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  • Review Article
  • Published:

The social network: deciphering fungal language

Nature Reviews Microbiology volume 9, pages 440–451 (2011)Cite this article

Subjects

Key Points

  • Fungi interact with one another and respond to environmental cues using a sophisticated series of extracellular signals and cellular responses. Here, we focus on molecules secreted by the largest phylum of fungi, the Ascomycota, and the quest to understand their biological functions.

  • Germination of asexual spores (conidia) is inhibited by auto-inhibitors, which are produced by a wide range of ascomycetes and have varying specificities and structures.

  • Unknown extracellular signals regulate cell fusion events between germinated conidia, which forms the basis of the interconnected hyphal network; coordination of germination results in faster establishment of colonies and networks. During the communication that precedes these fusion events in Neurospora crassa, cells alternate between signal-sending and signal-perceiving states in order to efficiently coordinate growth towards one another without undergoing terminal developmental differentiation.

  • Communication signals within an individual (or cellular network) are used to regulate growth and development. During starvation in Saccharomyces cerevisiae, connecting fibrils develop between cells, and these fibrils are proposed to have roles in cell–cell communication.

  • Asexual development is regulated by both environmental conditions and developmental age, and has been extensively studied in Aspergillus nidulans. Common regulatory pathways regulate asexual development and mycotoxin production in Aspergillus spp.

  • Many ascomycetes secrete compounds that inhibit the growth of other organisms, including fungi, in their immediate environment. These compounds can cause cell cycle arrest, membrane damage and cell wall stress, or can block asexual reproduction.

  • Mycoparasites, which are fungi that parasitize other fungi, use extracellular sensing to guide them towards their prey. In Trichoderma spp., mutations in a G protein subunit that is involved in signal transduction affect the balance between asexual reproduction and mycoparasitism.

Abstract

It has been estimated that up to one quarter of the world's biomass is of fungal origin, comprising approximately 1.5 million species. In order to interact with one another and respond to environmental cues, fungi communicate with their own chemical languages using a sophisticated series of extracellular signals and cellular responses. A new appreciation for the linkage between these chemical languages and developmental processes in fungi has renewed interest in these signalling molecules, which can now be studied using post-genomic resources. In this Review, we focus on the molecules that are secreted by the largest phylum of fungi, the Ascomycota, and the quest to understand their biological function.

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Figure 1: Extracellular signalling during the life cycle of Neurospora crassa.
Figure 2: Cell–cell communication during germling fusion in Neurospora crassa.
Figure 3: Antagonistic interactions between ascomycetes.
Figure 4: Asexual development in model filamentous ascomycete species.

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References

  1. McLaughlin, D. J., Hibbett, D. S., Lutzoni, F., Spatafora, J. W. & Vilgalys, R. The search for the fungal tree of life. Trends Microbiol. 17, 488–497 (2009).

    Article  CAS  PubMed  Google Scholar 

  2. Blackwell, M., Hibbett, D. S., Taylor, J. W. & Spatafora, J. W. Research coordination networks: a phylogeny for kingdom Fungi (Deep Hypha). Mycologia 98, 829–837 (2006).

    Article  PubMed  Google Scholar 

  3. Schoch, C. L. et al. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst. Biol. 58, 224–239 (2009). This paper presents the most taxonomically complete phylogeny of the Ascomycota (and refines our understanding of evolution of their major ecologies and lifestyles).

    Article  CAS  PubMed  Google Scholar 

  4. Greenwald, C. J. et al. Temporal and spatial regulation of gene expression during asexual development of Neurospora crassa. Genetics 186, 1217–1230 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Springer, M. L. & Yanofsky, C. A morphological and genetic analysis of conidiophore development in Neurospora crassa. Genes Dev. 3, 559–571 (1989).

    Article  CAS  PubMed  Google Scholar 

  6. Adams, T. H., Wieser, J. K. & Yu, J. H. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62, 35–54 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Allen, P. J. in Physiological Plant Pathology, (eds. R. Heitefull and P. H. Williams) 51–85 (Springer-Verlag, New York, 1976).

