Skip to main content
SpringerLink
Log in

Genes Acquired by Horizontal Transfer Are Potentially Involved in the Evolution of Phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, Two of the Major Pathogens of Cacao

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Moniliophthora perniciosa and Moniliophthora roreri are phytopathogenic basidiomycete species that infect cacao causing two important diseases in this crop: “Witches’ Broom” and “Frosty Pod Rot”, respectively. The ability of species from this genus (Moniliophthora) to cause disease is exceptional in the family Marasmiaceae. Species in closely related genera including, Marasmius, Crinipellis, and Chaetocalathus, are mainly saprotrophs and are not known to cause disease. In this study, the possibility that this phytopathogenic lifestyle has been acquired by horizontal gene transfer (HGT) was investigated. A stringent genome comparison pipeline was used to identify potential genes that have been obtained by Moniliophthora through HGT. This search led to the identification of three genes: a metallo-dependent hydrolase (MDH), a mannitol phosphate dehydrogenase (MPDH), and a family of necrosis-inducing proteins (NEPs). Phylogenetic analysis of these genes suggests that Moniliophthora acquired NEPs from oomycetes, MDH from actinobacteria and MPDH from firmicutes. Based on the known gene functions and on previous studies of M. perniciosa infection and development, a correlation between gene acquisition and the evolution of the phytopathogenic genus Moniliophthora can be postulated.

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

  • Aime MC, Phillips-Mora W (2005) The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia 97:1012–1022

    Article  CAS  PubMed  Google Scholar 

  • Almeida OC, Chiacchio FPB, Rocha HM (1997) Sobrevivência de Crinipellis perniciosa (Stahel) Singer em vassouras secas de cacaueiros (Theobroma cacao L.) do estado da Bahia. Agrotrópica 9:23–28

    Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Dijksterhuis J, De Vries RP (2006) Compatible solutes and fungal development. Biochem J 399(2):e3–e5

    Article  CAS  PubMed  Google Scholar 

  • Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311

    Article  CAS  PubMed  Google Scholar 

  • Flament MH, Kebe I, Clement D, Pieretti I, Risterucci AM, N’Goran JA, Cilas C, Despreaux D, Lanaud C (2001) Genetic mapping of resistance factors to Phytophthora palmivora in cocoa. Genome 44:79–85

    Article  CAS  PubMed  Google Scholar 

  • Garcia O, Macedo JA, Tiburcio R, Zaparoli G, Rincones J, Bittencourt LM, Ceita GO, Micheli F, Gesteira A, Mariano AC, Schiavinato MA, Medrano FJ, Meinhardt LW, Pereira GAG, Cascardo JC (2007) Characterization of necrosis and ethylene inducing proteins (NEP) in the basidiomycete Moniliophthora perniciosa, the causal agent of witches’ broom in Theobroma cacao. Mycol Res 111:443–455

    Article  CAS  PubMed  Google Scholar 

  • Gijzen M, Nurnberger T (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochem 67:1800–1807

    Article  CAS  Google Scholar 

  • Goodarzi H, Torabi N, Najafabadi HS, Archetti M (2008) Amino acid and codon usage profiles: adaptive changes in the frequency of amino acids and codons. Gene 407(1–2):30–41

    Article  CAS  PubMed  Google Scholar 

  • Griffith GW, Nicholson J, Nenninger A, Birch RN, Hedger JN (2003) Witches’ brooms and frosty pods: two major pathogens of cacao. New Zeal J Bot 41(3):423–435

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • Holm L, Sander C (1997) An evolutionary treasure: unification of a broad set of amidohydrolases related to urease. Proteins 28(1):72–82

    Article  CAS  PubMed  Google Scholar 

  • Hult K, Veide A, Gatenbeck S (1980) The distribution of the NADPH-regenerating mannitol cycle among fungal species. Arch Microbiol 128(2):253–255

    Article  CAS  PubMed  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher MP, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • Jenning JC, Apel-Birkhold PC, Bailey BA, Anderson JD (2000) Induction of ethylene biosynthesis and necrosis in weed leaves by a Fusarium oxysporum protein. Weed Sci 48:7–14

    Article  Google Scholar 

  • Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444(7115):97–101

    Article  PubMed  Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kempken F (1995) Horizontal transfer of a mitochondrial plasmid. Mol Gen Genet 2248:89–94

    Article  Google Scholar 

  • Khaldi N, Collemare J, Lebrun MH, Wolfe KH (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9:R18

    Article  PubMed  Google Scholar 

  • Liu Q, Ying SH, Feng MG, Jiang XH (2008) Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress. Antonie Van Leeuwenhoek 95(1):65–75

