Advertisement

Antifungal Plant Defensins: Insights into Modes of Action and Prospects for Engineering Disease-Resistant Plants

  • Jagdeep Kaur
  • Siva LS Velivelli
  • Dilip Shah
Chapter

Abstract

Defensins are small, cysteine-rich peptides that are ubiquitously present in all plants. They are important components of the plant immune system and serve as first line of defense against invading pathogens. Plant defensins share conserved tetradisulfide connectivity but vary in their sequence, net charge, and hydrophobicity. A number of plant defensins with potent broad-spectrum antifungal activity have been identified and characterized. Studies conducted during the past decade have highlighted the diverse modes of action (MOA) of a few antifungal defensins. Constitutive expression of these defensins has been demonstrated to confer in planta resistance to several economically important fungal and oomycete pathogens in transgenic crops. Here, we provide a brief review of recent findings that have contributed to our current understanding of the MOA of these peptides and their deployment for disease resistance in crops.

Keywords

Plant defensins Antifungal activity Mode of action Fungal resistance Genetic engineering 

References

  1. Abebe T, Skadsen RW, Kaeppler HF (2005) A proximal upstream sequence controls tissue-specific expression of Lem2, a salicylate-inducible barley lectin-like gene. Planta 221:170–183CrossRefGoogle Scholar
  2. Abebe T, Skadsen R, Patel M, Kaeppler H (2006) The Lem2 gene promoter of barley directs cell- and development-specific expression of gfp in transgenic plants. Plant Biotechnol J 4:35–44CrossRefGoogle Scholar
  3. Aerts AM, François IEJA, Cammue BPA, Thevissen K (2008) The mode of antifungal action of plant, insect and human defensins. Cell Mol Life Sci 65:2069–2079CrossRefGoogle Scholar
  4. Baxter AA, Richter V, Lay FT, Poon IKH, Adda CG, Veneer PK, Phan TK, Bleackley MR, Anderson MA, Kvansakul M, Hulett MD (2015) The tomato defensin TPP3 binds phosphatidylinositol (4,5)-bisphosphate via a conserved dimeric cationic grip conformation to mediate cell lysis. Mol Cell Biol 35:1964–1978CrossRefGoogle Scholar
  5. Baxter AA, Poon IKH, Hulett MD (2017) The lure of the lipids: how defensins exploit membrane phospholipids to induce cytolysis in target cells. Cell Death Dis 8:e2712CrossRefGoogle Scholar
  6. Bleackley MR, Payne JAE, Hayes BME, Durek T, Craik DJ, Shafee TMA, Poon IKH, Hulett MD, van der Weerden NL, Anderson MA (2016) Nicotiana alata defensin chimeras reveal differences in the mechanism of fungal and tumour cell killing and an enhanced antifungal variant. Antimicrob Agents Chemother 60:6302–6312CrossRefGoogle Scholar
  7. Broekaert WF, Cammue BPA, De Bolle MFC, Thevissen K, De Samblanx GW, Osborn RW, Nielson K (1997) Antimicrobial peptides from plants. Crit Rev Plant Sci 16:297–323CrossRefGoogle Scholar
  8. Carvalho Ade O, Gomes VM (2009) Plant defensins-prospects for the biological functions and biotechnological properties. Peptides 30:1007–1020CrossRefGoogle Scholar
  9. Colilla FJ, Rocher A, Mendez E (1990) Gamma-purothionins: amino acid sequence of two polypeptides of a new family of thionins from wheat endosperm. FEBS Lett 270:191–194CrossRefGoogle Scholar
  10. Collinge DB, Jorgensen HJ, Lund OS, Lyngkjaer MF (2010) Engineering pathogen resistance in crop plants: current trends and future prospects. Annu Rev Phytopathol 48:269–291CrossRefGoogle Scholar
  11. Cools TL, Vriens K, Struyfs C, Verbandt S, Ramada MHS, Brand GD, Block C Jr, Koch B, Traven A, Drijfhout JW, Demuyser L, Kucharikova S, Van Dijck P, Spasic D, Lammertyn J, Cammune BPA, Thevissen K (2017) The antifungal plant defensin HsAFP1 is a phosphatidic acid-interacting peptide inducing membrane permeabilization. Front Microbiol 8:2295. https://doi.org/10.3389/fmicb.2017.02295 CrossRefPubMedPubMedCentralGoogle Scholar
  12. De Coninck B, Cammue BPA, Thevissen K (2013) Modes of antifungal action and in planta functions of plant defensins and defensin-like peptides. Fungal Biol Rev 26:109–120CrossRefGoogle Scholar
