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Volatile sesquiterpenes from fungi: what are they good for?

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Abstract

Fungi can be found in almost all sorts of habitats competing with an even higher number of other organisms. As a consequence fungi developed a number of strategies for protection and communication with other organisms. This review focuses on the increasing number of volatile sesquiterpenes found to be produced by fungal species. The remarkable diversity of this type of volatile organic compound (VOC) within the kingdom fungi is presented and their benefits for the fungi are discussed. The majority of these compounds are hydrocarbons comprising several dozens of carbon skeletons. Together with oxygenated sesquiterpenes they include compounds unique to fungi. Only in recent years the interest shifted from a mere detection and characterization of compounds to their biological function. This review reveals highly diverse ecological functions including interactions with bacteria, other fungi, insects and plants. VOCs act as autoinducer, defend against competing species and play essential roles in attracting pollinators for spreading fungal spores. For many sesquiterpene VOCs sophisticated responses in other organisms have been identified. Some of these interactions are complex involving several partners or transformation of the emitted sesquiterpene. A detailed description of ecological functions of selected sesquiterpenes is given as well as their potential application as marker molecules for detection of mould species. Structures of all described sesquiterpenes are given in the review and the biosynthetic routes of the most common skeletons are presented. Summarizing, this article provides a detailed overview over the current knowledge on fungal sesquiterpene VOCs and gives an outlook on the future developments.

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References

  • Abate D, Abraham WR (1994) Antimicrobial metabolites from Lentinus crinitus. J Antibiot 47:1348–1350

    PubMed  CAS  Google Scholar 

  • Abraham W-R (2001) Bioactive sesquiterpenes produced by fungi: are they useful for humans as well? Curr Med Chem 8:583–606

    PubMed  CAS  Google Scholar 

  • Abraham W-R, Hanssen H-P (1987) Fragrance compounds from fungal liquid cultures. II. New benzofuran-terpenoids from Cystostereum murraii. In: Proceedings of 4th European congress on biotechnology, Amsterdam/NL, vol 3, pp 294–296

  • Abraham W-R, Ernst L, Witte L, Hanssen H-P, Sprecher E (1986) New trans-fused africanols from Leptographium lundbergii. Tetrahedron 42:4475–4480

    Article  CAS  Google Scholar 

  • Abraham W-R, Sprecher E, Hanssen H-P (1987) Accumulation of africanols in liquid cultures of Leptographium lundbergii. Flavor Fragr J 2:175–177

    Article  CAS  Google Scholar 

  • Abraham W-R, Hanssen H-P, Möhringer C (1988) Novel sesquiterpene ethers from liquid cultures of the wood-rotting fungus Lentinus lepideus. Z Naturforsch 43c:24–28

    Google Scholar 

  • Abraham W-R, Ernst L, Stumpf B (1990) Biotransformation of caryophyllene by Diplodia gossypina. Phytochemistry 29:115–120

    Article  CAS  Google Scholar 

  • Abraham W-R, Hanssen H-P, Urbasch I (1991) Lepistirones, major volatile metabolites from liquid cultures of Lepista irina (Basidiomycotina). Z Naturforsch 46c:169–171

    Google Scholar 

  • Agger S, Lopez-Gallego F, Schmidt-Dannert C (2009) Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Mol Microbiol 72:1181–1195

    Article  PubMed  CAS  Google Scholar 

  • Ainsworth AM, Rayner ADM, Broxholme SJ, Beeching JR, Pryke JA, Scard PR, Berriman J, Powell KA, Floyd AJ, Branch SK (1990) Production and properties of the sesquiterpene, (+)-torreyol, in degenerative mycelial interactions between strains of Stereum. Mycol Res 94:799–809

    Article  CAS  Google Scholar 

  • Andersen B, Frisvad JC, Søndergaard I, Rasmussen IS, Larsen LS (2011) Associations between fungal species and water-damaged building materials. Appl Environ Microbiol 77:4180–4188

    Article  PubMed  CAS  Google Scholar 

  • Anderson B, Terblanche JS, Ellis AG (2010) Predictable patterns of trait mismatches between interacting plants and insects. BMC Evol Biol 10:204

