Fungal Secondary Metabolism in the Light of Animal–Fungus Interactions: From Mechanism to Ecological Function

  • Marko RohlfsEmail author
Part of the Fungal Biology book series (FUNGBIO)


Animal grazing is a pervasive ecological factor threatening fungal fitness. This review summarizes the different approaches that have been used to test whether secondary metabolites serve as anti-fungivore defense agents. Assuming that secondary metabolites at least in part have evolved to mediate resistance against fungivores, this review evaluates the pros and cons of (1) using long-standing toxicity assays, (2) considering natural variation in fungal secondary metabolite formation, and (3) experiments with transgenic mutant fungi. Connecting inducible changes in fungal, molecular, genetic, biochemical, and morphological properties with fungivore behavioral and fitness assays is a new approach to investigate the functional relationship between secondary metabolite regulation and resistance against fungivores. Strengthening this dynamic view on fungus–fungivore interactions will certainly pave the way for a deeper understanding of how known (and still unknown) regulatory mechanisms act in concert with the biosynthesis of anti-fungivore compounds and the extent to which both constitutive and inducible variations in fungal chemical diversity represent an adaptation to animal grazing.


Adaptation Fungal defence Fungivory Genetic variation Inducibility Resistance Toxicity 



The work of M. R. is funded by the German Research Foundation (DFG), grant numbers RO3523/3-1, 3-2 and by the Georg-August-University of Göttingen.


  1. 1.
    Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites—strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22PubMedGoogle Scholar
  2. 2.
    Magan N, Aldred D (2007) Post-harvest control strategies: minimizing mycotoxins in the food chain. Int J Food Microbiol 119:131–139PubMedGoogle Scholar
  3. 3.
    Nielsen ML, Nielsen JB, Rank C, Klejnstrup ML, Holm DK, Brogaard KH et al (2011) A genome-wide polyketide synthase deletion library uncovers novel genetic links to polyketides and meroterpenoids in Aspergillus nidulans. FEMS Microbiol Lett 321:157–166PubMedGoogle Scholar
  4. 4.
    Sanchez JF, Somoza AD, Keller NP, Wang CCC (2012) Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat Prod Rep 29:351–371PubMedGoogle Scholar
  5. 5.
    Sarkar A, Funk AN, Scherlach K, Horn F, Schroeckh V, Chankhamjon P et al (2012) Differential expression of silent polyketide biosynthesis gene clusters in chemostat cultures of Aspergillus nidulans. J Biotechnol 160:64–71PubMedGoogle Scholar
  6. 6.
    Winter JM, Behnken S, Hertweck C (2011) Genomics-inspired discovery of natural products. Curr Opin Chem Biol 15:22–31PubMedGoogle Scholar
  7. 7.
    Deacon J (2006) Fungal biology. 4th ed. Blackwell, OxfordGoogle Scholar
  8. 8.
    Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11:481–487PubMedGoogle Scholar
  9. 9.
    Rodriguez-Romero J, Hedtke M, Kastner C, Müller S, Fischer R (2010) Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64:585–610PubMedGoogle Scholar
  10. 10.
    Bayram Ö Braus GH Fischer R Rodriguez-Romero J (2010) Spotlight on Aspergillus nidulans photosensory systems. Fungal Genet Biol 47:900–908PubMedGoogle Scholar
  11. 11.
    Bayram Ö, Braus GH (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins FEMS Microbiol Rev 36:1–24PubMedGoogle Scholar
  12. 12.
    Bayram Ö, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O et al (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506PubMedGoogle Scholar
  13. 13.
    Atoui A, Kastner C, Larey CM, Thokala R, Etxebeste O, Espeso EA et al (2010) Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet Biol. 47:962–972PubMedCentralPubMedGoogle Scholar
  14. 14.
    Schmidt-Heydt M, Rüfer C, Raupp F, Bruchmann A, Perrone G, Geisen R (2011) Influence of light on food relevant fungi with emphasis on ochratoxin producing species. Int J Food Microbiol 145:229–237PubMedGoogle Scholar
  15. 15.
