Intraspecific genotypic variability determines concentrations of key truffle volatiles

New Phytologist

Volumn 194, Issue 3, 2012, Pages 823-835

  Splivallo, Richard ^a   Valdez, Nayuf ^a   Kirchhoff, Nina ^a   Ona, Marta Castiella ^a   Schmidt, Jean Pierre ^b   Feussner, Ivo ^c   Karlovsky, Petr ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Georg August University ^*  (Switzerland)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

1 octen 3 ol; Amplified fragment length polymorphism (AFLP); Aroma variability; Truffle genetics; Tuber borchii; Tuber spp.; Tuber uncinatum; Volatile organic compounds (VOCs)

Indexed keywords

1 OCTEN 3 OL; 1-OCTEN-3-OL; FUNGAL DNA; OCTANOL; VOLATILE ORGANIC COMPOUND;

CONCENTRATION (COMPOSITION); DNA FINGERPRINTING; ENVIRONMENTAL FACTOR; FRUITING; GENOTYPE; GEOGRAPHICAL DISTRIBUTION; HOLISTIC APPROACH; INTRASPECIFIC VARIATION; MATURATION; MUSHROOM; VOLATILE ELEMENT; VOLATILE ORGANIC COMPOUND;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; ASCOMYCETES; CHEMISTRY; EUROPE; FRUITING BODY; GENETIC VARIABILITY; GENETICS; GENOTYPE; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCELIUM; SPECIES DIFFERENCE;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ASCOMYCOTA; DNA, FUNGAL; EUROPE; FRUITING BODIES, FUNGAL; GENETIC VARIATION; GENOTYPE; GEOGRAPHY; MYCELIUM; OCTANOLS; SPECIES SPECIFICITY; VOLATILE ORGANIC COMPOUNDS;

BACTERIA (MICROORGANISMS); TUBER (TRUFFLE); TUBER BORCHII; TUBER MAGNATUM; TUBER UNCINATUM;

EID: 84859577917     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04077.x     Document Type: Article

References (61)

1. Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ. 2004. Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. The Plant Cell 16: 3110-3131.
2. Barbieri E, Bertini L, Rossi I, Ceccaroli P, Saltarelli R, Guidi C, Zambonelli A, Stocchi V. 2005. New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiology Letters 247: 23-35.
3. Barbieri E, Guidi C, Bertaux J, Frey-Klett P, Garbaye J, Ceccaroli P, Saltarelli R, Zambonelli A, Stocchi V. 2007. Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environmental Microbiology 9: 2234-2246.
4. Barbieri E, Potenza L, Rossi I, Sisti D, Giomaro G, Rossetti S, Beimfohr C, Stocchi V. 2000. Phylogenetic characterization and in situ detection of a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii Vittad. ectomycorrhizal mycelium. Applied and Environmental Microbiology 66: 5035-5042.
5. Barbieri E, Riccioni G, Pisano A, Sisti D, Zeppa S, Agostini D, Stocchi V. 2002. Competitive PCR for quantitation of a Cytophaga-Flexibacter-Bacteroides phylum bacterium associated with the Tuber borchii Vittad. mycelium. Applied and Environmental Microbiology 68: 6421-6424.
6. Bensch S, Akesson M. 2005. Ten years of AFLP in ecology and evolution: why so few animals? Molecular Ecology 14: 2899-2914.
7. Bertault G, Raymond M, Berthomieu A, Callot G, Fernandez D. 1998. Trifling variation in truffles. Nature 394: 734.
8. Bonuso E, Zambonelli A, Bergemann SE, Iotti M, Garbelotto M. 2009. Multilocus phylogenetic and coalescent analyses identify two cryptic species in the Italian bianchetto truffle, Tuber borchii Vittad. Conservation Genetics 11: 1453-1466.
9. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ. 2011. Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genetics 7: e1001287.
10. Brodhun F, Göbel C, Hornung E, Feussner I. 2009. Identification of PpoA from Aspergillus nidulans as a fusion protein of a fatty acid heme dioxygenase/peroxidase and a cytochrome P450. The Journal of Biological Chemistry 284: 11792-11805.
11. Buzzini P, Gasparetti C, Turchetti B, Cramarossa MR, Vaughan-Martini A, Martini A, Pagnoni UM, Forti L. 2005. Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles. Archives of Microbiology 184: 187-193.
12. Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J. 2004. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Applied and Environmental Microbiology 70: 2823-2829.
13. Cho IH, Namgung H-J, Choi H-K, Kim Y-S. 2008. Volatiles and key odorants in the pileus and stipe of pine-mushroom (Tricholoma matsutake Sing.). Food Chemistry 106: 71-76.
14. Combet E, Henderson J, Eastwood DC, Burton KS. 2006. Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47: 317-326.
15. Costello A, Osborne J. 2005. Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. Practical Assessment, Research & Evaluation 10: 173-178.
16. Culleré L, Ferreira V, Chevret B, Venturini ME, Sánchez-Gimeno AC, Blanco D. 2010. Characterisation of aroma active compounds in black truffles (Tuber melanosporum) and summer truffles (Tuber aestivum) by gas chromatography-olfactometry. Food Chemistry 122: 300-306.
17. Diaz P, Ibanez E, Senorans FJ, Reglero G. 2003. Truffle aroma characterization by headspace solid-phase microextraction. Journal of Chromatography A 1017: 207-214.
18. Douhan GW, Vincenot L, Gryta H, Selosse M-A. 2011. Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biology 115: 569-597.
19. Garscha U, Oliw EH. 2009. Leucine/valine residues direct oxygenation of linoleic acid by (10R)- and (8R)-dioxygenases. Expression and site-directed mutagenesis of (10R)- dioxygenase with epoxyalcohol synthase activity. Journal of Biological Chemistry. 284: 13755-13765. M808665200.
20. Gioacchini AM, Menotta M, Bertini L, Rossi I, Zeppa S, Zambonelli A, Piccoli G, Stocchi V. 2005. Solid-phase microextraction gas chromatography/mass spectrometry: a new method for species identification of truffles. Rapid Communications in Mass Spectrometry 19: 2365-2370.
21. Gioacchini AM, Menotta M, Guescini M, Saltarelli R, Ceccaroli P, Amicucci A, Barbieri E, Giomaro G, Stocchi V. 2008. Geographical traceability of Italian white truffle (Tuber magnatum Pico) by the analysis of volatile organic compounds. Rapid Communications in Mass Spectrometry 22: 3147-3153.
22. Hochberg ME, Bertault G, Poitrineau K, Janssen A. 2003. Olfactory orientation of the truffle beetle, Leiodes cinnamomea. Entomologia Experimentalis et Applicata 109: 147-153.
23. Hollander M, Wolfe DA. 1973. Nonparametric statistical methods. New York, NY, USA: John Wiley & Sons.
24. Karban R, Baldwin IT. 1997. Induced responses to herbivory. Chicago, IL, USA: University of Chicago Press.
25. Kües U, Martin F. 2011. On the road to understanding truffles in the underground. Fungal Genetics and Biology 48: 555-560.
26. Leitner M, Boland W, Mithöfer A. 2005. Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytologist 167: 597-606.
27. March RE, Richards DS, Ryan RW. 2006. Volatile compounds from six species of truffle-head-space analysis and vapor analysis at high mass resolution. International Journal of Mass Spectrometry 249: 60-67.
28. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
29. Maser C, Claridge AW, Trappe JM. 2008. Trees, truffles, and beasts: how forests function. New Jersey, USA: Rutgers University Press.
30. Mauriello G, Marino R, DAuria M, Cerone G, Rana GL. 2004. Determination of volatile organic compounds from truffles via SPME-GC-MS. Journal of Chromatographic Science 42: 299-305.
