DaCunha M, Beltramini L, Rodrigues R (2011) Characterization, immune localization and antifungal activity of a lipid transfer protein from chili pepper (Capsicum annum) seeds with novel a-amylase inhibitory properties. Physiol Plantarum 142:233–246

    Article  CAS  Google Scholar 

  • Dos Santos IS, Carvalho ADO, De Souza-Filho GG, Do Nascimento VV, Machado OI, Gomes VM (2010) Purification of a defensin isolated from Vigna unguiculata seeds, its functional expression in Escherichia coli, and assessment of its insect α-amylase inhibitory activity. Protein Express Purif 71:8–15

    Article  CAS  Google Scholar 

  • Egorov TA, Odintsova TI (2012) Defense peptides of plant immunity. Russ J Bioorg Chem 38:1–9

    Article  CAS  Google Scholar 

  • Evans J, Wang Y, Shaw KP, Vernon LP (1989) Cellular responses to Pyrularia thionin are mediated by Ca2+ influx and phospholipase A2 activation and are inhibited by thionin tyrosine iodination. Proc Nat Acad Sci USA 86:5849–5853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan Y, Du K, Gao Y, Kong Y, Chu C, Sokolov V, Wang Y (2013) Transformation of LTP gene into Brassica napus to enhance its resistance to Sclerotinia sclerotiorum. Russ J Genet 49(4):380–387

    Article  CAS  Google Scholar 

  • Fant F, Vranken W, Broekaert W, Borremans F (1998) Determination of the three-dimensional solution structure of Raphanus sativus antifungal protein 1 by 1 H NMR. J Mol Biol 279:257–270

    Article  CAS  PubMed  Google Scholar 

  • Finkina EI, Shramova EI, Tagaev AA, Ovchinnikova TV (2008) A novel defensin from the lentil Lens culinaris seeds. Biochem Biophys Res Commun 371:860–865

    Article  CAS  PubMed  Google Scholar 

  • Finkina EI, Melnikova DN, Bogdanov IV, Ovchinnikova TV (2016) Lipid transfer proteins as components of the plant innate immune system: structure, functions, and applications. Acta Nat 8:47–61

    Article  CAS  Google Scholar 

  • Fujimura M, Minami Y, Watanabe K, Tadera K (2003) Purification, characterization, and sequencing of a novel type of antimicrobial peptides, Fa-AMP1 and Fa-AMP2, from seeds of buckwheat (Fagopyrum esculentum Moench.). Biosci Biotechnol Biochem 67:1636–1642

    Article  CAS  PubMed  Google Scholar 

  • Fujimura M, Ideguchi M, Minami Y, Watanabe K, Tadera K (2004) Purification, characterization, and sequencing of novel antimicrobial peptides, Tu-AMP 1 and Tu-AMP 2, from bulbs of tulip (Tulipagesneriana). Biosci Biotechnol Biochem 68:571–577

    Article  CAS  PubMed  Google Scholar 

  • Fujimura M, Ideguchi M, Minami Y, Watanabe K, Tadera K (2005) Amino acid sequence and antimicrobial activity of chitin-binding peptides, Pp-AMP 1 and Pp-AMP 2, from Japanese bamboo shoots (Phyllostachyspubescens). Biosci Biotechnol Biochem 69:642–645

    Article  CAS  PubMed  Google Scholar 

  • Games PD, dos Santos IS, Mello ÉO (2008) Isolation, characterization and cloning of a cDNA encoding a new antifungal defensin from Phaseolus vulgaris L. seeds. Peptides 29:2090–2100

    Article  CAS  PubMed  Google Scholar 

  • Gao AG, Hakimi SM, Mittanck CA, Wu Y, Woerner BM, Stark DM, Shah DM, Liang J, Rommens CM (2000) Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat Biotechnol 18:1307–1310

    Article  CAS  PubMed  Google Scholar 

  • Garcia AE, Camarero JA (2010) biological activities of natural and engineered cyclotides, a novel molecular scaffold for peptide-based therapeutics. Curr Mol Pharmacol 3:153–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gausing K (1987) Thionin genes specifically expressed in barley leaves. Planta 171:241–246

    Article  CAS  PubMed  Google Scholar 

  • Göransson U, Herrmann A, Burman R, Haugaard-Jönsson LM, Rosengren KJ (2009) The conserved glu in the cyclotide cycloviolacin O2 has a key structural role. ChemBioChem 10:2354–2360