    Article  PubMed  Google Scholar 

  • Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA, Allen JE, Bosdet IE, Brent MR, Chiu R, Doering TL, Donlin MJ, D’Souza CA, Fox DS, Grinberg V, Fu J, Fukushima M, Haas BJ, Huang JC, Janbon G, Jones SJ, Koo HL, Krzywinski MI, Kwon-Chung JK, Lengeler KB, Maiti R, Marra MA, Marra RE, Mathewson CA, Mitchell TG, Pertea M, Riggs FR, Salzberg SL, Schein JE, Shvartsbeyn A, Shin H, Shumway M, Specht CA, Suh BB, Tenney A, Utterback TR, Wickes BL, Wortman JR, Wye NH, Kronstad JW, Lodge JK, Heitman J, Davis RW, Fraser CM, Hyman RW (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307(5713):1321–1324

    Article  PubMed  Google Scholar 

  • Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452(7183):88–92

    Article  CAS  PubMed  Google Scholar 

  • Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22(6):695–700

    Article  CAS  PubMed  Google Scholar 

  • Massoudieh A, Mathew A, Lambertini E, Nelson KE, Ginn TR (2007) Horizontal gene transfer on surfaces in natural porous media: conjugation and kinetics. Vadose Zone J 6:306–315

    Article  Google Scholar 

  • Meinhardt LW, Rincones J, Bailey BA, Aime MC, Griffith GW, Zhang D, Pereira GA (2008) Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: what’s new from this old foe? Mol Plant Pathol 9(5):577–588

    Article  PubMed  Google Scholar 

  • Mondego JM, Carazzolle MF, Costa GG, Formighieri EF, Parizzi LP, Rincones J, Cotomacci C, Carraro DM, Cunha AF, Carrer H, Vidal RO, Estrela RC, García O, Thomazella DP, de Oliveira BV, Pires AB, Rio MC, Araújo MR, de Moraes MH, Castro LA, Gramacho KP, Gonçalves MS, Neto JP, Neto AG, Barbosa LV, Guiltinan MJ, Bailey BA, Meinhardt LW, Cascardo JC, Pereira GA (2008) A genome survey of Moniliophthora perniciosa gives new insights into Witches’ broom disease of cacao. BMC Genomics 9:548

    Article  PubMed  Google Scholar 

  • Noiraud N, Maurousset L, Lemoine R (2001) Transport of polyols in higher plants. Plant Physiol Biochem 39(9):717–728

    Article  CAS  Google Scholar 

  • Oliver RP, Solomon PS (2008) Recent fungal diseases of crop plants: is lateral gene transfer a common theme? Mol Plant Microbe Interact 21(3):287–293

    Article  CAS  PubMed  Google Scholar 

  • Pemberton CL, Salmond GPC (2004) The Nep1-like proteins—a growing family of microbial elicitors of plant necrosis. Mol Plant Pathol 5:353–359

    Article  CAS  Google Scholar 

  • Pereira JL, de Almeida LCC, Santos SM (1996) Witches’ broom disease of cocoa in Bahia: attempts at eradication and containment. Crop Prot 15(8):743–752

    Article  Google Scholar 

  • Phillips-Mora W (2003) Origin, biogeography, genetic diversity and taxonomic affinities of the cacao fungus Moniliophthora roreri as determined using molecular, phytopathological and morpho-physiological evidence, doctoral dissertation. University of Reading, Reading, UK, 349 pp

  • Poptsova MS, Gogarten JP (2007) The power of phylogenetic approaches to detect horizontally transferred genes. BMC Evol Biol 7:45

    Article  PubMed  Google Scholar 

  • Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16:1857–1864

    Article  CAS  PubMed  Google Scholar 

  • Rincones J, Scarpari LM, Carazzolle MF, Mondego JM, Formighieri EF, Barau JG, Costa GG, Carraro DM, Brentani HP, Vilas-Boas LA, de Oliveira BV, Sabha M, Dias R, Cascardo JM, Azevedo RA, Meinhardt LW, Pereira GA (2008) Differential gene expression between the biotrophic-like and saprotrophic mycelia of the witches’ broom pathogen Moniliophthora perniciosa. Mol Plant Microbe Interact 21(7):891–908

    Article  CAS  PubMed  Google Scholar 

  • Rio MCS, Oliveira BV, Thomazella DP, Fracassi da Silva JA, Pereira GAG (2008) Production of calcium oxalate crystals by the basidiomycete Moniliophthora perniciosa, the causal agent of the Witches’ broom disease of cacao. Curr Microbiol 56(4):363–370

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Sanders IR (2006) Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol Evol 21(12):656–658