    Chanda A, Roze LV, Kang S, Artymovich KA, Hicks GR, Raikhel NV et al (2009) A key role for vesicles in fungal secondary metabolism. Proc Natl Acad Sci U S A 106:19533–19538PubMedCentralPubMedGoogle Scholar
  16. 16.
    Schmidt-Heydt M, Magan N, Geisen R (2008) Stress induction of mycotoxin biosynthesis genes by abiotic factors. FEMS Microbiol Lett 284:142–149PubMedGoogle Scholar
  17. 17.
    Schmidt-Heydt M, Rüfer CE, Abdel-Hadi A, Magan N, Geisen R (2010) The production of aflatoxin B1 or G1 by Aspergillus parasiticus at various combinations of temperature and water activity is related to the ratio of aflS to aflR expression. Mycotoxin Res 26:241–246PubMedGoogle Scholar
  18. 18.
    Karlovsky P (2008) Secondary metabolites in soil ecology. In: Karlovsky P (ed) Secondary metabolites in soil ecology. Springer, Berlin Heidelberg, pp 1–22Google Scholar
  19. 19.
    Scherlach K, Graupner K, Hertweck C (2013) Molecular bacterial-fungal interactions with impact on the environment, food and medicine. Annu Rev Microbiol 67:375–397PubMedGoogle Scholar
  20. 20.
    Schroeckh V, Scherlach K, Nützmann H-W, Shelest E, Schmidt-Heck W, Schuemann J et al (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106:14558–14563PubMedCentralPubMedGoogle Scholar
  21. 21.
    Nützmann H-W, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, Gacek A et al (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci U S A 108:14282–14287PubMedCentralPubMedGoogle Scholar
  22. 22.
    Schoustra S, Rundle HD, Dali R, Kassen R (2010) Fitness-associated sexual reproduction in a filamentous fungus. Curr Biol 20:1350–1355PubMedGoogle Scholar
  23. 23.
    Sarikaya Bayram Ö, Bayram Ö, Valerius O, Park HS, Irniger S, Gerke J et al (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PloS Genet. 6:e1001226PubMedCentralPubMedGoogle Scholar
  24. 24.
    Illig J, Norton RA, Scheu S, Maraun M (2010) Density and community structure of soil- and bark-dwelling microarthropods along an altitudinal gradient in a tropical montane rainforest. Exp Appl Acarol 52:49–62PubMedCentralPubMedGoogle Scholar
  25. 25.
    Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26PubMedGoogle Scholar
  26. 26.
    Demain AL, Fang A (2000) The natural function of secondary metabolites. In: Sheper T (ed) Advances in biochemical engineering/biotechnology. Springer, Berlin, pp 1–39Google Scholar
  27. 27.
    Dowd PF (1992) Detoxification of mycotoxins by insects. In: Mullin CA, Scrott JG (eds) Molecular mechanisms of insecticide resistance. American Chemical Society, Washington, pp 264–275Google Scholar
  28. 28.
    Gloer JB (1995a) The chemistry of fungal antagonism and defense. Can J Bot 73:1265–1274Google Scholar
  29. 29.
    Janzen DH (1977) Why fruits rot, seeds mold and meat spoils. Am Nat 111:691–713Google Scholar
  30. 30.
    Marmeisse R, Nehls U, Öpik M, Selosse M-A, Pringle A (2013) Bridging mycorrhizal genomics, metagenomics and forest ecology. New Phytol 198:343–346PubMedGoogle Scholar
  31. 31.
    Rohlfs M, Churchill ACL (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48:23–34PubMedGoogle Scholar
  32. 32.
    Sherratt TN, Wilkinson DM, Bain RS (2005) Explaining dioscorides’ “double difference”: why are some mushrooms poisonous, and do they signal their unprofitability? Am Nat 166:767–775PubMedGoogle Scholar
  33. 33.