    Book  Google Scholar 

  8. Inoue, M. et al. Self-germination inhibitors from Colletotrichum fragariae. J. Chem. Ecol. 22, 2111–2122 (1996).

    Article  CAS  PubMed  Google Scholar 

  9. Leite, B. & Nicholson, R. I. Mycosporine-alanine: a self-inhibitor of germination from the conidial mucilage of Colletotrichum graminicola. Exp. Mycol. 16, 76–86 (1992).

    Article  CAS  Google Scholar 

  10. Tsurushima, T., Ueno, T., Fukami, H., Irie, H. & Inoue, M. Germination self-inhibitors from Colletotrichum gloeosporioides f. sp. jussiaea. Mol. Plant Microbe Interact. 8, 652–657 (1995).

    Article  CAS  Google Scholar 

  11. Chitarra, G. S., Abee, T., Rombouts, F. M., Posthumus, M. A. & Dijksterhuis, J. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl. Environ. Microbiol. 70, 2823–2829 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Horowitz, N. H., Charlang, G., Horn, G. & Williams, N. P. Isolation and identification of the conidial germination factor of Neurospora crassa. J. Bacteriol. 127, 135–140 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Charlang, G. W. & Horowitz, N. H. Germination and growth of Neurospora at low water activities. Proc. Natl Acad. Sci. USA 68, 260–262 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Köhler, E., Zur Kenntnis Der Vegetativen Anastomosen Der Pilze (II. Mitteilung). Planta 10, 495–522 (1930).

    Article  Google Scholar 

  15. Roca, M. G., Arlt, J., Jeffree, C. E. & Read, N. D. Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot. Cell 4, 911–919 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Roca, M. G. et al. Conidial anastomosis fusion between Colletotrichum species. Mycol. Res. 108, 1320–1326 (2004).

    Article  PubMed  Google Scholar 

  17. Ishikawa, F. H., Souza, E. A., Read, N. D. & Roca, M. G. Live-cell imaging of conidial fusion in the bean pathogen, Colletotrichum lindemuthianum. Fungal Biol. 114, 2–9 (2010).

    Article  PubMed  Google Scholar 

  18. Leu, L. S. Anastomosis in Venturia inaequalis (CKE) Wint. Thesis, Univ. Wisconsin, Madison (1967).

    Google Scholar 

  19. Wright, G. D., Arlt, J., Poon, W. C. K. & Read, N. D. Optical tweezer micromanipulation of filamentous fungi. Fungal Genet. Biol. 44, 1–13 (2007).

    Article  PubMed  Google Scholar 

  20. Berepiki, A., Lichius, A., Shoji, J. Y., Tilsner, J. & Read, N. D. F-actin dynamics in Neurospora crassa. Eukaryot. Cell 9, 547–557 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Roca, M. G., Kuo, H. C., Lichius, A., Freitag, M. & Read, N. D. Nuclear dynamics, mitosis, and the cytoskeleton during the early stages of colony initiation in Neurospora crassa. Eukaryot. Cell 9, 1171–1183 (2010). This paper evaluates the role of the cytoskeleton and nuclear dynamics during CAT formation and germling fusion.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pandey, A., Roca, M. G., Read, N. D. & Glass, N. L. Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot. Cell 3, 348–358 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Maerz, S. et al. The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179, 1313–1325 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Fleissner, A. et al. The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot. Cell 4, 920–930 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Fleissner, A., Leeder, A. C., Roca, M. G., Read, N. D. & Glass, N. L. Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc. Natl Acad. Sci. USA 106, 19387–19392 (2009). This paper describes signalling that occurs prior to cell fusion between N. crassa germlings, and forms the basis for the model of how genetically identical individuals undergo bidirectional communication without responding to their own signals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Macias, M. J., Wiesner, S. & Sudol, M. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Letts. 513, 30–37 (2002).

    Article  CAS  Google Scholar 

  27. Ruiz-Roldán, M. C. et al. Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum. Eukaryot. Cell 9, 1216–1224 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Lopez-Berges, M. S., Rispail, N., Prados-Rosales, R. C. & Di Pietro, A. A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22, 2459–2475 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kim, H. & Borkovich, K. A. Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot. Cell 5, 544–554 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kim, H. & Borkovich, K. A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol. Microbiol. 52, 1781–1798 (2004).