    Article  CAS  PubMed  Google Scholar 

  • Gran L (1973) On the effect of a polypeptide isolated from “Kalata-Kalata” (Oldenlandia affinis DC) on the oestrogen dominated uterus. Acta Pharmacol Toxicol (Copenh) 33:400–408

    Article  CAS  Google Scholar 

  • Greenwood KP, Daly NL, Brown DL, Stow JL, Craik DJ (2007) The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Inter J Biochem Cell Biol 39:2252–2264

    Article  CAS  Google Scholar 

  • Gruber CW (2010) Global cyclotide adventure: a journey dedicated to the discovery of circular peptides from flowering plants. Peptide Sci 94:565–572

    Article  CAS  Google Scholar 

  • Gruber CW, Cemazar M, Anderson MA, Craik DJ (2007) Insecticidal plant cyclotides and related cystine knot toxins. Toxicon 49:561–575

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Experi Bot 64:1755–1767

    Article  CAS  Google Scholar 

  • Hancock RE, Chapple DS (1999) Peptide antibiotics. Antimicrob Agents Chemother 43:1317–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanks JN, Snyder AK, Graham MA, Shah RK, Blaylock LA, Harrison MJ, Shah DM (2005) Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol Biol 58:385–399

    Article  CAS  PubMed  Google Scholar 

  • Harata K, Muraki M (2000) Crystal structures of Urtica dioica agglutinin and its complex with tri-N-acetylchitotriose. J Mol Biol 297:673

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Xie W, Gong Z (2000) Characteristics and antifungal activity of a chitin binding protein from Ginkgo biloba. FEBS Lett 478:123–126

    Article  CAS  PubMed  Google Scholar 

  • Huang RH, Xiang Y, Liu XZ, Zhang Y, Hu Z, Wang DC (2002) Two novel antifungal peptides distinct with a five-disulfide motif from the bark of Eucommia ulmoides Oliv. FEBS Lett 521:87–90

    Article  CAS  PubMed  Google Scholar 

  • Huang RH, Xiang Y, Tu GZ, Zhang Y, Wang DC (2004) Solution structure of Eucommia antifungal peptide: a novel structural model distinct with a five-disulfide motif. Biochemistry 43:6005–6012

    Article  CAS  Google Scholar 

  • Huang GJ, Lai HC, Chang YS, Sheu MJ, Lu TL, Huang SS, Lin YH (2008) Antimicrobial, dehydroascorbate reductase, and monodehydroascorbate reductase activities of defensin from sweet potato [Ipomoea batatas (L.) Lam. ‘tainong 57′] storage roots. J Agric Food Chem 56:2989–2995

    Article  CAS  PubMed  Google Scholar 

  • Ireland DC, Wang CK, Wilson JA, Gustafson KR, Craik DJ (2008) Cyclotides as natural anti-HIV agents. Peptide Sci 90:51–60

    Article  CAS  Google Scholar 

  • Iwai T, Kaku H, Honkura R, Nakamura S, Ochiai H, Sasaki T, Ohashi Y (2002) Enhanced resistance to seed-transmitted bacterial diseases in transgenic rice plants overproducing an oat cell-wall-bound thionin. Mol Plant Microb Inter 15:515–521

    Article  CAS  Google Scholar 

  • Jack HW, Tzi BN (2005) Vulgarinin, a broad-spectrum antifungal peptide from haricot beans (Phaseolus vulgaris). Inter J Biochem Cell Biol 37:1626–1632

    Article  CAS  Google Scholar 

  • James C (2013) global status of commercialized biotech/GM crops: 2013. ISAAA Brief No. 46. International Service for the Acquisition of Agri-biotech Applications (ISAAA), Ithaca, NY, USA, p 315

  • Jennings C, West J, Waine C, Craik D, Anderson M (2001) Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis. Proc Natl Acad Sci USA 98:10614–10619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha S, Chattoo BB (2009) Transgene stacking and coordinated expression of plant defensins confer fungal resistance in rice. Rice 2:143–154

    Article  Google Scholar 

  • Jha S, Tank HG, Prasad BD, Chattoo BB (2009) Expression of Dm-AMP1 in rice confers resistance to Magnaporthe oryzae and Rhizoctonia solani. Trans Res 18:59–69