    Spiteller P (2008) Chemical defence strategies of higher fungi. Chem A Eur J 14:9100–9110Google Scholar
  34. 34.
    Castillo M-A, Moya P, Cantín A, Miranda MA, Primo J, Hernández E et al (1999) Insecticidal, anti-juvenile hormone, and fungicial activities of organic extracts from different Penicillium species and their isolated active components. J Agric Food Chem 47:2120–2124PubMedGoogle Scholar
  35. 35.
    Dowd PF, Miller JD, Greenhalgh R (1989) Toxicity and interactions of some Fusarium graminearum metabolites to caterpillars. Mycologia 81:646–650Google Scholar
  36. 36.
    Gloer JB, Rinderknecht B, Wicklow DT, Dowd PF (1989) Nominine: a new insecticidal indole diterpene from the sclerotia of Aspergillus nomius. J Org Chem 54:2530–2532Google Scholar
  37. 37.
    Grove JF, Pople M (1981) The insecticidal activity of some fungal dihydroisocoumarins. Mycopathologia 76:65–67Google Scholar
  38. 38.
    Ondeyka JG, Dombrowski AW, Polishook JP, Felcetto T, Shoop WL, Guan Z et al (2003) Isolation and insecticidal activity of mellamide from Aspergillus melleus. J Ind Microbiol Biotechnol 30:220–224PubMedGoogle Scholar
  39. 39.
    Paz Z, Bilkis I, Gerson U, Kerem Z, Sztejnberg A (2011) Argovin, a novel natural product secreted by the fungus Meira argovae, is antagonistic to mites. Entomol Exp Appl 140:247–253Google Scholar
  40. 40.
    Paterson RRM, Simmonds MSJ, Blaney WM (1987) Mycopesticidal effects of characterized extracts of Penicillium isolates and purified secondary metabolites (including mycotoxins) on Drosophila melanogaster and Spodoptora littoralis. J Invertebr Pathol 50:124–133Google Scholar
  41. 41.
    Reiss J (1975) Insecticidal and larvicidal activities of the mycotoxins aflatoxin B1, rubratoxin B, patulin and diacetoxyscirpenol towards Drosophila melanogaster. Chem Biol Interact 10:339–342PubMedGoogle Scholar
  42. 42.
    Wicklow DT, Dowd PF, Gloer JB (1994) Antiisectan effects of Aspergillus metabolites. In: Powell KA, Renwick A, Peberdy JF (eds) The genus Aspergillus: from taxonomy and genetics to industrial applications. FEMS Symposium Series, vol 69. Plenum, New York, pp 93–114Google Scholar
  43. 43.
    Obana H, Kumeda Y, Nishimune T, Usami Y (1994) Direct detection using the Drosophila DNA-repair test and isolation of a DNA-damaging mycotoxin, 5,6-dihydropenicillic acid, in fungal culture. Food Chem Toxicol 32:37–43PubMedGoogle Scholar
  44. 44.
    Stark AA (1980) Mutagenicity and carcinogenicity of mycotoxins: DNA binding as a possible mode of action. Annu Rev Microbiol 34:235–262PubMedGoogle Scholar
  45. 45.
    Dowd PF (1988) Synergism of aflatoxin B1 toxicity with the co-occurring fungal metabolite kojic acid to two caterpillars. Entomol Exp Appl. 47:69–71Google Scholar
  46. 46.
    Chinnici JP, Gunst K, Llewellyn GC (1983) Effects of mycotoxin pretreatment on aflatoxin B1 post-treatment toxicity in Drosophila melanogaster (Diptera). J Invertebr Pathol 41:321–327PubMedGoogle Scholar
  47. 47.
    Brodhun F, Schneider S, Gobel C, Hornung E, Feussner I (2010) PpoC from Aspergillus nidulans is a fusion protein with only one active haem. Biochem J 425:553–565PubMedGoogle Scholar
  48. 48.
    Combet E, Eastwood DC, Burton KS, Henderson J (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326Google Scholar
  49. 49.