    Article  CAS  PubMed  Google Scholar 

  31. McMains, V. C., Liao, X. H. & Kimmel, A. R. Oscillatory signaling and network responses during the development of Dictyostelium discoideum. Ageing Res. Rev. 7, 234–248 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ishitani, C. & Sakaguchi, K. I. Hereditary variation and recombination in Koji-molds (Aspergillus oryzae and Asp. sojae). V. Heterocaryosis. J. Gen. Appl. Microbiol. 2, 345–400 (1956).

    Article  Google Scholar 

  33. Hickey, P. C., Jacobson, D., Read, N. D. & Glass, N. L. Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet. Biol. 37, 109–119 (2002).

    Article  PubMed  Google Scholar 

  34. Aldabbous, M. S. et al. The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiology 156, 2621–2629 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Read, N. D., Fleiβner, A., Roca, M. G. & Glass, N. L. in Cellular and Molecular Biology of Filamentous Fungi (eds Borkovich, K. A. & Ebbole, D. J.) 260–273 (ASM Press, Washington D. C., 2010). A comprehensive review of germling and hyphal fusion in filamentous ascomycetes.

    Book  Google Scholar 

  36. Simonin, A. R., Rasmussen, C. G., Yang, M. & Glass, N. L. Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet. Biol. 47, 855–868 (2010).

    Article  CAS  PubMed  Google Scholar 

  37. Gaillard, S., Bartoli, M., Castets, F. & Monneron, A., Striatin, a calmodulin-dependent scaffolding protein, directly binds caveolin-1. FEBS Lett. 508, 49–52 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Torralba, S. & Heath, I. Cytoskeletal and Ca2+ regulation of hyphal tip growth and initiation. Curr. Topic Dev. Biol. 51, 135–187 (2001).

    Article  CAS  Google Scholar 

  39. Craven, K. D., Velez, H., Cho, Y., Lawrence, C. B. & Mitchell, T. K. Anastomosis is required for virulence of the fungal necrotroph Alternaria brassicicola. Eukaryot. Cell 7, 675–683 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Prados Rosales, R. C. & Di Pietro, A. Vegetative hyphal fusion is not essential for plant infection by Fusarium oxysporum. Eukaryot. Cell 7, 162–171 (2008).

    Article  CAS  PubMed  Google Scholar 

  41. Sbrana, C., Fortuna, P. & Giovannetti, M. Plugging into the network: belowground connections between germlings and extraradical mycelium of arbuscular mycorrhizal fungi. Mycologia 103, 307–316 (2010).

    Article  PubMed  Google Scholar 

  42. Stephenson, L. W., Erwin, D. C. & Leary, J. V. Hyphal anastomosis in Phytophthora capsici. Phytopathol. 64, 149–150 (1974).

    Article  Google Scholar 

  43. Trinci, A. P. J. in The Ecology and Physiology of the Fungal Mycelium. (eds Jennings, D. H. & Rayner, A. D. M.) 23–52 (Cambridge Univ. Press, Cambridge, UK, 1984).

    Google Scholar 

  44. Bottone, E. J., Nagarsheth, N. & Chiu, K. Evidence of self-inhibition by filamentous fungi accounts for unidirectional hyphal growth in colonies. Can. J. Microbiol. 44, 390–393 (1998).

    Article  CAS  PubMed  Google Scholar 

  45. Varon, M. & Choder, M. Organization and cell-cell interaction in starved Saccharomyces cerevisiae colonies. J. Bacteriol. 182, 3877–3880 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Chen, H. & Fink, G. R. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev. 20, 1150–1161 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hall, R. A. et al. CO2 acts as a signalling molecule in populations of the fungal pathogen Candida albicans. PLoS Pathog. 6, e1001193 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  48. Hornby, J. M. et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67, 2982–2992 (2001). This report is the first structural identification of a fungal quorum sensing system, and details the common phenomenon of inoculum size effect.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mosel, D. D., Dumitru, R., Hornby, J. M., Atkin, A. L. & Nickerson, K. W. Farnesol concentrations required to block germ tube formation in Candida albicans in the presence and absence of serum. Appl. Environ. Microbiol. 71, 4938–4940 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Finkel, J. S. & Mitchell, A. P. Genetic control of Candida albicans biofilm development. Nature Rev. Microbiol. 9, 109–118 (2010).