    Article  PubMed  Google Scholar 

  • Asakawa Y, Ishida T, Toyota M, Takemoto T (1986) Terpenoid biotransformation in mammals. IV biotransformation of (+)-longifolene, (−)-caryophyllene, (−)-caryophyllene oxide, (−)-cyclocolorenone, (+)-nootkatone, (−)-elemol, (−)-abietic acid and (+)-dehydroabietic acid in rabbits. Xenobiotica 16:753–767

    Article  PubMed  CAS  Google Scholar 

  • Audouin P, Vidal JP, Richard H (1989) Volatile compounds from aroma of some edible mushrooms: morel (Morchella conica), wood blewit (Lepista nuda), clouded agaric (Clitocybe nebularis) and false chanterelle (Hygrophoropsis aurantiaca). Sci Aliments 9:185–193

    CAS  Google Scholar 

  • Ayer WA, Saeedi-Ghomi MH (1981) 1-Sterpurene-3,12,14-triol and 1-sterpurene, metabolites of silver-leaf disease fungus Stereum purpureum. Can J Chem 59:2536–2538

    Article  CAS  Google Scholar 

  • Ayoub N, Lass D, Schultze W (2009) Volatile constituents of the medicinal fungus chaga Inonotus obliquus (Pers.: Fr.) Pilát (Aphyllophoromycetideae). Int J Med Mushrooms 11:55–60

    Article  CAS  Google Scholar 

  • Back K, He S, Kim KU, Shin DH (1998) Cloning and bacterial expression of sesquiterpene cyclase, a key branch point enzyme for the synthesis of sesquiterpenoid phytoalexin capsidiol in UV-challenged leaves of Capsicum annuum. Plant Cell Physiol 39:899–904

    PubMed  CAS  Google Scholar 

  • Bahn YS, Xue C, Idnurm A, Rutherford JC, Heitman J, Cardenas ME (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5:57–69

    Article  PubMed  CAS  Google Scholar 

  • Benedict CR, Lu J-L, Pettigrew DW, Liu J, Stipanovic RD, Williams HJ (2001) The cyclization of farnesyl diphosphate and nerolidyl diphosphate by a purified recombinant δ-cadinene synthase. Plant Physiol 125:1754–1765

    Article  PubMed  CAS  Google Scholar 

  • Bicchi C, Cordero C, Liberto E, Rubiolo P, Sgorbini B (2004) Automated headspace solid-phase dynamic extraction to analyse the volatile fraction of food matrices. J Chromatogr A 1024:217–226

    Article  PubMed  CAS  Google Scholar 

  • Börjesson T, Stöllman U, Schnürer J (1990) Volatile metabolites and other indicators of Penicillium aurantiogriseum growth on different substrates. Appl Environ Microbiol 56:3705–3710

    PubMed  Google Scholar 

  • Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites—strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22

    Article  PubMed  CAS  Google Scholar 

  • Brehm-Stecher BF, Johnson EA (2003) Sensitization of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol, and apritone. Antimicrob Agents Chemother 47:3357–3360

    Article  PubMed  CAS  Google Scholar 

  • Bruheim I, Liu X, Pawliszyn J (2003) Thin-film microextraction. Anal Chem 75:1002–1010

    Article  PubMed  CAS  Google Scholar 

  • Calvert MJ, Ashton PR, Allemann RK (2002) Germacrene A is a product of the aristolochene synthase-mediated conversion of farnesylpyrophosphate to aristolochene. J Am Chem Soc 124:11636–11641

    Article  PubMed  CAS  Google Scholar 

  • Cane DE (1990) Enzymatic formation of sesquiterpenes. Chem Rev 90:1089–1103

    Article  CAS  Google Scholar 

  • Cane DE, King GGS (1976) The biosynthesis of ovalicin: Isolation of β-trans-bergamotene. Tetrahedron Lett 17:4737–4740

    Article  Google Scholar 

  • Cane DE, Rawlings BJ, Yang C-C (1987) Isolation of (−)-γ-cadinene and aristolochene from Aspergillus terreus. J Antibiot 40:1331–1334

    PubMed  CAS  Google Scholar 

  • Chang S-T, Chen P-F, Wang S-Y, Wu H-H (2001) Antimite activity of essential oils and their constituents from Taiwania cryptomerioides. J Med Entomol 38:455–457

    Article  PubMed  CAS  Google Scholar 

  • Chang HT, Cheng YH, Wu CL, Chang ST, Chang TT, Su YC (2008) Antifungal activity of essential oil and its constituents from Calocedrus macrolepis var. formosana Florin leaf against plant pathogenic fungi. Bioresour Technol 99:6266–6270

