Skip to main content
SpringerLink
Log in

New proteins orthologous to cerato-platanin in various Ceratocystis species and the purification and characterization of cerato-populin from Ceratocystis populicola

  • Biotechnologically relevant enzymes and proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Natural variants of cerato-platanin (CP), a pathogen associated molecular pattern (PAMP) protein produced by Ceratocystis platani (the causal agent of the plane canker stain), have been found to be produced by other four species of the genus Ceratocystis, including five clones of Ceratocystis fimbriata isolated from different hosts. All these fungal strains were known to be pathogenic to plants with considerable importance in agriculture, forestry, and as ornamental plants. The putative premature proteins were deduced on the basis of the nucleotide sequence of genes orthologous to the cp gene of C. platani; the deduced premature proteins of Ceratocystis populicola and Ceratocystis variospora reduced the total identity of all the others from 87.3% to 60.3%. Cerato-populin (Pop1), the CP-orthologous protein produced by C. populicola, was purified and characterized. Pop1 was a well-structured α/β protein with a different percentage of the α-helix than CP, and it self-assembled in vitro in ordered aggregates. Moreover, Pop1 behaved as PAMP, since it stimulated poplar leaf tissues to activate defence responses able to reduce consistently the C. populicola growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson M, Bocharova OV, Makarava N, Breydo L, Salnikov VV, Baskakov IV (2006) Polymorphism and ultrastructural organization of prion protein amyloid fibrils: an insight from high resolution atomic force microscopy. J Mol Biol 358:580–596

    Article  CAS  PubMed  Google Scholar 

  • Baker CJ, Harrington TC, Krauss U, Alfenas AC (2003) Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata. Phytopatology 93:1274–1284

    Article  CAS  Google Scholar 

  • Barnes I, Gaur A, Burgess T, Roux J, Wingfield BD, Wingfield MJ (2001) Microsatellite markers reflect similar relationship between isolates of the vascular wilt and canker pathogen Ceratocystis fimbriata. Mol Plant Path 2:319–325

    Article  CAS  Google Scholar 

  • Bennici A, Calamassi R, Pazzagli L, Comparini C, Schiff S, Bovelli R, Mori B, Tani C, Scala A (2005) Cytological and ultrastructural responses of Platanus acerifolia (Ait.) Willd. leaves to cerato-platanin, a protein from Ceratocystis fimbriata f. sp. platani. Phytopathol Mediterr 44:153–161

    Google Scholar 

  • Benson JR, Hare PE (1975) o-Phthalaldehyde: fluorogenic detection of primary amines in the picomole range. Comparison with fluorescamine and ninhydrin. Proc Natl Acad Sci USA 72:619–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436

    Article  CAS  PubMed  Google Scholar 

  • Boddi S, Comparini C, Calamassi R, Pazzagli L, Cappugi G, Scala A (2004) Cerato-platanin protein is located in the cell walls of ascospores, conidia and hyphae of Ceratocystis fimbriata f. sp. platani. FEMS Microbiol Lett 233:341–346

    Article  CAS  PubMed  Google Scholar 

  • Carresi L, Pantera B, Zoppi C, Cappugi G, Oliveira AL, Pertinhez TA, Spisni A, Scala A, Pazzagli (2006) Cerato-platanin, a phytotoxic protein from Ceratocystis fimbriata: expression in Pichia pastoris, purification and characterization. Protein Expr Purif 49:159–167

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366

    Article  CAS  PubMed  Google Scholar 

  • Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact 19:838–853

    Article  CAS  PubMed  Google Scholar 

  • Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelbrecht CJB, Harrington TA (2005) Intersterility, morphology and taxonomy of Ceratocystis fimbriata on sweet potato, cacao and sycamore. Mycologia 97:57–69

    Article  PubMed  Google Scholar 

  • Engelbrecht CJB, Harrington TC, Steimel J, Capretti P (2004) Genetic variation in eastern North American and putatively introduced populations of Ceratocystis fimbriata f. platani. Mol Ecol 13:2995–3005

    Article  CAS  PubMed  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut JS, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Research, Database Issue 36:D281–D288

    Article  CAS  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Fontana F, Santini A, Salvini M, Pazzagli L, Cappugi G, Scala A, Durante M, Bernardi R (2008) Cerato-platanin treated plane leaves restrict Ceratocystis platani growth and overexpress defence-related genes. J Plant Pathol 90:295–306

    CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Gressel J, Meir S, Herschkovitz Y, Al-Ahmad H, Greenspoon I, Olubukola B, Amsellem Z (2007) Approaches to and successes in developing transgenically enhanced mycoherbicides. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. Springer Netherlands, Amsterdam, pp 297–305

    Chapter  Google Scholar 

  • Hamberger B, Ellis M, Friedmann M, de Azevedo Souza C, Barbazuk B, Douglas CJ (2007) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201