    Article  CAS  Google Scholar 

  51. Chen, H., Fujita, M., Feng, Q., Clardy, J. & Fink, G. R. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc. Natl Acad. Sci. USA 101, 5048–5052 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Granshaw, T., Tsukamoto, M. & Brody, S. Circadian rhythms in Neurospora crassa: farnesol or geraniol allow expression of rhythmicity in the otherwise arrhythmic strains frq10, wc-1, and wc-2. J. Biol. Rhythms 18, 287–296 (2003).

    Article  CAS  PubMed  Google Scholar 

  53. Dunlap, J. C. et al. A circadian clock in Neurospora: how genes and proteins cooperate to produce a sustained, entrainable, and compensated biological oscillator with a period of about a day. Cold Spring Harbor Symp. Quant. Biol. 72, 57–68 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Lee, B. N. & Adams, T. H. The Aspergillus nidulans fluG gene is required for production of an extracellular developmental signal and is related to prokaryotic glutamine synthetase I. Genes Dev. 8, 641–651 (1994).

    Article  CAS  PubMed  Google Scholar 

  55. Etxebeste, O., Garzia, A., Espeso, E. A. & Ugalde, U. Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol. 18, 569–576 (2010). An up-to-date review of the regulation of asexual development in A. nidulans.

    Article  CAS  PubMed  Google Scholar 

  56. Mah, J. H. & Yu, J. H. Upstream and downstream regulation of asexual development in Aspergillus fumigatus. Eukaryot. Cell 5, 1585–1595 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ogawa, M., Tokuoka, M., Jin, F. J., Takahashi, T. & Koyama, Y. Genetic analysis of conidiation regulatory pathways in koji-mold Aspergillus oryzae. Fungal Genet. Biol. 47, 10–18 (2010).

    Article  CAS  PubMed  Google Scholar 

  58. Clutterbuck, A. The genetics of conidiophore pigmentation in Aspergillus nidulans. J. Gen. Microbiol. 136, 1731–1738 (1990).

    Article  CAS  PubMed  Google Scholar 

  59. Yu, J.-H. Regulation of development in Aspergillus nidulans and Aspergillus fumigatus. Mycobiology 38, 229–237 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Yu, J. H. Heterotrimeric G protein signaling and RGSs in Aspergillus nidulans. J. Microbiol. 44, 145–154 (2006).

    CAS  PubMed  Google Scholar 

  61. Soid-Raggi, G., Sánchez, O. & Aguirre, J. TmpA, a member of a novel family of putative membrane flavoproteins, regulates asexual development in Aspergillus nidulans. Mol. Microbiol. 59, 854–869 (2006).

    Article  CAS  PubMed  Google Scholar 

  62. Etxebeste, O. et al. Basic-zipper-type transcription factor FlbB controls asexual development in Aspergillus nidulans. Eukaryot. Cell 7, 38–48 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. Etxebeste, O. et al. The bZIP-type transcription factor FlbB regulates distinct morphogenetic stages of colony formation in Aspergillus nidulans. Mol. Microbiol. 73, 775–789 (2009).

    Article  CAS  PubMed  Google Scholar 

  64. Springer, M. L. Genetic control of fungal differentiation: The three sporulation pathways of Neurospora crassa. Bioessays 15, 365–374 (1993).

    Article  CAS  PubMed  Google Scholar 

  65. Berlin, V. & Yanofsky, C. Isolation and characterization of genes differentially expressed during conidiation of Neurospora crassa. Mol. Cell. Biol. 5, 849–855 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Olmedo, M., Ruger-Herreros, C. & Corrochano, L. M. Regulation by blue light of the fluffy gene encoding a major regulator of conidiation in Neurospora crassa. Genetics 184, 651–658.

  67. Colot, H. V. et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl Acad. Sci. USA 103, 10352–10357 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Liebmann, B., Muller, M., Braun, A. & Brakhage, A. A. The cyclic AMP-dependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect. Immun. 72, 5193–5203 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Banno, S. et al. A catalytic subunit of cyclic AMP-dependent protein kinase, PKAC-1, regulates asexual differentiation in Neurospora crassa. Genes Genet. Syst. 80, 25–34 (2005).