    Article  PubMed  CAS  Google Scholar 

  • Clericuzio M, Toma L, Vidari G (1999) Isolation of a new caryophyllane ester from Lactarius subumbonatus: conformational analysis and absolute configuration. Eur J Org Chem 2059–2065

  • Crespo R, Pedrini N, Juárez MP, Dal Bello GM (2008) Volatile organic compounds released by the entomopathogenic fungus Beauveria bassiana. Microbiol Res 163:148–151

    Article  PubMed  CAS  Google Scholar 

  • Cugini C, Calfee MW, Farrow JM III, Morales DK, Pesci EC, Hogan DA (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65:896–906

    Article  PubMed  CAS  Google Scholar 

  • Cushion MT, Collins MS, Linke MJ (2009) Biofilm formation by Pneumocystis spp. Eukaryot Cell 8:197–206

    Article  PubMed  CAS  Google Scholar 

  • Daniewski WM, Grieco PA, Huffman JC, Rymkiewicz A, Wawrzun A (1981) Isolation of 12-hydroxycaryophyllene-4,5-oxide, a sesquiterpene from Lactarius camphoratus. Phytochemistry 20:2733–2734

    Article  CAS  Google Scholar 

  • Davis-Hanna A, Piispanen AE, Stateva LI, Hogan DA (2008) Farnesol and dodecanol effects on the Candida albicans Ras1-cAMP signalling pathway and the regulation of morphogenesis. Mol Microbiol 67:47–62

    Article  PubMed  CAS  Google Scholar 

  • de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897

    Article  PubMed  CAS  Google Scholar 

  • Demyttenaere JCR, Morina RM, Sandra P (2003) Monitoring and fast detection of mycotoxin-producing fungi based on headspace solid-phase microextraction and headspace sorptive extraction of the volatile metabolites. J Chromatogr A 985:127–135

    Article  PubMed  CAS  Google Scholar 

  • Desjardins AE, Hohn TM, McCormick SP (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Rev 57:595–604

    PubMed  CAS  Google Scholar 

  • Deveau A, Piispanen AE, Jackson AA, Hogan DA (2010) Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the Ras-cyclic AMP signaling pathway. Eukaryot Cell 9:569–577

    Article  PubMed  CAS  Google Scholar 

  • Dichtl K, Ebel F, Dirr F, Routier FH, Heesemann J, Wagener J (2010) Farnesol misplaces tip-localized Rho proteins and inhibits cell wall integrity signalling in Aspergillus fumigatus. Mol Microbiol 76:1191–1204

    Article  PubMed  CAS  Google Scholar 

  • Dictionary of Natural Compounds (2008) Chapman and Hall Chemical Database, London

  • Dorn F, Arigoni D (1974) Ein bicyclischer Abkömmling von (−)-Longifolen aus Helminthosporium sativum und H. victoriae. Experientia 30:851–852

    Article  CAS  Google Scholar 

  • Duhl TR, Helmig D, Guenther A (2007) Sesquiterpene emissions from vegetation: a review. Biogeosci Discuss 4:3987–4023

    Article  Google Scholar 

  • Egli S, Gfeller H, Bigler P, Schlunegger U-P (1988) Isolierung und Identifikation des Sesquiterpenalkohols (±)-Torreyol aus Reinkulturen des Ektomykorrhizapilzes Cortinarius odorifer Britz. Eur J For Path 18:351–356

    Article  Google Scholar 

  • Fäldt J, Jonsell M, Nordlander G, Borg-Karlson A-K (1999) Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J Chem Ecol 25:567–590

    Article  Google Scholar 

  • Fekete C, Logrieco A, Giczey G, Hornok L (1997) Screening of fungi for the presence of the trichodiene synthase encoding sequence by hybridization to the Tri5 gene cloned from Fusarium poae. Mycopathologia 138:91–97

    Article  PubMed  CAS  Google Scholar 

  • Fischer G, Schwalbe R, Möller M, Ostrowski R, Dott W (1999) Species-specific production of microbial volatile organic compounds (MVOC) by airborne fungi from a compost facility. Chemosphere 39:795–810

    Article  PubMed  CAS  Google Scholar 

  • Fravel DR, Connick WJ Jr, Grimm CC, Lloyd SW (2002) Volatile compounds emitted by sclerotia of Sclerotinia minor, Sclerotinia sclerotiorum, and Sclerotium rolfsii. J Agric Food Chem 50:3761–3764