    Sawahata T, Shimano S, Suzuki M (2008) Tricholoma matsutake 1-octen-3-ol and methyl cinnamate repel mycophagous Proisotoma minuta (Collembola: Insecta). Mycorrhiza 18:111–114PubMedCentralPubMedGoogle Scholar
  50. 50.
    Inamdar AA, Masurekar P, Bennett JW (2010) Neurotoxicity of fungal volatiles organic compounds in Drosophila melanogaster. Toxicol Sci 117:418–426PubMedGoogle Scholar
  51. 51.
    Nakamori T, Suzuki A (2006) Repellency of injured ascomata of Ciborinia camelliae and Spathularia flavida to fungivorous collembolans. Mycoscience 47:290–292Google Scholar
  52. 52.
    Bengtsson G, Hedlund K, Rundgren S (1991) Selective odor perception in the soil Collembola Onychirus armatus. J Chem Ecol 17:2113–2125PubMedGoogle Scholar
  53. 53.
    Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odour discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869–875Google Scholar
  54. 54.
    Pierce AM, Pierce HD Jr, Borden JH, Oehlschlager AC (1991) Fungal volatiles: semiochemicals for stored-product beetles (Coleoptera: Cucujidae). J Chem Ecol 17:581–597PubMedGoogle Scholar
  55. 55.
    Wood WF, Archer CL, Largent DL (2001) 1-Octen-3-ol, a banana slug antifeedant from mushrooms. Biochem Syst Ecol 29:531–533PubMedGoogle Scholar
  56. 56.
    Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L et al (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357PubMedGoogle Scholar
  57. 57.
    Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trend Microbiol 15:109–118Google Scholar
  58. 58.
    Wright VF, Casas ED LAS, Harein PK (1980a) Evaluation of Penicillium mycotoxins for activity in stored-product Coleoptera. Environ Entomol 9:217–221Google Scholar
  59. 59.
    Tsai W-T, Mason LJ, Woloshuk CP (2007) Effect of three stored-grain fungi on the development of Typhaea stercorea. J Stored Prod Res 43:129–133Google Scholar
  60. 60.
    Niu G, Wen Z, Rupasinghe SG, Zeng RS, Berenbaum MR, Schuler MA (2008) Aflatoxin B1 detoxification by CYP321A1 in Helicoverpa zea. Arch Insect Biochem Physiol 69:32–45PubMedGoogle Scholar
  61. 61.
    Zeng RS, Wen Z, Niu G, Schuler MA, Berenbaum MR (2007) Allelochemical induction of cytochrome P450 monooxygenases and amelioration of xenobiotic toxicity in Helicoverpa zea. J Chem Ecol 33:449–461PubMedGoogle Scholar
  62. 62.
    Jaenike J, Grimaldi DA, Sluder AE, Greenleaf AL (1983) α-Amanitin tolerance in mycophagous Drosophila. Science 221:165–167PubMedGoogle Scholar
  63. 63.
    Stump AD, Jablonski SE, Bouton L, Wilder JA (2011) Distribution and mechanism of α-amanitin tolerance in mycophagous Drosophila (Diptera: Drosophilidae). Environ Entomol 40:1604–1612PubMedGoogle Scholar
  64. 64.
    Trienens M, Rohlfs M (2011) Experimental evolution of defense against a competitive mold confers reduced sensitivity to fungal toxins but no increased resistance in Drosophila larvae. BMC Evol Biol 11:206PubMedCentralPubMedGoogle Scholar
  65. 65.
    Wicklow DT, Dowd PF (1989) Entomotoxigenic potential of wild and domesticated yellow-green Aspergilli: toxicity to corn earworm and fall armyworm larvae. Mycologia 81:561–566Google Scholar
  66. 66.
    Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, Dean RA et al (2006) Whole genome comparison of Aspergillus flavus and A. oryzae. Med Mycol 44:9–11Google Scholar
  67. 67.