    Article  CAS  PubMed  Google Scholar 

  70. Rerngsamran, P., Murphy, M. B., Doyle, S. A. & Ebbole, D. J. Fluffy, the major regulator of conidiation in Neurospora crassa, directly activates a developmentally regulated hydrophobin gene. Mol. Microbiol. 56, 282–297 (2005).

    Article  CAS  PubMed  Google Scholar 

  71. Roncal, T., Cordobés, S., Sterner, O. & Ugalde, U. Conidiation in Penicillium cyclopium is induced by conidiogenone, an endogenous diterpene. Eukaryot. Cell 1, 823–829 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Park, D. & Robinson, P. M. Germination studies with Geotrichum candidum. Trans. Brit. Mycol. Soc. 54 83–92 (1970).

    Article  CAS  Google Scholar 

  73. Tsitsigiannis, D. I., Zarnowski, R. & Keller, N. P. The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. J. Biol. Chem. 279, 11344–11353 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Dagenais, T. R. T. et al. Defects in conidiophore development and conidium-macrophage interactions in a dioxygenase mutant of Aspergillus fumigatus. Infect. Immun. 76, 3214–3220 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Calvo, A. M., Wilson, R. A., Bok, J. W. & Keller, N. P. Relationship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev. 66, 447–459 (2002). This review explores the relationship between fungal development and secondary metabolism in the Aspergilli, providing new insights into the shared regulatory networks that link the two processes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Wieser, J., Yu, J. H. & Adams, T. H. Dominant mutations affecting both sporulation and sterigmatocystin biosynthesis in Aspergillus nidulans. Curr. Genet. 32, 218–224 (1997).

    Article  CAS  PubMed  Google Scholar 

  77. Roze, L. V. et al. Volatile profiling reveals intracellular metabolic changes in Aspergillus parasiticus: veA regulates branched chain amino acid and ethanol metabolism. BMC Biochem. 11, 33 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  78. Bayram, O., Krappmann, S., Seiler, S., Vogt, N. & Braus, G. H. Neurospora crassa ve-1 affects asexual conidiation. Fungal Genet. Biol. 45, 127–138 (2008).

    Article  CAS  PubMed  Google Scholar 

  79. Champe, S. P. & el-Zayat, A. A. Isolation of a sexual sporulation hormone from Aspergillus nidulans. J. Bacteriol. 171, 3982–3988 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Mazur, P., Meyers, H. & Nakanishi, K. Structural elucidation of sporogenic fatty acid metabolites from Aspergillus nidulans. Tetrahedron Lett. 31, 3837–3840 (1990).

    Article  CAS  Google Scholar 

  81. Tsitsigiannis, D. I., Kowieski, T., Zarnowski, R. & Keller, N. Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151, 1809–1821 (2005).

    Article  CAS  PubMed  Google Scholar 

  82. Brown, S. H. et al. Oxygenase coordination is required for morphological transition and the host–fungus interaction of Aspergillus flavus. Mol. Plant Microbe Interact. 22, 882–894 (2009).

    Article  CAS  PubMed  Google Scholar 

  83. Ncango, D. M. et al. Oxylipin-coated hat-shaped ascospores of Ascoidea corymbosa. Can. J. Microbiol. 52, 1046–1050 (2006).

    Article  CAS  PubMed  Google Scholar 

  84. Innocenti, F. D., Pohl, U. & Russo, V. E. Photoinduction of protoperithecia in Neurospora crassa by blue light. Photochem. Photobiol. 37, 49–51 (1983).

    Article  CAS  PubMed  Google Scholar 

  85. Pöggeler, S., Nowrousian, M. & Kuck, U. in The Mycota I (eds Kues, U. & Fischer, R.) 325–355 (Springer, 2006). A comprehensive review of sexual development in the filamentous ascomycete fungi.

    Google Scholar 

  86. Li, L., Wright, S. J., Krystofova, S., Park, G. & Borkovich, K. A. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 61, 423–452 (2007).

    Article  CAS  PubMed  Google Scholar 

  87. Bardwell, L. A walk-through of the yeast mating pheromone response pathway. Peptides 26, 339–350 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Bistis, G. N. Evidence for diffusable mating-type specific trichogyne attactants in Neurospora crassa. Exp. Mycol. 7, 292–295 (1983).

