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A synthetic antimicrobial peptide BTD-S expressed in Arabidopsis thaliana confers enhanced resistance to Verticillium dahliae

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Abstract

BTD-S is a synthetic non-cyclic θ-defensin derivative which was previously designed in our laboratory based on baboon θ-defensins (BTDs). It shows robust antimicrobial activity against economically important phytopathogen, Verticillium dahliae. Here, we deduced the coding nucleotide sequence of BTD-S and introduced the gene into wild-type (ecotype Columbia-0) Arabidopsis thaliana plants. Results demonstrated that BTD-S-transgenic lines displayed in bioassays inhibitory effects on the growth of V. dahliae in vivo and in vitro. Based on symptom severity, enhanced resistance was found in a survey of BTD-S-transgenic lines. Besides, crude protein extracts from root tissues of BTD-S-transformed plants significantly restricted the growth of fungal hyphae and the germination of conidia. Also, fungal biomass over time determined by real-time PCR demonstrated the overgrowth of V. dahliae in wild-type plants 2–3 weeks after inoculation, while almost no fungal DNA was detected in aerial tissues of their transgenic progenitors. The result suggested that fungus failed to invade and progress acropetally up to establish a systemic infection in BTD-S-transgenic plants. Moreover, the assessment of basal defense responses was performed in the leaves of WT and BTD-S-transgenic plants. The mitigated oxidative stress and low antioxidase level in BTD-S-transgenic plants revealed that BTD-S acts via permeabilizing target microbial membranes, which is in a category different from hypersensitive response-dependent defense. Taken together, our results demonstrate that BTD-S is a promising gene to be explored for transgenic engineering for plant protection against Verticillium wilt.

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References

  • 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 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  • Beringer PM, Bensman TJ, Ho H, Agnello M, Denovel N, Nguyen A, Wong-Beringer A, She R, Tran DQ, Moskowitz SM, Selsted ME (2016) Rhesus θ-defensin-1 (RTD-1) exhibits in vitro and in vivo activity against cystic fibrosis strains of Pseudomonas aeruginosa. J Antimicrob Chemother 71:181–188

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brogden KA, Ackermann M, McCray PB, Tack BF (2003) Antimicrobial peptides in animals and their role in host defences. Int J Antimicrob Agents 22:465–478

    Article  CAS  PubMed  Google Scholar 

  • Brown JK (2002) Yield penalties of disease resistance in crops. Curr Opin Plant Biol 5:339–344

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Xiaohong H, Mo J, Sun Q, Yang J, Liu J (2009) Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: a review. Afr J Biotechnol 8:7363–7372

    CAS  Google Scholar 

  • Chandrashekhara Niranjan-Raj S, Deepak S, Manjunath G, Shekar Shetty H (2010) Thionins (PR protein-13) mediate pearl millet downy mildew disease resistance. Arch Phytopathol Plant Protect 43:1356–1366

    Article  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Coca M, Peñas G, Gómez J, Campo S, Bortolotti C, Messeguer J, San Segundo B (2006) Enhanced resistance to the rice blast fungus Magnaporthe grisea conferred by expression of a cecropin A gene in transgenic rice. Planta 223:392–406

    Article  CAS  PubMed  Google Scholar 

  • Conibear AC, Craik DJ (2014) The chemistry and biology of theta defensins. Angew Chem Int Ed 53:10612–10623

    Article  CAS  Google Scholar 

  • Conibear AC, Rosengren KJ, Daly NL, Henriques ST, Craik DJ (2013) The cyclic cystine ladder in θ-defensins is important for structure and stability, but not antibacterial activity. J Biol Chem 288:10830–10840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conibear AC, Bochen A, Rosengren KJ, Stupar P, Wang C, Kessler H, Craik DJ (2014) The cyclic cystine ladder of theta-defensins as a stable, bifunctional scaffold: a proof-of-concept study using the integrin-binding RGD Motif. Chembiochem 15:451–459

    Article  CAS  PubMed  Google Scholar 

  • Daud MK, Sun Y, Dawood M, Hayat Y, Variath MT, Wu Y, Mishkat U, Najeeb U, Zhu S (2009) Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463–473

    Article  CAS  PubMed  Google Scholar 

  • De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem 41:863–870

    Article  Google Scholar 

  • Deshmukh SD, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci 103:18450–18457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474

    Google Scholar 

  • Egley GH, Paul RN Jr, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water-impermeable seed coats in Sida spinosa L. Planta 157:224–232