    Article  CAS  Google Scholar 

  • Jia Z, Gou J, Sun Y, Yuan L, Tang Q, Yang X, Pei Y, Luo K (2010) 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 30:1599–1605

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Barbero J, Cañada FJ, Asensio JL, Aboitiz N, Vidal P, Canales A, Groves P, Gabius HJ, Siebert HC (2006) Hevein domains: an attractive model to study carbohydrate-protein interactions at atomic resolution. Adv Carbohydr Chem Biochem 60:303–354

    Article  PubMed  Google Scholar 

  • Jung HW, Kim KD, Hwang BK (2005) Identification of pathogenresponsive regions in the promoter of pepper lipid transfer protein gene (CALTP1) and the enhanced resistance of the CALTP1 transgenic Arabidopsis against pathogen and environmental stresses. Planta 221:361–373

    Article  CAS  PubMed  Google Scholar 

  • Kader JC (1996) Lipid-transfer proteins in plants. Ann Rev Plant Biol 47:627–654

    Article  CAS  Google Scholar 

  • Kant P, Liu WZ, Pauls PK (2009) PDC1, a corn defensin peptide expressed in Escherichia coli and Pichia pastoris inhibits growth of Fusarium graminearum. Peptides 30:1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Kanzaki H, Nirasawa S, Saitoh H, Ito M, Nishihara M, Terauchi R, Nakamura I (2002) Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor Appl Genet 105:809–814

    Article  CAS  PubMed  Google Scholar 

  • Khan RS, Nishihara M, Yamamura S, Nakamura I, Mii M (2006) Transgenic potatoes expressing wasabi defensin peptide confer partial resistance to gray mold (Botrytis cinerea). Plant Biotechnol 23:179–183

    Article  Google Scholar 

  • Khan RS, Ntui VO, Chin DP, Nakamura I, Mii M (2011a) Production of marker-free disease-resistant potato using isopentenyl transferase gene as a positive selection marker. Plant Cell Rep 30:587–597

    Article  CAS  PubMed  Google Scholar 

  • Khan RS, Nakamura I, Mii M (2011b) Development of disease resistant marker-free tomato by R/RS site-specific recombination. Plant Cell Rep 30:1041–1053

    Article  CAS  PubMed  Google Scholar 

  • Khan RS, Darwish NA, Khattak B, Ntui V, Kong K, Shimomae K (2014) Retransformation of marker-free potato for enhanced resistance against fungal pathogens by pyramiding chitinase and Wasabi Defensin genes. Mol Biotechnol 56:814–823

    Article  CAS  PubMed  Google Scholar 

  • Kiba A, Nishihara M, Nakatsuka T, Yamamura S (2012) Gentian lipid transfer protein homolog with antimicrobial properties confers resistance to Botrytis cinerea in transgenic tobacco. Plant Biotechnol 29:95–101

    Article  CAS  Google Scholar 

  • Kini SG, Nguyen P, Weissbach S, Mallagaray A, Shin J, Yoon HS, Tam JP (2015) Studies on the chitin binding property of novel cysteine-rich peptides from Alternanthera sessilis. Biochem 54:6639–6649

    Article  CAS  Google Scholar 

  • Konarev AV, Anisimova IN, Gavrilova V, Vachrusheva T, Konechnaya GY, Lewis M, Shewry PR (2002) Serine proteinase inhibitors in the Compositae: distribution, polymorphism and properties. Phytochem 59:279–291

    Article  CAS  Google Scholar 

  • Kong K, Ntui VO, Makabe S, Khan RS, Mii M, Nakamura I (2014) 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 31:89–96

    Article  CAS  Google Scholar 

  • Koo JC, Lee B, Young ME, Koo SC, Cooper JA, Baek D, Lim CO, Lee SY, Yun DJ, Cho MJ (2004) Pn-AMP1, a plant defense protein, induces actin depolarization in yeasts. Plant Cell Physiol 45:1669–1680

    Article  CAS  PubMed  Google Scholar 

  • Kragh KM, Nielsen JE, Nielsen KK, Dreboldt S, Mikkelsen JD (1995) Characterization and localization of new antifungal cysteine-rich proteins from Beta vulgaris. Mol Plant Microbe Interact 8(3):424–434

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Yusuf MA, Yadav P, Narayan S, Kumar M, Cushman JC (2019) Overexpression of Chickpea defensin gene confers tolerance to water-deficit stress in Arabidopsis thaliana. Front Plant Sci 10:290. https://doi.org/10.3389/fpls.2019.00290