    Article  CAS  Google Scholar 

  89. Schmoll, M., Seibel, C., Tisch, D., Dorrer, M. & Kubicek, C. P. A novel class of peptide pheromone precursors in ascomycetous fungi. Mol. Microbiol. 77, 1483–1501 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Metzenberg, R. L. Do perithecia smell perithecia? Fungal Genet. Newsl. 40, 46–48 (1993).

    Google Scholar 

  91. Palkova, Z. & Forstova, J. Yeast colonies synchronise their growth and development. J. Cell Sci. 113, 1923–1928 (2000).

    CAS  PubMed  Google Scholar 

  92. Cutler, H. G., Cox, R. H. Crumley, F. G. & Cole, P. D., 6-pentyl-α-pyrone from Trichoderma harzianum – its plant-growth inhibitory and antimicrobial properties. Agric. Biol. Chem. 50, 2943–2945 (1986).

    CAS  Google Scholar 

  93. Scarselletti, R. & Faull, J. L. In vitro activity of 6-pentyl-α-pyrone, a metabolite of Trichoderma harzianum, in the inhibition of Rhizoctonia solani and Fusarium oxysporum f. sp. lycopersici. Mycol. Res. 98, 1207–1209 (1994).

    Article  CAS  Google Scholar 

  94. El-Hasan, A., Walker, F., Schone, J. & Buchenauer, H. Antagonistic effect of 6-pentyl-α-pyrone produced by Trichoderma harzianum toward Fusarium moniliforme. J. Plant Dis. Protect. 114, 62–68 (2007).

    Article  CAS  Google Scholar 

  95. Strobel, G. A., Dirkse, E., Sears, J. & Markworth, C. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiol. 147, 2943–2950 (2001).

    Article  CAS  Google Scholar 

  96. Lorek, J., Poggeler, S., Weide, M. R., Breves, R. & Bockmuhl, D. P. Influence of farnesol on the morphogenesis of Aspergillus niger. J. Basic Microbiol. 48, 99–103 (2008).

    Article  PubMed  Google Scholar 

  97. Semighini, C. P., Hornby, J. M., Dumitru, R., Nickerson, K. W. & Harris, S. D. Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol. Microbiol. 59, 753–764 (2006).

    Article  CAS  PubMed  Google Scholar 

  98. Dichtl, K. et al. Farnesol misplaces tip-localized Rho proteins and inhibits cell wall integrity signalling in Aspergillus fumigatus. Mol. Microbiol. 76, 1191–1204.

    Article  CAS  PubMed  Google Scholar 

  99. Semighini, C. P., Murray, N. & Harris, S. D. Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol. Lett. 279, 259–264 (2008).

    Article  CAS  PubMed  Google Scholar 

  100. Kim, K. K., Fravel, D. R. & Papavizas, G. C. Identification of a metabolite produced by Talaromyces flavus as glucose oxidase and its role in the biocontrol of Verticillium dahliae. Phytopathology 78, 488–492 (1988).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  102. Kerridge, D. The effect of actidione and other antifungal agents on nucleic acid and protein synthesis in Saccharomyces carlsbergensis. J. Gen. Microbiol. 19, 497–506 (1958).

    Article  CAS  PubMed  Google Scholar 

  103. Schrettl, M. et al. Self-protection against gliotoxin — a component of the gliotoxin biosynthetic cluster, GliT, completely protects Aspergillus fumigatus against exogenous gliotoxin. PLoS Pathog. 6, e1000952 (2010).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  104. Theis, T., Wedde, M., Meyer, V. & Stahl, U. The antifungal protein from Aspergillus giganteus causes membrane permeabilization. Antimicrob. Agents Chemo. 47, 588–593 (2003).

    Article  CAS  Google Scholar 

  105. Leiter, E. et al. Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob. Agents Chemo. 49, 2445–2453 (2005).

    Article  CAS  Google Scholar 

  106. Binder, U., Oberparleiter, C., Meyer, V. & Marx, F. The antifungal protein PAF interferes with PKC/MPK and cAMP/PKA signalling of Aspergillus nidulans. Mol. Microbiol. 75, 294–307 (2010).