    Shaw PJA (1988) A consistent hierarchy in the fungal feeding preference of the Collembola Onychiurus armatus. Pedobiologia 39:179–187Google Scholar
  68. 68.
    Wright VF, Harein PK, Collins NA (1980b) Preference of the confused flour beetle for certain Penicillium isolates. Environ Entomol 9:4Google Scholar
  69. 69.
    Belofsky GN, Gloer JB, Wicklow DT, Dowd PF (1995) Antiinsectan alkaloids: shearinines A-C and a new paxilline derivative from the ascostromata of Eupenicillium shearii. Tetrahedron 51:3959–3968Google Scholar
  70. 70.
    Gloer JB (1995b) Antiisectan natural products from fungal sclerotia. Acc Chem Res 28:343–350Google Scholar
  71. 71.
    Wang H, Gloer J, Wicklow D, Dowd P (1995) Aflavinines and other antiinsectan metabolites from the ascostromata of Eupenicillium crustaceum and related species. Appl Environ Microbiol 61:4429–4435Google Scholar
  72. 72.
    Whyte AC, Gloer JB (1996) Sclerotiamide: a new member of the paraherquamide class with potent antiisectan activity from the sclerotia of Aspergillus sclerotiorum. J Nat Prod 59:1093–1095PubMedGoogle Scholar
  73. 73.
    Wicklow DT, Shotwell OL (1983) Intrafungal distribution of aflatoxins among conidia and sclerotia of Aspergillus flavus and Aspergillus parasiticus. Can J Microbiol 29:1–5PubMedGoogle Scholar
  74. 74.
    Wicklow DT, Dowd PF, Alfatafta AA, Gloer JB (1996) Ochratoxin A: an antiinsectan metabolite from the sclerotia of Aspergillus carbonarius NRRL 369. Can J Microbiol 42:1100–1103PubMedGoogle Scholar
  75. 75.
    Wicklow DT, Dowd PF, Tepaske MR, Gloer JB (1988) Sclerotial metabolites of Aspergillus flavus toxic to a detritivorous maize insect (Carpophilus hemipterus, Nitidulidae). Trans Br Mycol Soc 91:433–438Google Scholar
  76. 76.
    Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores—their interaction with secondary plant metabolites. Academic, New York, pp. 3–54Google Scholar
  77. 77.
    Cary JW, Harris-Coward PY, Ehrlich KC, Di Mavungu JD, Malysheva SV, De Saeger S et al (2014) Functional characterization of a veA-dependent polyketide synthase gene in Aspergillus flavus necessary for the synthesis of asparasone, a sclerotium-specific pigment. Fung Genet Biol 64:25–35Google Scholar
  78. 78.
    Caballero Ortiz S Trienens M Rohlfs M (2013) Induced fungal resistance to insect grazing: reciprocal fitness consequences and fungal gene expression in the Drosophila-Aspergillus model system. PLoS One 8:e74951PubMedCentralPubMedGoogle Scholar
  79. 79.
    Janssens TKS, Staaden S, Scheu S, Mariën J, Ylstra B, Roelofs D (2010) Transcriptional responses of Folsomia candida upon exposure to Aspergillus nidulans secondary metabolites in single and mixed diets. Pedobiologia 54:45–52Google Scholar
  80. 80.
    Rohlfs M, Albert M, Keller NP, Kempken F (2007) Secondary chemicals protect mould from fungivory. Biol Lett 3:523–525PubMedCentralPubMedGoogle Scholar
  81. 81.
    Staaden S, Milcu A, Rohlfs M, Scheu S (2011) Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour. Soil Biol Biochem 43:1411–1416Google Scholar
  82. 82.
    Stötefeld L, Scheu S, Rohlfs M (2012) Fungal chemical defense alters density-dependent foraging ehaviour and success in a fungivorous soil arthropod. Ecol Entomol 37:323–329Google Scholar
  83. 83.
    Trienens M, Keller NP, Rohlfs M (2010) Fruit, flies and filamentous fungi—experimental analysis of animal-microbe competition using Drosophila melanogaster and Aspergillus as a model system. Oikos 119:1765–1775Google Scholar
  84. 84.