    Article  PubMed  Google Scholar 

  • Scarpari LM, Meinhardt LW, Mazzafera P, Pomella AW, Schiavinato MA, Cascardo JC, Pereira GA (2005) Biochemical changes during the development of witches’ broom: the most important disease of cacao in Brazil caused by Crinipellis perniciosa. J Exp Bot 56:865–877

    Article  CAS  PubMed  Google Scholar 

  • Solomon PS, Waters ODC, Jorgens CI, Lowe RGT, Rechberger J, Trengove RD, Oliver RP (2006) Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch). Biochem J 399:231–239

    Article  CAS  PubMed  Google Scholar 

  • Stanke M, Waack S (2003) Gene prediction with a hidden-markov model and a new intron submodel. Bioinformatics 19(Suppl. 2):215–225

    Google Scholar 

  • Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustalx windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576

    PubMed  Google Scholar 

  • Vélëz H, Glassbrook NJ, Daub ME (2008) Mannitol biosynthesis is required for plant pathogenicity by Alternaria alternata. FEMS Microbiol Lett 285(1):122–129

    Article  PubMed  Google Scholar 

  • Voegele RT, Hahn M, Lohaus G, Link T, Heiser I, Mendgen K (2005) Possible roles for mannitol and mannitol dehydrogenase in the biotrophic plant pathogen Uromyces fabae. Plant Physiol 137(1):190–198

    Article  CAS  PubMed  Google Scholar 

  • Wenzl P, Wong L, Kwang-Won K, Jefferson RA (2005) A functional screen identifies lateral transfer of beta-glucuronidase (gus) from bacteria to fungi. Mol Biol Evol 22:308–316

    Article  CAS  PubMed  Google Scholar 

  • Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699

    CAS  PubMed  Google Scholar 

  • Youssef NH, Elshahed MS (2009) Diversity rankings among bacterial lineages in soil. ISME J 3(3):305–313

    Article  CAS  PubMed  Google Scholar 

  • Zaparoli G, Cabrera OG, Medrano FJ, Tiburcio RA, Lacerda G, Pereira GAG (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

Acknowledgments

We thank Dr. Joana Rincones for review and commentaries about the article. We are indebted to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Secretaria de Agricultura, Irrigação e Reforma Agrária do Estado da Bahia (SEAGRI), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support.

Author information

Authors and Affiliations

  1. Laboratório de Genômica e Expressão, Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, 13083-970, Campinas, SP, Brazil

    Ricardo Augusto Tiburcio, Gustavo Gilson Lacerda Costa, Marcelo Falsarella Carazzolle & Gonçalo Amarante Guimarães Pereira

  2. Centro Nacional de Processamento de Alto Desempenho em São Paulo, Universidade Estadual de Campinas, CP 6141, Campinas, SP, 13083-970, Brazil

    Marcelo Falsarella Carazzolle

  3. Centro de Pesquisa e Desenvolvimento em Recursos Genéticos Vegetais, Instituto Agronômico de Campinas, Campinas, SP, 13083-970, Brazil

    Jorge Maurício Costa Mondego

  4. Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, 13083-970, Brazil

    Jorge Maurício Costa Mondego

  5. Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, 16802, USA

    Stephen C. Schuster

  6. School of Forest Resources, Pennsylvania State University, University Park, PA, 16802, USA

    John E. Carlson

  7. Department of Horticulture, Pennsylvania State University, University Park, PA, 16802, USA

    Mark J. Guiltinan

  8. Sustainable Perennial Crops Laboratory, USDA-ARS, 10300 Baltimore Av., BARC-W, Beltsville, MD, 20740, USA

    Bryan A. Bailey & Lyndel W. Meinhardt

  9. Department of Genetics, School of Medicine, University of North Carolina at Chapel Hill, Mary Ellen Jones, Room 921, 27599-3280, Chapel Hill, NC, USA

    Piotr Mieczkowski

Authors
  1. Ricardo Augusto Tiburcio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gustavo Gilson Lacerda Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcelo Falsarella Carazzolle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge Maurício Costa Mondego
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephen C. Schuster
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John E. Carlson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark J. Guiltinan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bryan A. Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Piotr Mieczkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lyndel W. Meinhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Gonçalo Amarante Guimarães Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gonçalo Amarante Guimarães Pereira.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tiburcio, R.A., Costa, G.G.L., Carazzolle, M.F. et al. Genes Acquired by Horizontal Transfer Are Potentially Involved in the Evolution of Phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, Two of the Major Pathogens of Cacao. J Mol Evol 70, 85–97 (2010). https://doi.org/10.1007/s00239-009-9311-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-009-9311-9

Keywords

Search

Navigation