    Article  PubMed  CAS  Google Scholar 

  • Gams W (2007) Biodiversity of soil-inhabiting fungi. Biodivers Conserv 16:69–72

    Article  Google Scholar 

  • Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 156:3814–3829

    Article  PubMed  CAS  Google Scholar 

  • Gross B, Gallois A, Spinnler H-E, Langlois D (1989) Volatile compounds produced by the lignilolytic fungus Phlebia radiata Fr. (Basidiomycotes) and influence of strain specificity on the odorous profile. J Biotechnol 10:303–308

    Article  CAS  Google Scholar 

  • Halls SC, Gang DR, Weber DJ (1994) Seasonal variation in volatile secondary compounds of Chrysothamnus nauseosus (Pallas) Britt.; Asteraceae ssp. hololeucus (Gray) Hall. & Clem. influences herbivory. J Chem Ecol 20:2055–2063

    Article  CAS  Google Scholar 

  • Hanssen H-P (1982) Sesquiterpene hydrocarbons from Lentinus lepideus. Phytochemistry 21:1159–1160

    Article  CAS  Google Scholar 

  • Hanssen H-P (1985a) Sesquiterpenes and other volatile metabolites from liquid cultures of Ceratocystis populina (Ascomycota)-essential oil compounds from fungi. In: Baerheim Svendsen A, Scheffer JIC (eds) Essential oils and aromatic plants. Martinus Nyhoff/Dr W. Junk Publishers, Dordrecht, pp 173–177

  • Hanssen H-P (1985b) Sesquiterpene alcohols from Lentinus lepideus. Phytochemistry 24:1293–1294

    Article  CAS  Google Scholar 

  • Hanssen H-P (2002) Von einer Laborspielerei zur Biotechnologie. Pharmazeutische Zeitung, issue 47. http://www.pharmazeutische-zeitung.de/index.php?id=24721

  • Hanssen H-P, Abraham W-R (1986) Volatiles from liquid cultures of Lentinellus cochleatus (Basidiomycotina). Z Naturforsch 41c:959–962

    Google Scholar 

  • Hanssen H-P, Abraham W-R (1988) Sesquiterpene alcohols with novel skeletons from the fungus Ceratocystis piceae (Ascomycotina). Tetrahedron 44:2175–2180

    Article  CAS  Google Scholar 

  • Hanssen H-P, Sinnwell V, Abraham W-R (1986a) Volatile fragrance compounds from the fungus Gloeophyllum odoratum (Basidiomycotina). Z Naturforsch 41c:825–829

    Google Scholar 

  • Hanssen H-P, Sprecher E, Abraham W-R (1986b) 6-Protoilludene, the major volatile metabolite from Ceratocystis piceae liquid cultures. Phytochemistry 25:1979–1980

    Article  CAS  Google Scholar 

  • Hanssen H-P, Sprecher E, Klingenberg A (1986c) Screening for volatile terpenes in yeasts. In: Brunke H (ed) Progress in essential oil research. Walter de Gruyter, Berlin, pp 395–403

    Google Scholar 

  • Harborne JB (2001) Twenty-five years of chemical ecology. Nat Prod Rep 18:361–379

    Article  PubMed  CAS  Google Scholar 

  • Hawksworth DC, Rossman AY (1987) Where are the undescribed fungi? Phytopathology 87:888–891

    Article  Google Scholar 

  • Hellwig V, Dasenbrock J, Schumann ST, Steglich W, Leonhardt K, Anke T (1998) New triquinane-type sesquiterpenoids from Macrocystidia cucumis (Basidiomycetes). Eur J Org Chem 73–79

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking 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, Kõljalg 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, Schüssler 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 

  • Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67:2982–2992

    Article  PubMed  CAS  Google Scholar 

  • Hubbell SP, Wiemer DF, Adejare A (1983) An antifungal terpenoid defends a neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia 60:321–327

    Article  Google Scholar 

  • Hynes J, Müller CT, Jones TH, Boddy L (2007) Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol 33:43–57

    Article  PubMed  CAS  Google Scholar 

  • Inoue Y, Shiraishi A, Hada T, Hirose K, Hamashima H, Shimada J (2004) The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiol Lett 237:325–331