  13. El-Mounadi K, Islam KT, Hernández-Ortiz P, Read ND, Shah DM (2016) Antifungal mechanisms of a plant defensin MtDef4 are not conserved between the ascomycete fungi Neurospora crassa and Fusarium graminearum. Mol Microbiol 100:542–559CrossRefGoogle Scholar
  14. 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 18:1307–1310CrossRefGoogle Scholar
  15. Gaspar YM, McKenna JA, McGinness BS, Hinch J, Poon S, Connelly AA, Anderson MA, Heath RL (2014) Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J Exp Bot 65:1541–1550CrossRefGoogle Scholar
  16. Himmelbach A, Liu L, Zierold U, Altschmied L, Maucher H, Beier F, Müller D, Hensel G, Heise A, Schützendübel A, Kumlehn J, Schweizer P (2010) Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. Plant Cell 22:937–952CrossRefGoogle Scholar
  17. Hwang S-H, Lee IA, Yie SW, Hwang D-J (2008) Identification of an OsPR10a promoter region responsive to salicylic acid. Planta 227:1141–1150CrossRefGoogle Scholar
  18. Islam KT, Velivelli SLS, Berg RH, Oakley B, Shah DM (2017) A novel bi-domain plant defensin MtDef5 with potent broad-spectrum antifungal activity binds to multiple phospholipids and forms oligomers. Sci Rep 7:16157CrossRefGoogle Scholar
  19. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323CrossRefGoogle Scholar
  20. Kaur J, Sagaram US, Shah D (2011) Can plant defensins be used to engineer durable commercially useful fungal resistance in crop plants? Fungal Biol Rev 25:128–135CrossRefGoogle Scholar
  21. Kaur J, Thokala M, Robert-Seilaniantz A, Zhao P, Peyret H, Berg H, Pandey S, Jones J, Shah D (2012) Subcellular targeting of an evolutionarily conserved plant defensin MtDef4.2 determines the outcome of plant-pathogen interaction in transgenic Arabidopsis. Mol Plant Pathol 13:1032–1046CrossRefGoogle Scholar
  22. Kaur J, Fellers J, Adholeya A, Velivelli SL, El-Mounadi K, Nersesian N, Clemente T, Shah D (2017) 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 26:37–49CrossRefGoogle Scholar
  23. Kvansakul M, Lay FT, Adda CG, Veneer PK, Baxter AA, Phan TK, Poon IKH, Hulett MD (2016) Binding of phosphatidic acid by NsD7 mediates the formation of helical defensin-lipid oligomeric assemblies and membrane permeabilization. Proc Natl Acad Sci 113:11202–11207CrossRefGoogle Scholar
  24. Lay FT, Brugliera F, Anderson MA (2003) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131:1283–1293CrossRefGoogle Scholar
  25. Lay FT, Mills GD, Poon IK, Cowieson NP, Kirby N, Baxter AA, van der Weerden NL, Dogovski C, Perugini MA, Anderson MA, Kvansakul M, Hulett MD (2012) Dimerization of plant defensin NaD1 enhances its antifungal activity. J Biol Chem 287:19961–19972CrossRefGoogle Scholar
  26. Lay FT, Poon S, McKenna JA, Connelly AA, Barbeta BL, McGinness BS, Fox JL, Daly NL, Craik DJ, Heath RL, Anderson MA (2014) The C-terminal propeptide of a plant defensin confers cytoprotective and subcellular targeting functions. BMC Plant Biol 14:41CrossRefGoogle Scholar
  27. Liu W, Mazarei M, Rudis MR, Fethe MH, Stewart CN (2011) Rapid in vivo analysis of synthetic promoters for plant pathogen phytosensing. BMC Biotechnol 11:108–108CrossRefGoogle Scholar
  28. Lobo DS, Pereira IB, Fragel-Madeira L, Medeiros LN, Cabral LM, Faria J, Bellio M, Campos RC, Linden R, Kurtenbach E (2007) Antifungal Pisum sativumdefensin 1 interacts with Neurospora crassa Cyclin F related to the cell cycle. Biochemistry 46:987–996CrossRefGoogle Scholar
  29. Mendez E, Moreno A, Colilla F, Pelaez F, Limas GG, Mendez R, Soriano F, Salinas M, de Haro C (1990) Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, gamma-hordothionin, from barley endosperm. Eur J Biochem 194:533–539CrossRefGoogle Scholar
  30. Munoz A, Chu M, Marris PI, Sagaram US, Kaur J, Shah DM, Read ND (2014) Specific domains of plant defensins differentially disrupt colony initiation, cell fusion and calcium homeostasis in Neurospora crassa. Mol Microbiol 92:1357–1374CrossRefGoogle Scholar
  31. Poon IKH, Baxter AA, Lay FT, Mills GD, Adda CG, Payne JAE, Phan TK, Ryan GF, White JA, Veneer PK, van der Weerden NL, Anderson MA, Kvansakul M, Hulett MD (2014) Phosphoinositide-mediated oligomerization of a defensin induces cell lysis. elife 3:e01808CrossRefGoogle Scholar