    Article  PubMed  PubMed Central  Google Scholar 

  • Lascombe MB, Buhot N, Bakan B, Marion D, Blein JP, Lamb CJ, Prangé T (2006) Crystallization of DIR1, a LTP2-like resistance signalling protein from Arabidopsis thaliana. Acta Crystallographica Section F. Struct Biol Crystal Commun 62:702–704

    Article  CAS  Google Scholar 

  • Lay F, Anderson M (2005) Defensins-components of the innate immune system in plants. Curr Protein Pept Sci 6:85–101

    Article  CAS  Google Scholar 

  • Lay FT, Brugliera F, Anderson MA (2003a) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131:1283–1293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lay FT, Schirra HJ, Scanlon MJ, Anderson MA, Craik DJ (2003b) The three-dimensional solution structure of nad1, a new floral defensin from Nicotianaalata and its application to a homology model of the crop defense protein alfafp. J Mol Biol 325:175–188

    Article  CAS  PubMed  Google Scholar 

  • Lee OS, Lee B, Park N, Koo JC, Kim YH, Karigar C, Chun HJ, Jeong BR, Kim DH, Nam J (2003) Pn-AMPs, the hevein-like proteins from Pharbitis nil confers disease resistance against phytopathogenic fungi in tomato, Lycopersicum esculentum. Phytochem 62:1073–1079

    Article  CAS  Google Scholar 

  • Lin P, Ng TB (2009) Brassiparin, an antifungal peptide from Brassica parachinensis seeds. J Appl Microbiol 106:554–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin P, Xia L, Wong JH, Shi X (2007) Lipid transfer proteins from Brassica campestris and mung bean surpass mung bean chitinase in exploitability. J Peptide Sci 13:642–648

    Article  CAS  Google Scholar 

  • Lipkin A, Anisimova V, Nikonorova A, Babakov A, Krause E, Bienert M, Grishin E, Egorov T (2005) An antimicrobial peptide Ar-AMP from amaranth (Amaranth.s retroflexus L.) seeds. Phytochem 66:2426–2431

    Article  CAS  Google Scholar 

  • Ma X, Liu D, Tang H, Wang Y, Wu T, Li Y, Yang J, Yang J, Sun S, Zhang F (2013) Purification and characterization of a novel antifungal protein with antiproliferation and anti-HIV-1 reverse transcriptase activities from Peganum harmala seeds. Acta Biochim Biophys Sin 45:87–94

    Article  CAS  PubMed  Google Scholar 

  • Martins JC, Enassar M, Willem R, Wieruzeski JM, Lippens G, Wodak SJ (2001) Solution structure of the main α-amylase inhibitor from amaranth seeds. Eur J Biochem 268:2379–2389

    Article  CAS  PubMed  Google Scholar 

  • Mendez E, Moreno A, Colilla F, Pelaez F, Limas GG, Mendez R, Soriano F, Salinas M, Haro C (1990) Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, γ-hordothionin, from barley endosperm. Eur J Biochem 194:533–539

    Article  CAS  Google Scholar 

  • Mew TW, Vera Cruz CM, Medalla ES (1992) Changes in the race frequency of Xanthomonas oryzae pv. oryzae in response to the planting of rice cultivars in the Philippines. Plant Dis 76:1029–1032

    Article  Google Scholar 

  • Ml Colgrave, Craik DJ (2004) Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochem 43:5965–5975

    Article  CAS  Google Scholar 

  • Molina A, Garcia-Olmedo F (1997) Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J 12:669–675

    Article  CAS  PubMed  Google Scholar 

  • Molina A, Segura A, García-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316:119–122

    Article  CAS  PubMed  Google Scholar 

  • Montesinos E (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol Lett 270:1–11

    Article  CAS  PubMed  Google Scholar 

  • Nawrot R, Barylski J, Nowicki G, Broniarczyk J, Buchwald W, Go´zdzicka ozefiak A (2014) Plant antimicrobial peptides. Folia Microbiol 59:181–196

    Article  CAS  Google Scholar 

  • Nguyen LD, Heitz A, Chiche L, Castro B, Boigegrain RA, Favel A, Coletti-Previero MA (1990) Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 72:431–435