    Article  CAS  PubMed  Google Scholar 

  • Ellendorff U, Fradin EF, De Jonge R, Thomma BP (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 60:591–602

    Article  CAS  PubMed  Google Scholar 

  • Emani C, Garcia JM, Lopata Finch E, Pozo MJ, Uribe P, Kim DJ, Sunilkumar G, Cook DR, Kenerley CM, Rathore KS (2003) Enhanced fungal resistance in transgenic cotton expressing an endochitinase gene from Trichoderma virens. Plant Biotechnol J 1:321–336

    Article  CAS  PubMed  Google Scholar 

  • Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7:71–86

    Article  CAS  PubMed  Google Scholar 

  • Gallo SA, Wang W, Rawat SS, Jung G, Waring AJ, Cole AM, Lu H, Yan X, Daly NL, Craik DJ (2006) θ-defensins prevent HIV-1 Env-mediated fusion by binding gp41 and blocking 6-helix bundle formation. J Biol Chem 281:18787–18792

    Article  CAS  PubMed  Google Scholar 

  • Gao A, 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 

  • Gayoso C, Pomar F, Novo-Uzal E, Merino F, de Ilárduya ÓM (2010) The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol 10:232–251

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibeaut DM, Hulett J, Cramer GR, Seemann JR (1997) Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiol 115:317–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillon AD, Saska I, Jennings CV, Guarino RF, Craik DJ, Anderson MA (2008) Biosynthesis of circular proteins in plants. Plant J 53:505–515

    Article  CAS  PubMed  Google Scholar 

  • Goyal RK, Mattoo AK (2014) Multitasking antimicrobial peptides in plant development and host defense against biotic/abiotic stress. Plant Sci 228:135–149

    Article  CAS  PubMed  Google Scholar 

  • Goyal RK, Hancock RE, Mattoo AK, Misra S (2013) Expression of an engineered heterologous antimicrobial peptide in potato alters plant development and mitigates normal abiotic and biotic responses. PLoS One 8:e77505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guaní-Guerra E, Santos-Mendoza T, Lugo-Reyes SO, Terán LM (2010) Antimicrobial peptides: general overview and clinical implications in human health and disease. Clin Immunol 135:1–11

    Article  PubMed  Google Scholar 

  • Gupta P, Lackman-Smith C, Snyder B, Ratner D, Rohan LC, Patton D, Ramratnam B, Cole AM (2013) Antiviral activity of retrocyclin RC-101, a candidate microbicide against cell-associated HIV-1. AIDS Res Hum Retrov 29:391–396

    CAS  Google Scholar 

  • Hayes BM, Bleackley MR, Wiltshire JL, Anderson MA, Traven A, van der Weerden NL (2013) Identification and mechanism of action of the plant defensin NaD1 as a new member of the antifungal drug arsenal against Candida albicans. Antimicrob Agents Ch 57:3667–3675

    Article  CAS  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Díaz RM, Cirulli M, Bubici G, Del Mar Jiménez-Gasco M, Antoniou PP, Tjamos EC (2012) Verticillium wilt, a major threat to olive production: current status and future prospects for its management. Plant Dis 96:304–329

    Article  Google Scholar 

  • Karademir E, Karademir C, Ekinci R, Baran B, SAĞIR A (2010) Assessment of tolerance level of some Cotton (Gossypium hirsutum L.) varieties against Verticillium wilt (Verticillium dahliae Kleb.) disease. Not Bot Horti Agrobot 38:196–202

    Google Scholar 

  • Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiol 155:780–790

    Article  CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48:251–275

    Article  CAS  Google Scholar 

  • Lan Y, Ye Y, Kozlowska J, Lam JK, Drake AF, Mason AJ (2010) Structural contributions to the intracellular targeting strategies of antimicrobial peptides. BBA Biomembr 1798:1934–1943

    Article  CAS  Google Scholar 

  • Lehrer RI, Cole AM, Selsted ME (2012) θ-Defensins: cyclic peptides with endless potential. J Biol Chem 287:27014–27019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Zhu Y, Xie C, Jue D, Hong Y, Chen M, Hubdar AK, Yang Q (2012) Transgenic potato plants expressing StoVe1 exhibit enhanced resistance to Verticillium dahliae. Plant Mol Biol Rep 30:1–8

    Article  Google Scholar 

  • Lu Z, Zhang Z, Su Y, Liu C, Shi G (2013) Cultivar variation in morphological response of peanut roots to cadmium stress and its relation to cadmium accumulation. Ecotoxicol Environ Saf 91:147–155