    Article  CAS  Google Scholar 

  • Jeong JS, Mitchell TK, Dean RA (2007) The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence. FEMS Microbiol Lett 273:157–165

    Article  CAS  PubMed  Google Scholar 

  • Johnson JA, Harrington TC, Engelbrecht C (2005) Phylogeny and taxonomy of the North American clade of the Ceratocystis fimbriata complex. Mycologia 97:1067–1092

    Article  CAS  PubMed  Google Scholar 

  • Krebs MR, MacPhee CE, Miller AF, Dunlop IE, Dobson CM, Donald AM (2004) The formation of spherulites by amyloid fibrils of bovine insulin. Proc Natl Acad Sci USA 101:14420–14424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28:118–121

    Article  CAS  PubMed  Google Scholar 

  • Kurup VP, Banerjee B, Hemmann S, Greenberger PA, Blaser K, Crameri R (2000) Selected recombinant Aspergillus fumigatus allergens bind specifically to IgE in ABPA. Clin Exp Allergy 30:988–993

    Article  CAS  PubMed  Google Scholar 

  • Kwan AH, Winefield RD, Sunde M, Matthews JM, Haverkamp RG, Templeton MD, Mackay JP (2006) Structural basis for rodlet assembly in fungal hydrophobins. Proc Natl Acad Sci USA 103:3621–3626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Laemnli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  Google Scholar 

  • LeVine H (1999) Quantification of the β-sheet amyloid fibril structures with Thioflavin T. Method Enzymol 309:274–284

    Article  CAS  Google Scholar 

  • Mao FL, Su ZC, Olman V, Dam P, Liu ZJ, Xu YN (2006) Mapping of orthologous genes in the context of biological pathways: an application of integer programming. Proc Natl Acad Sci USA 103:129–134

    Article  CAS  PubMed  Google Scholar 

  • Marcos JF, Mũnoz A, Pérez-Payá E, Misra S, Lopez-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 

  • Ocasio-Morales RG, Tsopelas P, Harrington TA (2007) Origin of Ceratocystis platani on native Platanus orientalis in Greece and its impact on natural forests. Plant Dis 91:901–904

    Article  PubMed  Google Scholar 

  • Oliveira AL, Pazzagli L, Pantera B, Cappugi G, Benedetti CE, Spisni A, Pertinhez TA (2006) 1H, 15N and 13C resonance assignments of cerato-platanin, a phytotoxic protein from Ceratocystis fimbriata. J Biomol NMR 36:50

    Article  PubMed  Google Scholar 

  • Oliveira AL, Pazzagli L, Cappugi G, Scala A, Gallo M, Cicero DO, Pantera B, Spisni A, Benedetti CE, Pertinhez TA (2009) The solution structure of cerato-platanin reveals a new fold among the protein fungal elicitors. ChemBioChem, submitted

  • Pan S, Cole GT (1995) Molecular and biochemical characterization of a Coccidoides immitis-specific antigen. Infect Immun 63:3994–4002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panconesi A (1999) Canker stain of plane trees: a serious danger to urban plantings in Europe. J Plant Pathol 81:3–15

    Google Scholar 

  • Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, Scala A (1999) Purification of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. J Biol Chem 274:24959–24964

    Article  CAS  PubMed  Google Scholar 

  • Pazzagli L, Pantera B, Carresi L, Zoppi C, Pertinhez TA, Spisni A, Tegli S, Scala A, Cappugi G (2006) Cerato-platanin, the first member of a new fungal protein family: cloning, expression and characterization. Cell Biochem Biophys 44:512–521

    Article  CAS  PubMed  Google Scholar 

  • Pontis RE (1951) A canker disease of the coffee tree in Colombia and Venezuela. Phytopathology 41:178–184

    Google Scholar 

  • Santini A, Capretti P (2000) Analysis of the Italian population of Ceratocystis fimbriata f. sp. platani using RAPD and minisatellite markers. Plant Pathol 49:461–467

    Article  CAS  Google Scholar 

  • Sbrana F, Bongini L, Cappugi G, Fanelli D, Guarino A, Pazzagli L, Scala A, Vassalli M, Zoppi C, Tiribilli B (2007) Atomic force microscopy images suggest aggregation mechanism in cerato-platanin. Eur Biophys J Biophy 36:727–732

    Article  CAS  Google Scholar 

  • Scala A, Tegli S, Comparini C, Mittempergher L, Scala F, Del Sorbo G (1994) Influence of fungal inoculum on cerato-ulmin production, purification of cerato-ulmin and detection in elm sucker cuttings. Petria 4:53–63

    Google Scholar 

  • Scala F, Bertelli E, Coppola L, Del Sorbo G, Tegli S, Scala A (1997) Comparative determination of cerato-ulmin on cell surface and in mycelial extracts of pathogenic and non-pathogenic Ophiostoma species. Mycol Res 101:829–834