    Article  PubMed  Google Scholar 

  • Nguyen PQ, Wang S, Kumar A, Yap LJ, Luu TT, Lescar J, Tam JP (2014) Discovery and characterization of pseudocyclic cystine-knot α-amylase inhibitors with high resistance to heat and proteolytic degradation. FEBS J 281:4351–4366

    Article  CAS  PubMed  Google Scholar 

  • Nguyen PQ, Luu TT, Bai Y, Nguyen GK, Pervushin K, Tam JP (2015) Allotides: proline-rich cystine knot α-amylase inhibitors from Allamanda cathartica. J Nat Prod 78:695–704

    Article  CAS  PubMed  Google Scholar 

  • Ntui VO, Thirukkumaran G, Azadi P, Khan RS, Nakamura I, Mii M (2010) 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 29:943–954

    Article  CAS  PubMed  Google Scholar 

  • Ntui VO, Azadi P, Thirukkumaran G, Khan RS, Chin DP, Nakamura I, Mii M (2011) Increased resistance to fusarium wilt in transgenic tobacco lines co-expressing chitinase and wasabi defensin genes. Plant Pathol 60:221–231

    Article  CAS  Google Scholar 

  • Ochoa-Zarzosa A, Loeza-Angeles H, Sagrero-Cisneros E, Villagómez-Gómez E, Lara-Zárate L, López-Meza JE (2008) Antibacterial activity of thionin Thi2.1 from Arabidopsis thaliana expressed by bovine endothelial cells against Staphylococcus aureus isolates from bovine mastitis. Vet Microbiol 127:425–430

    Article  CAS  PubMed  Google Scholar 

  • Odintsova TI, Vassilevski AA, Slavokhotova AA, Musolyamov AK, Finkina EI, Khadeeva NV, Rogozhin EA, Korostyleva TV, Pukhalsky VA, Grishin EV (2009) A novel antifungal hevein-type peptide from Triticum kiharae seeds with a unique 10-cysteine motif. FEBS J 276:4266–4275

    Article  CAS  PubMed  Google Scholar 

  • Osborn RW, De Samblanx GW, Thevissen K, Goderis I, Torrekens S, Van Leuven F, Attenborough S, Rees SB, Broekaert WF (1995) Isolation and characterisation of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae. FEBS Lett 368:257–262

    Article  CAS  PubMed  Google Scholar 

  • Padovan L, Scocchi M, Tossi A (2010) Structural aspects of plant antimicrobial peptides. Curr Protein Pept Sci 11:210–219

    Article  CAS  Google Scholar 

  • Pagnussat L, Burbach C, Baluška F, de la Canal L (2012) An extracellular lipid transfer protein is relocalized intracellularly during seed germination. J Experi Bot 63:6555–6563

    Article  CAS  Google Scholar 

  • Pallaghy PK, Norton RS, Nielsen KJ, Craik DJ (1994) A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci 3:1833–1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelegrini PB, Quirino BF, Franco OL (2007a) Plant cyclotides: an unusual class of defense compounds. Peptides 28:1475–1481

    Article  CAS  PubMed  Google Scholar 

  • Pelegrini PB, Quirino F, Franco OL (2007b) Plant cyclotides: an unusual class of defense compounds. Peptides 28:1475–1481

    Article  CAS  PubMed  Google Scholar 

  • Pelegrini PB, Lay FT, Murad AM, Anderson MA, Franco OL (2008) Novel insights on the mechanism of action of α-amylase inhibitors from the plant defensin family. Proteins 73:719–729

    Article  CAS  PubMed  Google Scholar 

  • Picart P, Pirttila AM, Raventos D, Kristensen HH, Sahl HG (2012) Identification of defensin-encoding genes of Piceaglauca: characterization of PgD5, a conserved spruce defensin with strong antifungal activity. BMC Plant Biol 12:180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinto MF, Fensterseifer IC, Migliolo L, Sousa DA, De Capdville G, Arboleda-Valencia JW, Colgrave ML, Craik DJ, Magalhães BS, Dias SC (2012) Identification and structural characterization of novel cyclotide with activity against an insect pest of sugar cane. J Biol Chem 287:134–147

    Article  CAS  PubMed  Google Scholar 

  • Pränting M, Lööv C, Burman R, Göransson U, Andersson DI (2010) The cyclotide cycloviolacin O2 from Viola odorata has potent bactericidal activity against Gram-negative bacteria. J Antimicrobial Chemoth 65:1964–1971