    Article  CAS  PubMed  Google Scholar 

  107. Binder, U., Chu, M. L., Read, N. D. & Marx, F. The antifungal activity of the Penicillium chrysogenum protein PAF disrupts calcium homeostasis in Neurospora crassa. Eukaryot. Cell 9, 1374–1382 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Marquina, D., Santos, A. & Peinado, J. M., Biology of killer yeasts. Int. Microbiol. 5, 65–71 (2002).

    Article  CAS  PubMed  Google Scholar 

  109. Chet, I., Harman, G. E. & Baker, R. Trichoderma hamatum:its hyphal interactions with Rhizoctonia solani and Pythium spp. Microbial Ecol. 7, 29–38 (1981).

    Article  CAS  Google Scholar 

  110. Elad, Y., Chet, I., Boyle, P. & Henis, Y. Parasitism of Trichoderma spp. on Rhizoctonia solani and Sclerotium rolfsii — scanning electron-microscopy and fluorescence microscopy. Phytopathol. 73, 85–88 (1983).

    Article  Google Scholar 

  111. Nordbring-Hertz, B., Frimnan, E. & Veenhuis, M. Hyphal fusion during initial stages of trap formation in Arthrobotrys oligospora. Antonie Van Leeuwenhoek 55, 237–244 (1989).

    Article  CAS  PubMed  Google Scholar 

  112. Rocha-Ramirez, V., Omero, C., Chet, I., Horwitz, B. A. & Herrera-Estrella, A. Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 1, 594–605 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Reithner, B. et al. The G protein α-subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet. Biol. 42, 749–760 (2005). This paper studied the impact of deletion of the tga1 gene (encoding the Gα subunit of a G protein) on mycoparasitism-related processes in T. atroviride.

    Article  CAS  PubMed  Google Scholar 

  114. Mukherjee, M., Mukherjee, P. K. & Kale, S. P. cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153, 1734–1742 (2007).

    Article  CAS  PubMed  Google Scholar 

  115. Omero, C. et al. G protein activators and cAMP promote mycoparasitic behaviour in Trichoderma harzianum. Mycol. Res. 103, 1637–1642 (1999).

    Article  CAS  Google Scholar 

  116. Reithner, B. et al. Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk 1 differentially affects mycoparasitism and plant protection. Fungal Genet. Biol. 44, 1123–1133 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Mendoza-Mendoza, A. et al. Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc. Natl Acad. Sci. USA 100, 15965–15970 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Mukherjee, P. K., Latha, J., Hadar, R. & Horwitz, B. A. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot. Cell 2, 446–455 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Seidl, V. et al. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genomics 10, 567 (2009).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  120. Tucker, C. L., High-throughput cell-based assays in yeast. Drug Discov. Today 7, S125–S130 (2002).

    Article  CAS  PubMed  Google Scholar 

  121. Dunlap, J. C. et al. Enabling a community to dissect an organism: overview of the Neurospora functional genomics project. Adv. Genet. 57, 49–96 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. & Lorito, M. Trichoderma species — opportunistic, avirulent plant symbionts. Nature Rev. Microbiol. 2, 43–56 (2004).

    Article  CAS  Google Scholar 

  123. Nemcovic, M., Jakubikova, L., Viden, I. & Farkas, V. Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol. Lett. 284, 231–236 (2008).

    Article  CAS  PubMed  Google Scholar 

  124. Garrett, M. K. & Robinson, P. M. A stable inhibitor of spore germination produced by fungi. Arch. Mikrobiol. 67, 370–371 (1969).

    Article  CAS  PubMed  Google Scholar 

  125. Antonov, A., Stewart, A. & Walter, M. Inhibition of conidium germination and mycelial growth of Botrytis cinerea by natural products. Proc. 50th N.Z. Plant Protection Conf. 159–164 (1997).

  126. Stinson, M., Ezra, D., Hess, W. M., Sears, J. & Strobel, G. An endophytic Gliocladium sp of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Sci. 165, 913–922 (2003).

    Article  CAS  Google Scholar 

  127. Aneja, M., Gianfagna, T. J. & Hebbar, P. K. Trichoderma harzianum produces nonanoic acid, an inhibitor of spore germination and mycelial growth of two cacao pathogens. Physiol. Mol. Plant Pathol. 67, 304–307 (2005).