    Trienens M, Rohlfs M (2012) Insect-fungus interference competition—the potential role of global secondary metabolite regulation, pathway-specific mycotoxin expression and formation of oxylipins. Fungal Ecol 5:191–199Google Scholar
  85. 85.
    Yin W-B, Amaike S, Wohlbach DJ, Gasch AP, Chiang Y-M, Wang CCC et al (2012) An Aspergillus nidulans bZIP response pathway hardwired for defensive secondary metabolism operates through aflR. Mol Microbiol 83:1024–1034PubMedCentralPubMedGoogle Scholar
  86. 86.
    Scheu S, Folger M (2004) Single and mixed diets in Collembola: effects on reproduction and stable isotope fractionation. Funct Ecol 18:94–102Google Scholar
  87. 87.
    Scheu S, Simmerling F (2004) Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets. Oecologia 139:347–353PubMedGoogle Scholar
  88. 88.
    Balogh J, Tunlid A, Rosén S (2003) Deletion of a lectin gene does not affect the phenotype of the nematode-trapping fungus Arthrobotrys oligospora. Fung Genet Biol 39:128–135Google Scholar
  89. 89.
    Palmer JM, Keller NP (2010) Secondary metabolism in fungi: does chromosomal location matter? Curr Opin Microbiol 13:431–436PubMedCentralPubMedGoogle Scholar
  90. 90.
    Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3:527–535PubMedCentralPubMedGoogle Scholar
  91. 91.
    Kale SP, Milde L, Trapp MK, Frisvad JC, Keller NP, Bok JW (2008) Requirement of LaeA for secondary metabolism and sclerotial production in Aspergillus flavus. Fungal Genet Biol 45:1422–1429PubMedCentralPubMedGoogle Scholar
  92. 92.
    Karimi-Aghcheh R, Bok JW, Phatale PA, Smith KM, Baker SE, Lichius A et al (2013) Functional analyses of Trichoderma reesei LAE1 reveal conserved and contrasting roles of this regulator. G3 3:369–378Google Scholar
  93. 93.
    Kim H-K, Lee S, Jo S-M, McCormick SP, Butchko RAE, Proctor RH et al (2013) Functional roles of FgLaeA in controlling secondary metabolism, sexual development, and virulence in Fusarium graminearum. PLoS One 8:e68441PubMedCentralPubMedGoogle Scholar
  94. 94.
    Kosalková K, García-Estrada C, Ullán R V, Godio RP, Feltrer R, Teijeira F et al (2009) The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum. Biochimie 91:214–225PubMedGoogle Scholar
  95. 95.
    Perrin RM, Fedorova ND, Bok JW, Cramer RA Jr, Wortman JR, Kim HS et al (2007) Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 3:e50PubMedCentralPubMedGoogle Scholar
  96. 96.
    Wiemann P, Brown DW, Kleigrewe K, Bok JW, Keller NP, Humpf H-U et al (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77:972–994PubMedCentralPubMedGoogle Scholar
  97. 97.
    Wu D, Oide S, Zhang N, Choi MY, Turgeon BG (2012) ChLae1 and ChVel1 regulate T-toxin production, virulence, oxidative stress response, and development of the maize pathogen Cochliobolus heterostrophus. PLoS Pathog 8:e1002542PubMedCentralPubMedGoogle Scholar
  98. 98.
    Albert M (2007) Der Einfluss des Sekundärmetabolismus von Aspergillus nidulans auf Reproduktion, Überleben und Nahrungswahl pilzfressender Collembolen. Christian-Albrechts Universität Kiel. p. 43Google Scholar
  99. 99.
    Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050PubMedGoogle Scholar
  100. 100.
    Duhamel M, Pel R, Ooms A, Bücking H, Jansa J, Ellers J et al (2013) Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology 94:2019–2029PubMedGoogle Scholar
  101. 101.