    Article  CAS  PubMed  Google Scholar 

  • Malcolm GM, Kuldau GA, Gugino BK, Jiménez-Gasco MDM (2013) Hidden host plant associations of soilborne fungal pathogens: an ecological perspective. Phytopathol 103:538–544

    Article  CAS  Google Scholar 

  • Marcos JF, Muñoz A, Pérez-Payá E, Misra S, López-García B (2008) Identification and rational design of novel antimicrobial peptides for plant protection. Annu Rev Phytopathol 46:273–301

    Article  CAS  PubMed  Google Scholar 

  • Maskin L, Gudesblat GE, Moreno JE, Carrari FO, Frankel N, Sambade A, Rossi M, Iusem ND (2001) Differential expression of the members of the Asr gene family in tomato (Lycopersicon esculentum). Plant Sci 161:739–746

    Article  CAS  Google Scholar 

  • Meyer P (1995) Understanding and controlling transgene expression. Trends Biotechnol 13:332–337

    Article  CAS  Google Scholar 

  • Miao W, Wang X, Li M, Song C, Wang Y, Hu D, Wang J (2010) Genetic transformation of cotton with a harpin-encoding gene hpaXoo confers an enhanced defense response against different pathogens through a priming mechanism. BMC Plant Biol 10:67

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Montesinos E, Bardaji E (2008) Synthetic antimicrobial peptides as agricultural pesticides for plant-disease control. Chem Biodivers 5:1225–1237

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Murray F, Llewellyn D, McFadden H, Last D, Dennis ES, Peacock WJ (1999) Expression of the Talaromyces flavus glucose oxidase gene in cotton and tobacco reduces fungal infection, but is also phytotoxic. Mol Breed 5:219–232

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nanni V, Schumacher J, Giacomelli L, Brazzale D, Sbolci L, Moser C, Tudzynski P, Baraldi E (2014) VvAMP2, a grapevine flower-specific defensin capable of inhibiting Botrytis cinerea growth: insights into its mode of action. Plant Pathol 63:899–910

    Article  CAS  Google Scholar 

  • Nawrot R, Barylski J, Nowicki G, Broniarczyk J, Buchwald W, Goździcka-Józefiak A (2014) Plant antimicrobial peptides. Folia Microbiol 59:181–196

    Article  CAS  Google Scholar 

  • Nguyen GKT, Lim WH, Nguyen PQT, Tam JP (2012) Novel cyclotides and uncyclotides with highly shortened precursors from Chassalia chartacea and effects of methionine oxidation on bioactivities. J Biol Chem 287:17598–17607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen GKT, Lian Y, Pang EWH, Nguyen PQT, Tran TD, Tam JP (2013) Discovery of linear cyclotides in monocot plant Panicum laxum of Poaceae family provides new insights into evolution and distribution of cyclotides in plants. J Biol Chem 288:3370–3380

    Article  CAS  PubMed  Google Scholar 

  • Ni M, Zhao Y, Bibi N, Shao M, Yuan S, Fan K, Zhang G, Li F, Wang X (2013) A non-cyclic baboon θ-defensin derivative exhibiting antimicrobial activity against the phytopathogen Verticillium dahliae. Appl Microbiol Biotechnol 97:2043–2052

    Article  CAS  PubMed  Google Scholar 

  • Ong ZY, Wiradharma N, Yang YY (2014) Strategies employed in the design and optimization of synthetic antimicrobial peptide amphiphiles with enhanced therapeutic potentials. Adv Drug Deliv Rev 78:28–45

    Article  CAS  PubMed  Google Scholar 

  • Parkhi V, Kumar V, Campbell LM, Bell AA, Shah J, Rathore KS (2010) Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res 19:959–975

    Article  CAS  PubMed  Google Scholar 

  • Pegg GF, Brady BL (2002) Verticillium wilts. CABI Publishing, Wallingford, p 552

    Book  Google Scholar 

  • Prenner EJ, Lewis RN, McElhaney RN (1999) The interaction of the antimicrobial peptide gramicidin S with lipid bilayer model and biological membranes. BBA Biomembr 1462:201–221

    Article  CAS  Google Scholar 

  • Rajasekaran K, Cary JW, Jaynes JM, Cleveland TE (2005) Disease resistance conferred by the expression of a gene encoding a synthetic peptide in transgenic cotton (Gossypium hirsutum L.) plants. Plant Biotechnol J 3:545–554