    Article  CAS  Google Scholar 

  • Ramana Rao M, Parameswari C, Sripriya R, Veluthambi K (2011) Transgene stacking and marker elimination in transgenic rice by sequential Agrobacterium-mediated co-transformation with the same selectable marker gene. Plant Cell Rep 30:1241–1252

    Article  CAS  PubMed  Google Scholar 

  • Regente MC, de la Canal L (2000) Purification, characterization and antifungal properties of a lipid-transfer protein from sunflower (Helianthus annuus) seeds. Physiol Plant 110:158–163

    Article  CAS  Google Scholar 

  • Rivero M, Furman N, Mencaccia N, Picca P, Toum L, Lentz E et al (2012) Stacking of antimicrobial genes in potato transgenic plants confers increased resistance to bacterial and fungal pathogens. J Biotechnol 157:334–343

    Article  CAS  PubMed  Google Scholar 

  • Rivillas-Acevedo LA, Soriano-Garcıa M (2007) Isolation and biochemical characterization of an antifungal peptide from Amaranthus hypochondriacus seeds. J Agric Food Chem 55:10156–10161

    Article  CAS  PubMed  Google Scholar 

  • Roy-Barman S, Sautter C, Chatto BB (2006) Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses. Trans Res 15:435–446

    Article  CAS  Google Scholar 

  • Sagaram US, Pandurangi R, Kaur J, Smith TJ, Shah DM (2011) Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS ONE 6(4):e18550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sales PM, Souza PM, Simeoni LA, Magalhães PO, Silveira D (2012) α-Amylase inhibitors: a review of raw material and isolated compounds from plant source. J Phar Pharma Sci 15:141–183

    Article  Google Scholar 

  • Sarowa S, kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) 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 28:419–427

    Article  CAS  Google Scholar 

  • Schröder JM (1999) Epithelial antimicrobial peptides: innate local host response elements. Cell Mol Life Sci 56:32–46

    Article  PubMed  Google Scholar 

  • Segura A, Moreno M, García-Olmedo F (1993) Purification and antipathogenic activity of lipid transfer proteins (LTPs) from the leaves of Arabidopsis and spinach. FEBS Lett 332:243–246

    Article  CAS  PubMed  Google Scholar 

  • Segura A, Moreno MA, Molina A, Garc´ıa-Olmedo F (1998) Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett 435:159–162

    Article  CAS  PubMed  Google Scholar 

  • Selitrennikoff CP (2001) Antifungal proteins. Appl Environ Microbiol 67:2883–2894

    Article  CAS  Google Scholar 

  • Silverstein KA, Graham MA, Paape TD, VandenBosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha M, Singh RP, Kushwaha GS, Iqbal N, Singh A, Kaushik S, Kaur P, Sharma S, Singh TP (2014) Current overview of allergens of plant pathogenesis related protein families. Sci World J 2014:543195

    Google Scholar 

  • Sitaram N (2006) Antimicrobial peptides with unusual amino acid compositions and unusual structures. Curr Med Chem 13:679–696

    Article  CAS  PubMed  Google Scholar 

  • Sjahril R, Chin DP, Khan RS, Yamamura S, Nakamura I, Amemiya Y, Mii M (2006) Transgenic Phalaenopsis plants with resistance to Erwinia carotovora produced by introducing wasabi defensin gene using Agrobacterium method. Plant Biotechnol 23:191–194

    Article  CAS  Google Scholar 

  • Stec B (2006) Plant thionins: the structural perspective. Cell Mol Life Sci 63:1370–1385

    Article  CAS  PubMed  Google Scholar 

  • Stec B, Markman O, Rao U, Heffron G, Henderson S, Vernon L, Brumfeld V, Teeter M (2004) Proposal for molecular mechanism of thionins deduced from physico-chemical studies of plant toxins. Chem Biol Drug Des 64:210–224

    CAS  Google Scholar 

  • Stotz HU, Thomson J, Wang Y (2009) Plant defensins: defense, development and application. Plant signal Behav 4:1010–1012

    Article  CAS  Google Scholar 

  • Takakura Y, Ito T, Saito H, Inoue T, Komari T, Kuwata S (2000) Flower predominant expression of a gene encoding a novel class I chitinase in rice (Oryza sativa L.). Plant Mol Biol 42:883–897