    PubMed  CAS  Google Scholar 

  • Jabra-Rizk MA, Meiller TF, James CE, Shirtliff ME (2006) Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial susceptibility. Antimicrob Agents Chemother 50:1463–1469

    Article  PubMed  CAS  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox C, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold EA, Amtoft A, Stajich JE, Hosaka K, Sung G-H, 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 PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton J, 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 D, Spatafora J, Vilgalys R (2006) Reconstructing the early evolution of the fungi using a six gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • Jelen HH (2002) Volatile sesquiterpene hydrocarbons characteristic for Penicillium roqueforti strains producing PR toxin. J Agric Food Chem 50:6569–6574

    Article  PubMed  CAS  Google Scholar 

  • Jelen H, Latus-Zietkiewicz D, Wasowicz E, Kaminski E (1997) Trichodiene as a volatile marker for trichothecenes biosynthesis. J Microbiol Methods 31:45–49

    Article  Google Scholar 

  • Jelén HH, Mirocha CJ, Wasowicz E, Kamiński E (1995) Production of volatile sesquiterpenes by Fusarium sambucinum strains with different abilities to synthesize trichothecenes. Appl Environ Microbiol 61:3815–3820

    PubMed  Google Scholar 

  • Karlshøj K, Nielsen PV, Larsen TO (2007) Differentiation of closely related fungi by electronic nose analysis. J Food Sci 72:M187–M192

    Article  PubMed  CAS  Google Scholar 

  • Koster B, Wong B, Straus N, Malloch D (2009) A multi-gene phylogeny for Stachybotrys evidences lack of trichodiene synthase (tri5) gene for isolates of one of three intrageneric lineages. Mycol Res 113:877–886

    Article  PubMed  CAS  Google Scholar 

  • Kühne B, Hanssen H-P, Abraham W-R, Wray V (1991) A phytotoxic eremophilane ether from Hypomyces odoratus (Ascomycotina). Phytochemistry 30:1463–1466

    Article  Google Scholar 

  • Kunert G, Otto S, Röse USR, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8:596–603

    Article  Google Scholar 

  • Lago JH, Soares MG, Batista-Pereira LG, Silva MF, Corrêa AG, Fernandes JB, Vieira PC, Roque NF (2006) Volatile oil from Guarea macrophylla ssp. tuberculata: seasonal variation and electroantennographic detection by Hypsipyla grandella. Phytochemistry 67:589–594

    Article  PubMed  CAS  Google Scholar 

  • Langford ML, Atkin AL, Nickerson KW (2009) Cellular interactions of farnesol, a quorum-sensing molecule produced by Candida albicans. Future Microbiol 4:1353–1362

    Article  PubMed  CAS  Google Scholar 

  • Larsen TO (1998) Volatile flavour production by Penicillium caseifulvum. Int Dairy J 8:883–887

    Article  CAS  Google Scholar 

  • Lin H, Ji-Kai L (2002) The first humulene type sesquiterpene from Lactarius hirtipes. Z Naturforsch 57c:571–574

    Google Scholar 

  • Lindequist U, Niedermeyer THJ, Jülich W-D (2005) The pharmacological potential of mushrooms. Evid Based Complement Alternat Med 2:285–299

    Article  PubMed  Google Scholar 

  • Liu J-K (2007) Secondary metabolites from higher fungi in China and their biological activity. Drug Disc Ther 1:94–103

    CAS  Google Scholar 

  • Liu X, Pawliszyn R, Wang L, Pawliszyn J (2004) On-site monitoring of biogenic emissions from Eucalyptus dunnii leaves using membrane extraction with sorbent interface combined with a portable gas chromatograph system. The Analyst 129:55–62

    Article  PubMed  CAS  Google Scholar 

  • Lorek J, Pöggeler S, Weide MR, Breves R, Bockmühl DP (2008) Influence of farnesol on the morphogenesis of Aspergillus niger. J Basic Microbiol 48:99–103

    Article  PubMed  Google Scholar 

  • Lundgren L, Bergström G (1975) Wing scents and scent-released phases in the courtship behavior of Lycaeides argyrognomon (Lepidoptera: Lycaenidae). J Chem Ecol 1:399–412

    Article  CAS  Google Scholar 

  • Malherbe S, Watts V, Nieuwoudt HH, Bauer FF, du Toit M (2009) Analysis of volatile profiles of fermenting grape must by headspace solid-phase dynamic extraction coupled with gas chromatography-mass spectrometry (HS-SPDE GC-MS): novel application to investigate problem fermentations. J Agric Food Chem 57:5161–5166