    Article  CAS  Google Scholar 

  128. El-Hasan, A., Walker, F., Schone, J. & Buchenauer, H. Detection of viridiofungin A and other antifungal metabolites excreted by Trichoderma harzianum active against different plant pathogens. Eur. J. Plant Pathol. 124, 457–470 (2009).

    Article  CAS  Google Scholar 

  129. Harris, G. H. et al. Isolation and structure elucidation of viridiofungin-A, viridiofungin-B and viridiofungin-C. Tetrahedron Lett. 34, 5235–5238 (1993).

    Article  CAS  Google Scholar 

  130. Park, D. & Robinson, P. M. Isolation and bioassay of a fungal morphogen. Nature 203, 988–989 (1964).

    Article  Google Scholar 

  131. Robinson, P. M. & Park, D. Citrinin — a fungistatic antibiotic and narrowing factor. Nature 211, 883–884 (1966).

    Article  CAS  PubMed  Google Scholar 

  132. Brian, P. W. & Hemming, H. G. Production of antifungal and antibacterial substances by fungi; preliminary examination of 166 strains of Fungi Imperfecti. J. Gen. Microbiol. 1, 158–167 (1947).

    Article  CAS  PubMed  Google Scholar 

  133. Jang, K. S., Kim, H. M. & Chung, B. K. Purification and antifungal activities of an antibiotic produced by Gliocladium virens G1 against plant pathogens. Plant Pathol. J. 17, 52–56 (2001).

    Google Scholar 

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Acknowledgements

A.C.L. and J.P.-G. are supported by a research grant from the US National Science Foundation, which was awarded to N.L.G. for studies on germling and hyphal anastomosis. We thank M. North for helpful comments on the manuscript and colleagues for their contributions to the work described.

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  1. Plant and Microbial Biology Department, The University of California, Berkeley, 94720-3102, CA, USA

    Abigail C. Leeder, Javier Palma-Guerrero & N. Louise Glass

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  1. Abigail C. Leeder
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  2. Javier Palma-Guerrero
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Correspondence to N. Louise Glass.

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Supplementary information

Glossary

Hyphae

Multicellular filaments that grow by tip extension.

Mycelium

A fungal colony made up of interconnected hyphae.

Conidiophores

Specialized structures that produce asexual spores (conidia).

Germlings

Aexual spores that have recently germinated.

Chemotropism

Growth of a cell towards a concentration gradient of a chemical stimulus.

Optical tweezers

A microscope equipped with a highly focused laser beam that provides attractive or repulsive forces, which allows for the manipulation of objects such as cells.

Non-autonomous trait

The phenomenon of a genetic mutation in one cell affecting the phenotype of other cells, regardless of their genotype

Orthologue

One of two or more functionally equivalent genes that are derived from a common ancestor.

Basal fungi

Four diverse fungal groups (arbuscular mycorrhizal fungi, microsporidia, chytrids and zygomycetes) that form the base of the fungal phylogenetic tree.

Oomycota

A phylogenetically distinct lineage of fungus-like eukaryotes.

Negative autotropism

A mode of behaviour in which cells actively grow away from one another.

Quorum sensing

Extracellular signalling that coordinates cellular behaviour according to population density.

Pseudohyphae

Chains of elongated cells that arise by budding.

G proteins

Guanine-nucleotide-binding proteins that coordinate extracellular-signal transmission and/or reception responses within a cell.

Metabolome

The complete set of cellular metabolites (including hormones, small-molecule signals and metabolite intermediates).

Antibiosis

Antagonistic interactions between two or more individuals that occur at a distance through the production of extracellular molecules.

Mycoparasitism

A situation in which one fungus parasitizes (that is, benefits at the expense of) a prey fungus.

Deletion collections

Collections of strains containing individuals that are derived from a common parent. Within the collection, each strain contains a single deletion of a predicted gene.

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Leeder, A., Palma-Guerrero, J. & Glass, N. The social network: deciphering fungal language. Nat Rev Microbiol 9, 440–451 (2011). https://doi.org/10.1038/nrmicro2580

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