    Article  CAS  PubMed  Google Scholar 

  • Terras F, Schoofs H, De Bolle M, Van Leuven F, Rees SB, Vanderleyden J, Cammue B, Broekaert WF (1992a) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J Biol Chem 267:15301–15309

    CAS  PubMed  Google Scholar 

  • Terras FR, Goderis IJ, Van Leuven F, Vanderleyden J, Cammue BP, Broekaert WF (1992b) In vitro antifungal activity of a radish (Raphanus sativus L.) seed protein homologous to nonspecific lipid transfer proteins. Plant Physiol 100:1055–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terras FR, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, Rees SB, Torrekens S, Van Leuven F, Vanderleyden J (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thevissen K, Ghazi A, De Samblanx GW, Brownlee C, Osborn RW, Broekaert WF (1996) Fungal membrane responses induced by plant defensins and thionins. J Biol Chem 271:15018–15025

    Article  CAS  PubMed  Google Scholar 

  • Thevissen K, Terras FR, Broekaert WF (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65:5451–5458

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thevissen K, Cammue BP, Lemaire K, Winderickx J, Dickson RC, Lester RL, Ferket KK, Van Even F, Parret AH, Broekaert WF (2000) A gene encoding a sphingolipid biosynthesis enzyme determines the sensitivity of Saccharomyces cerevisiae to an antifungal plant defensin from dahlia (Dahlia merckii). Proc Natl Acad Sci USA 97:9531–9536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thevissen K, Warnecke DC, François IE, Leipelt M, Heinz E, Ott C, Zähringer U, Thomma BP, Ferket KK, Cammue BP (2004) Defensins from insects and plants interact with fungal glucosylceramides. J Biol Chem 6:3900–3905

    Article  Google Scholar 

  • Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216:193–202

    Article  CAS  PubMed  Google Scholar 

  • Van Den Bergh KP, Proost P, Van Damme J, Coosemans J, Van Damme EJ, Peumans WJ (2002) Five disulfide bridges stabilize a hevein-type antimicrobial peptide from the bark of spindle tree (Euonymus europaeus L.). FEBS Lett 530:181–185

    Article  PubMed  Google Scholar 

  • Wang SY, Wu JH, Ng TB, Ye YX, Rao PF (2004) A non-specific lipid transfer protein with antifungal and antibacterial activities from the mung bean. Peptides 25:1235–1242

    Article  CAS  PubMed  Google Scholar 

  • Wang CK, Colgrave ML, Ireland DC, Kaas Q, Craik DJ (2009a) Despite a conserved cystine knot motif, different cyclotides have different membrane binding modes. Biophys J 97:1471–1481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Rao P, Ye X (2009b) Isolation and biochemical characterization of a novel leguminous defense peptide with antifungal and antiproliferative potency. Appl Microbiol Biotechnol 82:79–86

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Zhang Y, Zhang W, Yuan S, Ng T, Ye X (2019) Purification of an antifungal peptide from seeds of Brassica oleracea var. gongylodes and investigation of its antifungal activity and mechanism of action. Molecules 24:1337

    Article  CAS  PubMed Central  Google Scholar 

  • Wei K, Zhong X (2014) Non-specific lipid transfer proteins in maize. BMC Plant Biol 14:281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijaya R, Neumann GM, Condron R, Hughes AB, Polya GM (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

    Article  CAS  PubMed  Google Scholar 

  • Wong JH, Ng TB (2005) Lunatusin, a trypsin-stable antimicrobial peptide from lima beans (Phaseolus lunatus L.). Peptides 26:2086–2092

    Article  CAS  PubMed  Google Scholar 

  • Wong JH, Xia L, Ng T (2007) A review of defensins of diverse origins. Curr Protein Pep Sci 8:446–459

    Article  CAS  Google Scholar 

  • Wong JH, Ip DCW, Ng TB, ChanYS Fang Fand, Pan WL (2012) A defensin-like peptide from Phaseolus vulgaris cv. “King Pole Bean”. Food Chem 135:408–414

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Sun J, Zhang G, Wang H, Ng TB (2011) An antifungal defensin from Phaseolus vulgaris cv. Cloud Bean. Phytomedicine 18:104–109

    Article  CAS  Google Scholar 

  • Xiang Y, Huang RH, Liu XZ, Zhang Y, Wang DC (2004) Crystal structure of a novel antifungal protein distinct with five disulfide bridges from Eucommia ulmoides Oliver at an atomic resolution. J Struct Biol 148:86–97