    Article  PubMed  CAS  Google Scholar 

  • Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515

    Article  PubMed  CAS  Google Scholar 

  • Martins M, Henriques M, Azeredo J, Rocha SM, Coimbra MA, Oliveira R (2007) Morphogenesis control in Candida albicans and Candida dubliniensis through signaling molecules produced by planktonic and biofilm cells. Eukaryot Cell 6:2429–2436

    Article  PubMed  CAS  Google Scholar 

  • Matysik S, Herbarth O, Mueller A (2008) Determination of volatile metabolites originating from mould growth on wall paper and synthetic media. J Microbiol Meth 75:182–187

    Article  CAS  Google Scholar 

  • McAlester G, O’Gara F, Morrissey JP (2008) Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. J Med Microbiol 57:563–569

    Article  PubMed  CAS  Google Scholar 

  • Mehta G, Karra SR (1991) Polyquinanes from (R)-(+)-limonene. enantioselective total synthesis of the novel tricyclic sesquiterpene (−)-ceratopicanol. J Chem Soc Chem Commun 1367–1368

  • Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 11:844–854

    Article  PubMed  CAS  Google Scholar 

  • Minerdi D, Bossi S, Maffei ME, Gullino ML, Garibaldi A (2011) Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol Ecol 76:342–351. doi:10.1111/j.1574-6941.2011.01051.x. (Epub ahead of print)

  • Morales DK, Hogan DA (2010) Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog 6:e1000886

    Article  PubMed  CAS  Google Scholar 

  • Mueller GM, Schmit JP (2007) Fungal biodiversity: what do we know? What can we predict? Biodivers Conserv 16:1–5

    Article  Google Scholar 

  • Nair MSR, Anchel M (1973) Metabolic products of Clitocybe illudens. X. (+)-Torreyol. Lloydia 36:106

    CAS  Google Scholar 

  • Nielsen GD, Larsen ST, Olsen O, Løvik M, Poulsen LK, Glue C, Wolkoff P (2007) Do indoor chemicals promote development of airway allergy? Indoor Air 17:236–255

    Article  PubMed  CAS  Google Scholar 

  • Nishino C, Washio H, Tsuzuki K, Bowers WS, Tobin TR (1977) Electroantennogram responses to a stimulant, T-cadinol, in the American cockroach. Agric Biol Chem 41:405–406

    Article  CAS  Google Scholar 

  • Nozoe S, Machida Y (1972) The structures of trichodiol and trichodiene. Tetrahedron 28:5105–5111

    Article  CAS  Google Scholar 

  • Nozoe S, Kobayashi H, Morisaki N (1976a) Isolation of β-trans-bergamotene from Aspergillus fumigatus a fumagillin producing fungi. Tetrahedron Lett 17:4625–4626

    Article  Google Scholar 

  • Nozoe S, Furukawa J, Sankawa U, Shibata S (1976b) Isolation, structure and synthesis of hirsutene, a precursor hydrocarbon of coriolin biosynthesis. Tetrahedron Lett 17:195–198

    Article  Google Scholar 

  • Nozoe S, Kobayashi H, Urano S, Furukawa J (1977) Isolation of Δ6-protoilludene and the related alcohols. Tetrahedron Lett 18:1381–1384

    Article  Google Scholar 

  • Pasanen AL, Lappalainen S, Pasanen P (1996) Volatile organic metabolites associated with some toxic fungi and their mycotoxins. Analyst 121:1949–1953

    Article  CAS  Google Scholar 

  • Pestka JJ, Yike I, Dearborn DG, Ward MD, Harkema JR (2008) Stachybotrys chartarum, trichothecene mycotoxins, and damp building-related illness: new insights into a public health enigma. Toxicol Sci 104:4–26

    Article  PubMed  CAS  Google Scholar 

  • Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811

    Article  PubMed  CAS  Google Scholar 

  • Polizzi V, Fazzini L, Adams A, Picco AM, De Saeger S, Van Peteghem C, De Kimpe N (2011) Autoregulatory properties of (+)-thujopsene and influence of environmental conditions on its production by Penicillium decumbens. Microb Ecol. doi:10.1007/s00248-011-9905-9