  32. Portieles R, Ayra C, Gonzalez E, Gallo A, Rodriguez R, Chacon O, Lopez Y, Rodriguez M, Castillo J, Pujol M, Enriquez G, Borroto C, Trujillo L, Thomma BP, Borras-Hidalgo O (2010) NmDef02, a novel antimicrobial gene isolated from Nicotiana megalosiphon confers high-level pathogen resistance under greenhouse and field conditions. Plant Biotechnol J 8:678–690CrossRefGoogle Scholar
  33. Sagaram US, El-Mounadi K, Buchko GW, Berg HR, Kaur J, Pandurangi RS, Smith TJ, Shah DM (2013) Structural and functional studies of a phosphatidic acid-binding antifungal plant defensin MtDef4: identification of an RGFRRR motif governing fungal cell entry. PLoS One 8(12):e82485CrossRefGoogle Scholar
  34. Sharma KK, Pothana A, Prasad K, Shah D, Kaur J, Bhatnagar D, Chen ZY, Raruang Y, Cary JW, Rajasekaran K, Sudini HK, Bhatnagar-Mathur P (2017) Peanuts that keep aflatoxin at bay: a threshold that matters. Plant Biotechnol J 16:1024. https://doi.org/10.1111/pbi.12846 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Spelbrink RG, Dilmac N, Allen A, Smith TJ, Shah DM, Hockerman GH (2004) Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiol 135:2055–2067CrossRefGoogle Scholar
  36. Thakare D, Zhang J, Wing RA, Cotty PJ, Schmidt MA (2017) Aflatoxin-free transgenic maize using host-induced gene silencing. Sci Adv 3:e1602382CrossRefGoogle Scholar
  37. 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 271:15018–15025CrossRefGoogle Scholar
  38. Thevissen K, Osborn RW, Acland DP, Broekaert WF (1997) Specific, high affinity binding sites for an antifungal plant defensin on Neurospora crassahyphae and microsomal membranes. J Biol Chem 272:32176–32181CrossRefGoogle Scholar
  39. Thevissen K, Terras FRG, Broekaert WF (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65:5451–5458PubMedPubMedCentralGoogle Scholar
  40. 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 U S A 97:9531–9536CrossRefGoogle Scholar
  41. Thevissen K, François IEJA, Takemoto JY, Ferket KKA, Meert EM, Cammue BPA (2003) DmAMP1, an antifungal palnt defensins from dahlia (Dahlia merckii), interats with sphingolipids from Saccharomyces cerevisiae. FEMS Microbiol Lett 226:169–173CrossRefGoogle Scholar
  42. Thevissen K, Warnecke DC, François IEJA, Leipelt M, Heinz E, Ott C, Zähringer U, Thomma BPHJ, Ferket KKA, Cammue BPA (2004) Defensins from insects and plants interact with fungal glucosylceramides. J Biol Chem 279:3900–3905CrossRefGoogle Scholar
  43. Thevissen K, Francois IE, Aerts AM, Cammue BP (2005) Fungal sphingolipids as targets for the development of selective antifungal therapeutics. Curr Drug Targets 6:923–928CrossRefGoogle Scholar
  44. Thevissen K, Francois IE, Winderickx J, Pannecouque C, Cammue BP (2006) Ceramide involvement in apoptosis and apoptotic diseases. Mini Rev Med Chem 6:699–709CrossRefGoogle Scholar
  45. Thevissen K, Kristensen H-H, Thomma BPHJ, Cammue BPA, François IEJA (2007) Therapeutic potential of antifungal plant and insect defensins. Drug Discov Today 12:966–971CrossRefGoogle Scholar
  46. Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216(2):193–202CrossRefGoogle Scholar
  47. van der Weerden NL, Lay FT, Anderson MA (2008) The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J Biol Chem 283:14445–14452CrossRefGoogle Scholar
  48. van der Weerden NL, Hancock REW, Anderson MA (2010) Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J Biol Chem 285:37513–37520CrossRefGoogle Scholar
  49. van der Weerden NL, Bleackley MR, Anderson MA (2013) Properties and mechanisms of action of naturally occurring antifungal peptides. Cell Mol Life Sci CMLS 70:3545–3570CrossRefGoogle Scholar
  50. Vriens K, Peigneur S, De Coninck B, Tytgat J, Cammue BPA, Thevissen K (2016) The antifungal plant defensin AtPDF2.3 from Arabidopsis thaliana blocks potassium channels. Sci Rep 6:32121CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Donald Danforth Plant Science CenterSt. LouisUSA
  2. 2.Monsanto CompanyChesterfieldUSA

Personalised recommendations