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Zhang H, Niu L, Wang X (2011) Efficient screening of a novel antimicrobial peptide from Jatropha curcas by cell membrane affinity chromatography. J Agric Food Chem 59:1145–1151

    Article  CAS  PubMed  Google Scholar 

  • Yamano A, Heo NH, Teeter MM (1997) Crystal structure of Ser-22/Ile-25 form crambin confirms solvent, side chain substate correlations. J Biol Chem 272:9597–9600

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Li J, Li X, She R, Pei Y (2006) Isolation andcharacterization of a novel thermostable non-specific lipidtransfer protein-like antimicrobial protein from motherwort(Leonurus japonicas Houtt) seeds. Peptides 27:3122–3128

    Article  CAS  PubMed  Google Scholar 

  • Yeats TH, Rose JK (2008) The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci 17:191–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokohama S, Iida Y, Kawasaki Y, Minami Y, Watanabe K, Yagi F (2009) The chitin-binding capability of Cy-AMP1 from cycad is essential to antifungal activity. J Pep Sci 15:492–497

    Article  CAS  Google Scholar 

  • Yu G, Du Hou X, Wang L, Wu H, Zhao L, Kong L, Wang H (2014) Identification of wheat non-specific lipid transfer proteins involved in chilling tolerance. Plant Cell Rep 33:1757–1766

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Song WY, Chen L, Ruan D, Taylor N, Ronald PC et al (1998) Transgenic elite indica rice varieties, resistant to Xanthomonas oryzae pv. oryzae. Mol Breed 4:551–558

    Article  CAS  Google Scholar 

  • Zhao J-Z et al (2003) Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat Biotechnol 21:1493–1497

    Article  CAS  PubMed  Google Scholar 

  • Zhao M, Ma Y, Pan YH, Zhang CH, Yuan WX (2011) A hevein-like protein and a class I chitinase with antifungal activity from leaves of the paper mulberry. Biomed Chrom 25:908–912

    Article  CAS  Google Scholar 

  • Zhao QC, Liu MH, Zhang XW, Lin CY, Zhang Q, Shen ZC (2015) Generation of insect-resistant and glyphosate-tolerant rice by introduction of a T-DNA containing two Bt insecticidal genes and an EPSPS gene. J Zhejiang Univ (Science B) 16:824–831

    Article  CAS  Google Scholar 

  • Zhu YJ, Agbayani R, Moore PH (2007) Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor. Planta 226:87–89

    Article  CAS  PubMed  Google Scholar 

  • Zottich U, Da Cunha M, CarvalhoAéO, Dias GB, Silva Nádia CM, Santos IS, do Nacimento VV, Miguel Eílio C, Machado OLT, Gomes VM (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 1810(4):375–383

    Article  CAS  PubMed  Google Scholar 

  • Zuidmeer L, Van Ree R (2007) Lipid transfer protein allergy: primary food allergy or pollen/food syndrome in some cases. Curr Opin Allerg Clin Immunol 7:269–273

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biotechnology, Abdul Wali Khan University Mardan, Mardan, Pakistan

    Aneela Iqbal, Raham Sher Khan, Kashmala Shehryar, Anum Imran, Faryal Ali & Syeda Attia

  2. Department of Agronomy, The University of Agriculture, Peshawar, Pakistan

    Shahen Shah

  3. Graduate School of Horticulture, Chiba University, Chiba, Japan

    Masahiro Mii

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  1. Aneela Iqbal
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  2. Raham Sher Khan
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  3. Kashmala Shehryar
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  4. Anum Imran
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  5. Faryal Ali
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  6. Syeda Attia
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  7. Shahen Shah
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  8. Masahiro Mii
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Contributions

AI, compiled headings and subheadings of the collected research articles, and wrote the manuscript with support from KS, AI, FA and SA. RSK, checked the manuscript time to time for improvement. SS, had a look on the manuscript for sequence of the headings and subheadings. MM, finally reviewed and approved for submission.

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Correspondence to Raham Sher Khan.

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Iqbal, A., Khan, R.S., Shehryar, K. et al. Antimicrobial peptides as effective tools for enhanced disease resistance in plants. Plant Cell Tiss Organ Cult 139, 1–15 (2019). https://doi.org/10.1007/s11240-019-01668-6

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