    Article  Google Scholar 

  • Scala A, Pazzagli L, Comparini C, Santini A, Tegli S, Cappugi G (2004) Cerato-platanin, an early-produced protein by Ceratocystis fimbriata f. sp. platani, elicits phytoalexin synthesis in host and non-host plants. J Plant Pathol 86:23–29

    Google Scholar 

  • Seidl V, Marchetti M, Schandl R, Allmaier G, Kubicek CP (2006) Epl1, the major secreted protein of Hypocrea atroviridis on glucose, is a member of a strongly conserved protein family comprising plant defense response elicitors. FEBS J 273:4346–4359

    Article  CAS  PubMed  Google Scholar 

  • Sharen AL, Krupinski G (1970) Cultural and inoculation studies of Septoria nodorum, cause of Glume Blotch of wheat. Phytopathology 60:1480–1485

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Templeton MD, Rikkerink EHA, Beever RE (1994) Small, cysteine-rich proteins and recognition in fungal–plant interactions. Mol Plant-Microbe Interact 7:320–325

    Article  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Van Wyk M, Al Adawi AO, Khan IA, Deadman ML, Al Jahwari AA, Wingfield BD, Ploetz R, Wingfield MJ (2007) Ceratocystis manginecans sp. nov., causal agent of a destructive mango wilt disease in Oman and Pakistan. Fungal Divers 27:213–230

    Google Scholar 

  • Vargas WA, Djonovic S, Sukno SA, Kenerley CM (2008) Dimerization controls the activity of Fungal elicitors that trigger systemic resistance in plants. J Biol Chem 283:19804–19815

    Article  CAS  PubMed  Google Scholar 

  • Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB (1999) Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274:25945–25952

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic, London, pp 315–322

    Google Scholar 

  • Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400

    Article  CAS  PubMed  Google Scholar 

  • Wilson LM, Idnurm A, Howlett BJ (2002) Characterization of a gene (sp1) encoding a secreted protein from Leptosphaeria maculans, the blackleg pathogen of Brassica napus. Mol Plant Pathol 3:487–493

    Article  CAS  PubMed  Google Scholar 

  • Witthuhn RC, Wingfield BD, Wingfield MJ, Wolfaardt M, Harrington TC (1998) Monophyly of the conifer species in the Ceratocystis coerulescens complex based on DNA sequence data. Mycologia 90:96–101

    Article  CAS  Google Scholar 

  • Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    Article  PubMed  Google Scholar 

  • Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaparoli G, Cabrera OG, Medrano FJ, Tiburcio R, Lacerda G, Guimarães Pereira G (2009) Identification of a second family of genes in Moniliophthora perniciosa, the causal agent of witches broom disease in cacao, encoding necrosis-inducing proteins similar to cerato-platanins. Mycol Res 113:61–72

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work was supported by the Ministero Italiano dell’Università e della Ricerca Scientifica, Progetti di Ricerca di Interesse Nazionale 2005 and 2007 to A. Scala, G. Cappugi, and A. Santini.

Author information

Authors and Affiliations

  1. Dipartimento di Biotecnologie Agrarie, Sezione di Patologia Vegetale, Università di Firenze, Via della Lastruccia 10, 50019, Sesto Fiorentino, Italy

    Cecilia Comparini, Lara Carresi, Federico Sebastiani, Nicola Luchi, Paolo Capretti & Aniello Scala

  2. Dipartimento di Scienze Biochimiche, Università di Firenze, Viale Morgagni 50, 50134, Firenze, Italy

    Eleonora Pagni, Luigia Pazzagli & Gianni Cappugi

  3. Istituto per la Protezione delle Piante del CNR, Sezione di Firenze, Via Madonna del Piano, Palazzo E, 50019, Sesto Fiorentino, Italy

    Alberto Santini

  4. C.S.D.C, Dip. Fisica, Università di Firenze, Via Sansone 1, 50019, Sesto Fiorentino, Italy

    Francesca Sbrana & Bruno Tiribilli

Authors
  1. Cecilia Comparini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lara Carresi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eleonora Pagni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesca Sbrana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Federico Sebastiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicola Luchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alberto Santini
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paolo Capretti
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bruno Tiribilli
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Luigia Pazzagli
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Gianni Cappugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Aniello Scala
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aniello Scala.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM-1. (PDF 16 kb)

ESM-2. (PDF 113 kb)

ESM-3. (PDF 256 kb)

ESM-4. (PDF 86 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Comparini, C., Carresi, L., Pagni, E. et al. New proteins orthologous to cerato-platanin in various Ceratocystis species and the purification and characterization of cerato-populin from Ceratocystis populicola . Appl Microbiol Biotechnol 84, 309–322 (2009). https://doi.org/10.1007/s00253-009-1998-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-009-1998-4

Keywords

Search

Navigation