31. Mello A, Cantisani A, Vizzini A, Bonfante P. 2002. Genetic variability of Tuber uncinatum and its relatedness to other black truffles. Environmental Microbiology 4: 584-594.
32. Mello A, Miozzi L, Vizzini A, Napoli C, Kowalchuk G, Bonfante P. 2010. Bacterial and fungal communities associated with Tuber magnatum-productive niches. Plant Biosystems 144: 323-332.
33. Mello A, Murat C, Vizzini A, Gavazza V, Bonfante P. 2005. Tuber magnatum Pico, a species of limited geographical distribution: its genetic diversity inside and outside a truffle ground. Environmental Microbiology 7: 55-65.
34. Mendes-Ferreira A, Barbosa C, Jimenez-Marti E, Del Olmo ML, Mendes-Faia A. 2010. The wine yeast strain-dependent expression of genes implicated in sulfide production in response to nitrogen availability. Journal of Microbiology and Biotechnology 20: 1314-1321.
35. Molina AM, Swiegers JH, Varela C, Pretorius IS, Agosin E. 2007. Influence of wine fermentation temperature on the synthesis of yeast-derived volatile aroma compounds. Applied Microbiology and Biotechnology 77: 675-687.
36. Murat C, Díez J, Luis P, Delaruelle C, Dupré C, Chevalier G, Bonfante P, Martin F. 2004. Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytologist 164: 401-411.
37. Murat C, Riccioni C, Belfiori B, Cichocki N, Labbé J, Morin E, Tisserant E, Paolocci F, Rubini A, Martin F. 2011. Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genetics and Biology 48: 592-601.
38. Nei M. 1972. Genetic distance between populations. The American Naturalist 106: 283-292.
39. Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
40. Pacioni G, Leonardi M, Aimola P, Ragnelli AM, Rubini A, Paolocci F. 2007. Isolation and characterization of some mycelia inhabiting Tuber ascomata. Mycological Research 111: 1450-1460.
41. Paolocci F, Rubini A, Riccioni C, Arcioni S. 2006. Reevaluation of the life cycle of Tuber magnatum. Applied and Environmental Microbiology 72: 2390-2393.
42. Paolocci F, Rubini A, Riccioni C, Topini F, Arcioni S. 2004. Tuber aestivum and Tuber uncinatum: two morphotypes or two species? FEMS Microbiology Letters 235: 109-115.
43. Reineke A, Karlovsky P. 2000. Simplified AFLP protocol: replacement of primer labeling by the incorporation of alpha-labeled nucleotides during PCR. BioTechniques 28: 622-623.
44. Risticevic S, Lord H, Gorecki T, Arthur CL, Pawliszyn J. 2010. Protocol for solid-phase microextraction method development. Nature Protocols 5: 122-139.
45. Rubini A, Belfiori B, Riccioni C, Arcioni S, Martin F, Paolocci F. 2011a. Tuber melanosporum: mating type distribution in a natural plantation and dynamics of strains of different mating types on the roots of nursery-inoculated host plants. New Phytologist 189: 723-735.
46. Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci F. 2011b. Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytologist 189: 710-722.
47. Splivallo R, Bossi S, Maffei M, Bonfante P. 2007a. Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction. Phytochemistry 68: 2584-2598.
48. Splivallo R, Novero M, Bertea C, Bossi S, Bonfante P. 2007b. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytologist 175: 417-424.
49. Splivallo R, Ottonello S, Mello A, Karlovsky P. 2011. Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytologist 189: 688-699.
50. 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 Biology and Biochemistry 43: 1411-1416.
51. Steeghs M, Bais HP, de Gouw J, Goldan P, Kuster W, Northway M, Fall R, Vivanco JM. 2004. Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiology 135: 47-58.
52. Stemmer WP. 1991. A 20-minute ethidium bromide/high-salt extraction protocol for plasmid DNA. BioTechniques 10: 726.
53. Talou T, Gaset A, Delmas M, Kulifaj M, Montant C. 1990. Dimethyl sulphide: the secret for black truffle hunting by animals? Mycological Research 94: 277-278.
54. Tang YJ, Wang G, Li YY, Zhong JJ. 2009. Fermentation condition outweighed truffle species in affecting volatile organic compounds analyzed by chromatographic fingerprint system. Analytica Chimica Acta 647: 40-45.
55. Tsitsigiannis DI, Kowieski TM, Zarnowski R, Keller NP. 2005. Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151: 1809-1821.
56. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23: 4407-4414.
57. Wenke K, Kai M, Piechulla B. 2010. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231: 499-506.
58. Wurzenberger M, Grosch W. 1983. Determination of 1-octen-3-ol in mushrooms and in products containing mushrooms. Zeitschrift für Lebensmittel-Untersuchung und -Forschung 176: 16-19.
59. Wurzenberger M, Grosch W. 1984. Stereochemistry of the cleavage of the 10-hydroperoxide isomer of linoleic acid to 1-octen-3-ol by a hydroperoxide lyase from mushrooms (Psalliota bispora). Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 795: 163-165.
60. Zeppa S, Gioacchini AM, Guidi C, Guescini M, Pierleoni R, Zambonelli A, Stocchi V. 2004. Determination of specific volatile organic compounds synthesised during Tuber borchii fruit body development by solid-phase microextraction and gas chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry 18: 199-205.
61. Zhang Z-M, Wu W-W, Li G-K. 2008. A GC-MS study of the volatile organic composition of straw and oyster mushrooms during maturity and its relation to antioxidant activity. Journal of Chromatographic Science 46: 690-696.