  • Qina X-D, Donga Z-J, Liu J-K (2006) Two new compounds from the ascomycete Daldinia concentrica. Helv Chim Acta 89:450–455

    Article  Google Scholar 

  • Ramage G, Saville SP, Wickes BL, López-Ribot JL (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68:5459–5463

    Article  PubMed  CAS  Google Scholar 

  • Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  PubMed  CAS  Google Scholar 

  • Rasser F, Anke T, Sterner O (2000) Secondary metabolites from a Gloeophyllum species. Phytochemistry 54:511–516

    Article  PubMed  CAS  Google Scholar 

  • Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9:847–859

    Article  PubMed  CAS  Google Scholar 

  • Risticevic S, Niri VH, Vuckovic D, Pawliszyn J (2009) Recent developments in solid-phase microextraction. Anal Bioanal Chem 393:781–795

    Article  PubMed  CAS  Google Scholar 

  • Rohlfs M, Churchill AC (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48:23–34

    Article  PubMed  CAS  Google Scholar 

  • Rösecke J, Pietsch M, König WA (2000) Volatile constituents of wood-rotting basidiomycetes. Phytochemistry 54:747–750

    Article  PubMed  Google Scholar 

  • Scher JM, Speakman JB, Zapp J, Becker H (2004) Bioactivity guided isolation of antifungal compounds from the liverwort Bazzania trilobata (L.) S.F. Gray. Phytochemistry 65:2583–2588

    Article  PubMed  CAS  Google Scholar 

  • Schnürer J, Olsson J, Börjesson T (1999) Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet Biol 27:209–217

    Article  PubMed  Google Scholar 

  • Semighini CP, Hornby JM, Dumitru R, Nickerson KW, Harris SD (2006) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59:753–764

    Article  PubMed  CAS  Google Scholar 

  • Semighini CP, Murray N, Harris S (2008) Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol Lett 279:259–264

    Article  PubMed  CAS  Google Scholar 

  • Smedsgaard J, Nielsen J (2005) Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. J Exp Bot 56:273–286

    Article  PubMed  CAS  Google Scholar 

  • Sprecher E (1963) Über ätherisches Öl aus Pilzen. Planta Med 11:119–127

    Article  CAS  Google Scholar 

  • Sprecher E, Kubeczka K-H, Ratschko M (1975) Flüchtige Terpene in Pilzen. Arch Pharm 308:843–851

    Article  CAS  Google Scholar 

  • Steele CL, Crock J, Bohlmann J, Croteau R (1998) Sesquiterpene synthases from grand fir (Abies grandis). J Biol Chem 273:2078–2089

    Article  PubMed  CAS  Google Scholar 

  • Sterner O, Bergman R, Kihlberg J, Wickberg B (1985) The sesquiterpenes of Lactarius vellereus and their role in a proposed chemical defense system. J Nat Prod 48:279–288

    Article  CAS  Google Scholar 

  • Sterner O, Bergendorff O, Bocchio F (1989) The isolation of a guaiane sesquiterpene from fruit bodies of Lactarius sanguifluus. Phytochemistry 28:2501–2502

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R (2010) Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81:187–193

    Article  PubMed  CAS  Google Scholar 

  • Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950

    PubMed  CAS  Google Scholar 

  • Sunesson A-L, Vaes WHJ, Nilsson C-A, Blomquist G, Andersson B, Carlson R (1995) Identification of volatile metabolites from five fungal species cultivated on two media. Appl Environ Microbiol 61:2911–2918

    PubMed  CAS  Google Scholar 

  • Tkachev AV (1987) The chemistry of caryophyllene and related compounds. Chem Nat Comp 23:393–412

    Article  Google Scholar 

  • Townsend BJ, Poole A, Blake CJ, Llewellyn DJ (2005) Antisense suppression of a (1)-d-cadinene synthase gene in cotton prevents the induction of this defense response gene during bacterial blight infection but not its constitutive expression. Plant Physiol 138:516–528

    Article  PubMed  CAS  Google Scholar 

  • Tursch B, Braekman JC, Daloze D, Fritz P, Kelecon A, Karlsson R, Losman D (1974) Chemical studies of marine invertebrates. VIII. Africanol, an unusual sesquiterpene from Lemalia africana (Coelenterata, Octocorallia, Alcyonacea). Tetrahedron Lett 9:747–750

  • Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485

    Article  PubMed  CAS  Google Scholar 

  • Urbasch I, Kühne B, Hanssen H-P, Abraham W-R (1991) Fungicidal activity of hypodoratoxide from Hypomyces odoratus (Ascomycotina). Planta Medica 57:(Suppl 2):A18

  • Van Eijk GW, Roeijmans HJ, Verwiel PEJ (1984) Isolation and identification of the sesquiterpenoid (+)-torreyol from Xylobolus frustulatus. Exp Mycol 8:273–275

    Article  Google Scholar 

  • Van Lancker F, Adams A, Delmulle B, De Saeger S, Moretti A, Van Peteghem C, De Kimpe N (2008) Use of headspace SPME-GC-MS for the analysis of the volatiles produced by indoor molds grown on different substrates. J Environ Monit 10:1127–1133

    Article  PubMed  CAS  Google Scholar 

  • Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JP (2002) Extensive fungal diversity in plant roots. Science 295:2051

    Article  PubMed  Google Scholar 

  • Wang L, Lord H, Morehead R, Dorman F, Pawliszyn J (2002) Sampling and monitoring of biogenic emissions by Eucalyptus leaves using membrane extraction with sorbent interface (MESI). J Agric Food Chem 50:6281–6286

    Google Scholar 

  • Wasser SP (2011) Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Appl Microbiol Biotechnol 89:1323–1332

    Article  PubMed  CAS  Google Scholar 

  • Westwater C, Balish E, Schofield DA (2005) Candida albicans-conditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot Cell 4:1654–1661

    Article  PubMed  CAS  Google Scholar 

  • Wilkins K (2000) Volatile sesquiterpenes from Stachybotrys chartarum. Environ Sci Pollut Res 7:77–78

    Article  CAS  Google Scholar 

  • Wilkins K, Larsen K, Simkus M (2000) Volatile metabolites from mold growth on building materials and synthetic media. Chemosphere 41:437–446

    Article  PubMed  CAS  Google Scholar 

  • Wilkins K, Nielsen KF, Din SU (2003) Patterns of volatile metabolites and nonvolatile trichothecenes produced by isolates of Stachybotrys, Fusarium, Trichoderma, Trichothecium and Memnoniella. Environ Sci Pollut Res 10:162–166

    Article  CAS  Google Scholar 

  • Winter REK, Dorn F, Arigoni D (1990) The structure of helminthogermacrene. J Org Chem 45:4786–4789

    Article  Google Scholar 

  • Wu SM, Krings U, Zorn H, Berger RG (2005) Volatile compounds from the fruiting bodies of beefsteak fungus Fistulina hepatica (Schaeffer: Fr.) Fr. Food Chem 92:221–226

    Article  CAS  Google Scholar 

  • Wu S, Zorn H, Krings U, Berger RG (2007) Volatiles from submerged and surface-cultured beefsteak fungus, Fistulina hepatica. Flavour Fragr J 22:53–60

    Article  CAS  Google Scholar 

  • Xu D, Sheng Y, Zhou Z-Y, Liu R, Leng Y, Liu J-K (2009) Sesquiterpenes from cultures of the Basidiomycete Clitocybe conglobata and their 11β-hydroxysteroid dehydrogenase inhibitory activity. Chem Pharm Bull 57:433–435

    Article  PubMed  CAS  Google Scholar 

  • Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55:491–503

    Article  PubMed  CAS  Google Scholar 

  • Zeringue HJ, Bhatnagar D, Cleveland TE (1993) C(15)H(24) Volatile compounds unique to aflatoxigenic strains of Aspergillus flavus. Appl Environ Microbiol 59:2264–2270

    PubMed  CAS  Google Scholar 

  • Zheng W, Miao K, Liu Y, Zhao Y, Zhang M, Pan S, Dai Y (2010) Chemical diversity of biologically active metabolites in the sclerotia of Inonotus obliquus and submerged culture strategies for up-regulating their production. Appl Microbiol Biotechnol 87:123712–123754

    Google Scholar 

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  1. Helmholtz Center for Infection Research, Chemical Microbiology, Inhoffenstrasse 7, 38124, Braunschweig, Germany

    Rolf Kramer & Wolf-Rainer Abraham

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Kramer, R., Abraham, WR. Volatile sesquiterpenes from fungi: what are they good for?. Phytochem Rev 11, 15–37 (2012). https://doi.org/10.1007/s11101-011-9216-2

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