Skip to main content
SpringerLink
Log in
Book cover

Evolutionary Biology – Concepts, Molecular and Morphological Evolution pp 317–328Cite as

Convergent Evolution of Morphogenetic Processes in Fungi

  • Chapter
  • First Online:

Abstract

Eumycetes fungi are a diverse group of organisms whose evolution is characterized by frequent changes in nutritional strategy and the corresponding developmental programs. The reasons for this versatility are unknown. We previously discovered that the NADPH oxidase Nox2 and the tetraspanin Pls1 are used in two radically different cell types to achieve the same purpose: exiting from a reinforced cell, suggesting that convergent evolution of morphogenetic processes could account for the repetitive switches in trophic modes during fungal evolution. However, we recently observed that saprobic fungi are also able to differentiate appressorium-like structure closely resembling those of phytopathogenic species, arguing that the ability to differentiate such cells is an ancient property of filamentous fungi. Adaptation of parasitic and mutualistic fungi to plant may thus not solely reside in their ability to penetrate their host.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13:111–118

    Article  PubMed  CAS  Google Scholar 

  • Beckett A, Barton R, Wilson IM (1968) Fine structure of the wall and appendage formation in ascospores of Podospora anserina. J Gen Microbiol 53:89–94

    PubMed  CAS  Google Scholar 

  • Brun S, Malagnac F, Bidard F, Lalucque H, Silar P (2009) Functions and regulation of the Nox family in the filamentous fungus Podospora anserina: a new role in cellulose degradation. Mol Microbiol 74:480–496

    Article  PubMed  CAS  Google Scholar 

  • Cano-Dominguez N, Alvarez-Delfin K, Hansberg W, Aguirre J (2008) NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa. Eukaryot Cell 7:1352–1361

    Article  PubMed  CAS  Google Scholar 

  • Clergeot PH, Gourgues M, Cots J, Laurans F, Latorse MP, Pepin R, Tharreau D, Notteghem JL, Lebrun MH (2001) PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc Natl Acad Sci USA 98:6963–6968

    Article  PubMed  CAS  Google Scholar 

  • Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoria in plant infection. Microbes Infect 2:1631–1641

    Article  PubMed  CAS  Google Scholar 

  • Dujon B (2005) Hemiascomycetous yeasts at the forefront of comparative genomics. Curr Opin Genet Dev 15:614–620

    Article  PubMed  CAS  Google Scholar 

  • Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci USA 104:11772–11777

    Article  PubMed  CAS  Google Scholar 

  • Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Segurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Dequard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarre B, Sellem CH, Debuchy R, Wincker P, Weissenbach J, Silar P (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9:R77

    Article  PubMed  Google Scholar 

  • Giesbert S, Schurg T, Scheele S, Tudzynski P (2008) The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol Plant Pathol 9:317–327

    Article  PubMed  CAS  Google Scholar 

  • Gourgues M, Brunet-Simon A, Lebrun MH, Levis C (2004) The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619–629

    Article  PubMed  CAS  Google Scholar 

  • Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655

    Article  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547

    Article  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 GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, 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, Lucking R, Budel 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  PubMed  CAS  Google Scholar 

  • Lalucque H, Silar P (2003) NADPH oxidase: an enzyme for multicellularity? Trends Microbiol 11:9–12

    Article  PubMed  CAS  Google Scholar 

  • Lambou K, Malagnac F, Barbisan C, Tharreau D, Lebrun MH, Silar P (2008) A crucial role for the Pls1 tetraspanin during ascospore germination of the saprophytic fungus Podospora anserina. Eukaryot Cell 7:1809–1818

    Article  PubMed  CAS  Google Scholar 

  • Lara-Ortiz T, Riveros-Rosas H, Aguirre J (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50:1241–1255

    Article  PubMed  CAS  Google Scholar 

  • Loganantharaj R, Atwi M (2007) Towards validating the hypothesis of phylogenetic profiling. BMC Bioinformatics 8(Suppl 7):S25

    Article  PubMed  Google Scholar 

  • Malagnac F, Bidard F, Lalucque H, Brun S, Lambou K, Lebrun MH, Silar P (2008) Convergent evolution of morphogenetic processes in fungi: role of tetraspanins and NADPH oxidases 2 in plant pathogens and saprobes. Commun Integr Biol 1:180–181

    Article  PubMed  Google Scholar 

  • Malagnac F, Lalucque H, Lepere G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin DJ, Hibbett DS, Lutzoni F, Spatafora JW, Vilgalys R (2009) The search for the fungal tree of life. Trends Microbiol 17:488–497

    Article  PubMed  CAS  Google Scholar 

  • Miller AN, Huhndorf SM (2005) Multi-gene phylogenies indicate ascomal wall morphology is a better predictor of phylogenetic relationships than ascospore morphology in the Sordariales (Ascomycota, Fungi). Mol Phylogenet Evol 35:60–75

    Article  PubMed  CAS  Google Scholar 

  • Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361

    Article  PubMed  CAS  Google Scholar 

  • Segmuller N, Kokkelink L, Giesbert S, Odinius D, van Kan J, Tudzynski P (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant Microbe Interact 21:808–819

    Article  PubMed  Google Scholar 

  • Semighini CP, Harris SD (2008) Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 179:1919–1932

    Article  PubMed  CAS  Google Scholar 

  • Silar P (2005) Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant. Mycol Res 109:137–149

    Article  PubMed  CAS  Google Scholar 

  • Slot JC, Hibbett DS (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS ONE 2:e1097

    Article  PubMed  Google Scholar 

  • Takemoto D, Tanaka A, Scott B (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44:1065–1076

    Article  PubMed  CAS  Google Scholar 

  • Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006a) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:580–583

    Article  PubMed  CAS  Google Scholar 

  • Veneault-Fourrey C, Lambou K, Lebrun MH (2006b) Fungal Pls1 tetraspanins as key factors of penetration into host plants: a role in re-establishing polarized growth in the appressorium? FEMS Microbiol Lett 256:179–184

    Article  PubMed  CAS  Google Scholar 

  • Veneault-Fourrey C, Parisot D, Gourgues M, Lauge R, Lebrun MH, Langin T (2005) The tetraspanin gene ClPLS1 is essential for appressorium-mediated penetration of the fungal pathogen Colletotrichum lindemuthianum. Fungal Genet Biol 42:306–318

    Article  PubMed  CAS  Google Scholar 

  • Webster J (2007) Introduction to fungi, 3rd edn. Cambridge University Press, U.K

    Book  Google Scholar 

Download references

Acknowledgments

This work was supported by ANR grant n°ANR-05-Blan-0385-02.

Author information

Authors and Affiliations

  1. UFR des Sciences du Vivant, Université de Paris 7 – Denis Diderot, 75205, Paris Cedex 13, France

    Sylvain Brun & Philippe Silar

  2. Institut de Génétique et Microbiologie, UMR CNRS – Université de Paris 11, UPS Bât. 400, 91405, Orsay cedex, France

    Sylvain Brun & Philippe Silar

Authors
  1. Sylvain Brun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Silar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philippe Silar .

Editor information

Editors and Affiliations

  1. CNRS UMR 6632, Labo. Evolution Biologique et, Université d'Aix-Marseille, place Victor Hugo 3, Marseille CX 03, 13331, France

    Pierre Pontarotti

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Brun, S., Silar, P. (2010). Convergent Evolution of Morphogenetic Processes in Fungi. In: Pontarotti, P. (eds) Evolutionary Biology – Concepts, Molecular and Morphological Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12340-5_19

Download citation

Publish with us

Policies and ethics

Search

Navigation