    Crowther TW, Boddy L, Jones TH (2011a) Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167:535–545PubMedGoogle Scholar
  102. 102.
    Crowther TW, Jones TH, Boddy L, Baldrian P (2011b) Invertebrate grazing determines enzyme production by basidiomycete fungi. Soil Biol Biochem 43:2060–2068Google Scholar
  103. 103.
    Hedlund K, Boddy L, Preston CM (1991) Mycelial responses of the soil fungus, Mortierella isabellina, to grazing by Onychiurus armatus (Collembola). Soil Biol Biochem 23:361–366Google Scholar
  104. 104.
    Kampichler C, Rolschewski J, Donnelly DP, Boddy L (2004) Collembolan grazing affects the growth strategy of the cord-forming fungus Hypholoma fasciculare. Soil Biol Biochem 36:591–599Google Scholar
  105. 105.
    Bretherton S, Tordoff GM, Jones TH, Lynne Boddy (2006) Compensatory growth of Phanerochaete velutina ehavio systems grazed by Folsomia candida (Collembola). FEMS Microbiol Ecol 58:33–40PubMedGoogle Scholar
  106. 106.
    Bleuler-Martínez S, Butschi A, Garbani M, Wälti MA, Wohlschlager T, Potthoff E et al (2011) A lectin-mediated resistance of higher fungi against predators and parasites. Mol Ecol 20:3056–3070PubMedGoogle Scholar
  107. 107.
    Vasconcelos IM, Oliveira JTA (2004) Antinutritional properties of plant lectins. Toxicon 44:385–403PubMedGoogle Scholar
  108. 108.
    Lakkireddy KKR, Navarro-González M, Velagapudi R, Kües U (2011) Proteins expressed during hyphal aggregation for fruiting body formation in basidiomycetes. In: Savoie J-M, Foulongne-Oriol M, Largeteau M, Barroso G (eds) Proceedings of the 7th international conference on mushroom biology and mushroom products; 4–7 Oct 2011, Arcachon, France. INRA, Bordeaux, pp. 82–94Google Scholar
  109. 109.
    May GS. Mitogen-activated protein kinase pathways in Aspergilli. In Goldman GH, Osmani SA (eds) The Aspergilli—genomics, medical aspects, biotechnology, and research methods. Taylor & Francis, Boca Raton, 2007. pp. 121–128Google Scholar
  110. 110.
    Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531PubMedGoogle Scholar
  111. 111.
    Nielsen MT, Klejnstrup M, Rohlfs M, Anyaogu DC, Nielsen JB, Gotfredsen CH et al (2013) Aspergillus nidulans synthesize insect juvenile hormones upon expression of a heterologous regulatory protein and in response to grazing by Drosophila melanogaster larvae. PLoS One 8:e73369PubMedCentralPubMedGoogle Scholar
  112. 112.
    Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone behaviour pathway in insect development. Ann Rev Entomol 58:181–204Google Scholar
  113. 113.
    Döll K, Chatterjee S, Scheu S, Karlovsky P, Rohlfs M (2013) Fungal metabolic plasticity and sexual development mediate induced resistance to arthropod fungivory. Proc R Soc B Biol Sci 280:20131219Google Scholar
  114. 114.
    Chiang Y-M, Szewczyk E, Nayak T, Davidson AD, Sanchez JF, Lo H-C et al (2008) Molecular genetic mining of the Aspergillus secondary metabolome: discovery of the emericellamide biosynthetic pathway. Chem Biol 15:527–532PubMedCentralPubMedGoogle Scholar
  115. 115.
    Lo H-C, Entwistle R, Guo C-J, Ahuja M, Szewczyk E, Hung J-H et al (2012) Two separate gene clusters encode the biosynthetic pathway for the meroterpenoids austinol and dehydroaustinol in Aspergillus nidulans. J Am Chem Soc 134:4709–44720PubMedCentralPubMedGoogle Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.J.F. Blumenbach Institute of Zoology and AnthropologyGeorg-August-University GöttingenGöttingenGermany

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