title: Induced fungal resistance to insect grazing: reciprocal fitness consequences and fungal gene expression in the Drosophila-Aspergillus model system.
abstract: BACKGROUND
  Fungi are key dietary resources for many animals. Fungi, in consequence, have evolved sophisticated physical and chemical defences for repelling and impairing fungivores. Expression of such defences may entail costs, requiring diversion of energy and nutrients away from fungal growth and reproduction. Inducible resistance that is mounted after attack by fungivores may allow fungi to circumvent the potential costs of defence when not needed. However, no information exists on whether fungi display inducible resistance. We combined organism and fungal gene expression approaches to investigate whether fungivory induces resistance in fungi.
  
  
  RESULTS
  Here we show that grazing by larval fruit flies, Drosophila melanogaster, induces resistance in the filamentous mould, Aspergillus nidulans, to subsequent feeding by larvae of the same insect. Larval grazing triggered the expression of various putative fungal resistance genes, including the secondary metabolite master regulator gene laeA. Compared to the severe pathological effects of wild type A. nidulans, which led to 100% insect mortality, larval feeding on a laeA loss-of-function mutant resulted in normal insect development. Whereas the wild type fungus recovered from larval grazing, larvae eradicated the chemically deficient mutant. In contrast, mutualistic dietary yeast, Saccharomyces cerevisiae, reached higher population densities when exposed to Drosophila larval feeding.
  
  
  CONCLUSIONS
  Our study presents novel evidence that insect grazing is capable of inducing resistance to further grazing in a filamentous fungus. This phenotypic shift in resistance to fungivory is accompanied by changes in the expression of genes involved in signal transduction, epigenetic regulation and secondary metabolite biosynthesis pathways. Depending on reciprocal insect-fungus fitness consequences, fungi may be selected for inducible resistance to maintain high fitness in fungivore-rich habitats. Induced fungal defence responses thus need to be included if we wish to have a complete conception of animal-fungus co-evolution, fungal gene regulation, and multitrophic interactions.
authors.affiliation: Johann-Friedrich-Blumenbach Institute for Zoology and Anthropology, Georg-August-University Göttingen, Göttingen, Germany.
authors.forename: Silvia
authors.initials: S
authors.lastname: Caballero Ortiz
authors.forename: Monika
authors.initials: M
authors.lastname: Trienens
authors.forename: Marko
authors.initials: M
authors.lastname: Rohlfs
mesh_terms: D000818:Animals; D001233:Aspergillus nidulans / Q000235:genetics* / Q000276:immunology / Q000502:physiology*; D004331:Drosophila melanogaster / Q000382:microbiology*; D005247:Feeding Behavior / Q000502:physiology*; D005260:Female; D015966:Gene Expression Regulation, Fungal; D056084:Genetic Fitness; D007814:Larva / Q000502:physiology; D008954:Models, Biological
references.citation: PLoS One. 2012;7(7):e42238
references.pmid: 22860093
references.citation: Mycol Res. 2007 Nov;111(Pt 11):1345-51
references.pmid: 18023167
references.citation: Trends Ecol Evol. 2005 Nov;20(11):617-24
references.pmid: 16701445
references.citation: Trends Microbiol. 2007 Mar;15(3):109-18
references.pmid: 17276068
references.citation: Mol Ecol. 2011 Jul;20(14):3056-70
references.pmid: 21486374
references.citation: Mol Microbiol. 2012 Mar;83(5):1024-34
references.pmid: 22283524
references.citation: Toxicol Sci. 2010 Oct;117(2):418-26
references.pmid: 20643751
references.citation: Science. 2008 Jun 13;320(5882):1504-6
references.pmid: 18556559
references.citation: Appl Environ Microbiol. 2012 Jul;78(14):4869-73
references.pmid: 22582060
references.citation: Trends Plant Sci. 2011 Oct;16(10):524-31
references.pmid: 21782492
references.citation: Mol Ecol Resour. 2011 Mar;11(2):294-304
references.pmid: 21429136
references.citation: J Mol Med (Berl). 2006 Nov;84(11):901-10
references.pmid: 16972087
references.citation: FEMS Microbiol Lett. 2011 Aug;321(2):157-66
references.pmid: 21658102
references.citation: BMC Evol Biol. 2011 Jul 14;11:206
references.pmid: 21756302
references.citation: Nat Rev Microbiol. 2013 Jan;11(1):21-32
references.pmid: 23178386
references.citation: Nucleic Acids Res. 2009 Apr;37(6):e45
references.pmid: 19237396
references.citation: Microb Biotechnol. 2013 Sep;6(5):453-92
references.pmid: 23336673
references.citation: Toxins (Basel). 2012 Sep;4(9):695-717
references.pmid: 23105976
references.citation: Appl Environ Microbiol. 2012 Dec;78(23):8485-7
references.pmid: 23001676
references.citation: PLoS Genet. 2012;8(7):e1002816
references.pmid: 22829779
references.citation: Eukaryot Cell. 2004 Apr;3(2):527-35
references.pmid: 15075281
references.citation: J Am Chem Soc. 2012 Mar 14;134(10):4709-20
references.pmid: 22329759
references.citation: Oecologia. 2009 Oct;161(4):781-90
references.pmid: 19597847
references.citation: Neurotoxicology. 2011 Jan;32(1):123-9
references.pmid: 20971131
references.citation: Mol Microbiol. 2010 Aug;77(4):972-94
references.pmid: 20572938
references.citation: J Nat Prod. 2007 Apr;70(4):515-20
references.pmid: 17323993
references.citation: Biochimie. 2009 Feb;91(2):214-25
references.pmid: 18952140
references.citation: Oecologia. 1980 Jul;46(1):135-137
references.pmid: 28310639
references.citation: Chemistry. 2008;14(30):9100-10
references.pmid: 18601235
references.citation: Biochem J. 2010 Jan 15;425(3):553-65
references.pmid: 19878096
references.citation: Annu Rev Plant Biol. 2008;59:41-66
references.pmid: 18031220
references.citation: FEMS Microbiol Rev. 2012 Jan;36(1):1-24
references.pmid: 21658084
references.citation: Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14918-23
references.pmid: 22927395
references.citation: Front Zool. 2005 Jan 27;2(1):2
references.pmid: 15679898