    Article  CAS  PubMed  Google Scholar 

  • Ralhan A, Schöttle S, Thurow C, Iven T, Feussner I, Polle A, Gatz C (2012) The vascular pathogen Verticillium longisporum requires a jasmonic acid-independent COI1 function in roots to elicit disease symptoms in Arabidopsis shoots. Plant Physiol 159:1192–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao KM, Sresty T (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rivero M, Furman N, Mencacci N, Picca P, Toum L, Lentz E, Bravo-Almonacid F, Mentaberry A (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 

  • Saska I, Gillon AD, Hatsugai N, Dietzgen RG, Hara-Nishimura I, Anderson MA, Craik DJ (2007) An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J Biol Chem 282:29721–29728

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Won H, Kim J, Mishig-Ochir T, Lee B (2012) Antimicrobial peptides for therapeutic applications: a review. Molecules 17:12276–12286

    Article  CAS  PubMed  Google Scholar 

  • Su Z, Mao L, Li N, Feng X, Yuan Z, Wang L, Lin F, Zhang C (2013) Evidence for biotrophic lifestyle and biocontrol potential of dark septate endophyte Harpophora oryzae to rice blast disease. PLoS One 8:e61332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang YQ, Yuan J, Ösapay G, Ösapay K, Tran D, Miller CJ, Ouellette AJ, Selsted ME (1999) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated α-defensins. Science 286:498–502

    Article  CAS  PubMed  Google Scholar 

  • Thordal Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    Article  CAS  PubMed  Google Scholar 

  • Tran D, Tran PA, Tang Y, Yuan J, Cole T, Selsted ME (2002) Homodimeric θ-Defensins from Rhesus macaque Leukocytes: isolation, synthesis, antimicrobial activities, and bacterial binding properties of the cyclic peptides. J Biol Chem 277:3079–3084

    Article  CAS  PubMed  Google Scholar 

  • Tran D, Tran P, Roberts K, Ösapay G, Schaal J, Ouellette A, Selsted ME (2008) Microbicidal properties and cytocidal selectivity of rhesus macaque theta defensins. Antimicrob Agents Chemother 52:944–953

    Article  CAS  PubMed  Google Scholar 

  • Vanacker H, Carver TL, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. Plant J 35:574–587

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806–4816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wimley WC, Hristova K (2011) Antimicrobial peptides: successes, challenges and unanswered questions. J Membr Biol 239:27–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Won H, Jung S, Kim HE, Seo M, Lee B (2004) Systematic peptide engineering and structural characterization to search for the shortest antimicrobial peptide analogue of gaegurin 5. J Biol Chem 279:14784–14791

    Article  CAS  PubMed  Google Scholar 

  • Xia XJ, Zhou YH, Ding J, Shi K, Asami T, Chen Z, Yu JQ (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol 191:706–720

    Article  CAS  PubMed  Google Scholar 

  • Xing H, Lawrence CB, Chambers O, Davies HM, Everett NP, Li QQ (2006) Increased pathogen resistance and yield in transgenic plants expressing combinations of the modified antimicrobial peptides based on indolicidin and magainin. Planta 223:1024–1032

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 62:5607–5621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasin B, Wang W, Pang M, Cheshenko N, Hong T, Waring AJ, Herold BC, Wagar EA, Lehrer RI (2004) θ-defensins protect cells from infection by herpes simplex virus by inhibiting viral adhesion and entry. J Virol 78:5147–5156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang X, Yang S, Chi J, Zhang G, Ma Z (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30:2085–2096

    Article  CAS  PubMed  Google Scholar 

  • Zhao P, Zhao Y, Jin Y, Zhang T, Guo H (2014) Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein Cell 5:94–98

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank Prof. Zhigang Zhou of College of Fisheries and Life Science, Shanghai Ocean University, China for kindly providing the Arabidopsis (Col-0) seeds transformed with empty vector pCAMBIA 1301.

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  1. Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Feng Li, Hao Shen, Ming Wang, Kai Fan, Noreen Bibi, Mi Ni, Shuna Yuan & Xuede Wang

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Correspondence to Xuede Wang.

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This work was financially supported by the National Natural Science Foundation of China (31171616 and 31471567) and the Public Technology Application Research Project of Zhejiang Province (2014C32007).

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Li, F., Shen, H., Wang, M. et al. A synthetic antimicrobial peptide BTD-S expressed in Arabidopsis thaliana confers enhanced resistance to Verticillium dahliae . Mol Genet Genomics 291, 1647–1661 (2016). https://doi.org/10.1007/s00438-016-1209-9

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