Genomic profiling of carbohydrate metabolism in the ectomycorrhizal fungus Tuber melanosporum

New Phytologist

Volumn 189, Issue 3, 2011, Pages 751-764

  Ceccaroli, P ^a   Buffalini, M ^a   Saltarelli, R ^a   Barbieri, E ^a   Polidori, E ^a   Ottonello, S ^b   Kohler, A ^c   Tisserant, E ^c   Martin, F ^c   Stocchi, V ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

^c UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Carbohydrate metabolism; Ectomycorrhizal fungi; Genome wide repertoire; Invertase; Mannitol; Trehalose; Tuber melanosporum

Indexed keywords

BETA FRUCTOFURANOSIDASE; CITRIC ACID;

ALCOHOL; CARBOHYDRATE; CARBON; CARBOXYLIC ACID; ECTOMYCORRHIZA; ENZYME ACTIVITY; FRUITING; GENOME; IDENTIFICATION METHOD; METABOLISM; NITROGEN; PHOSPHATE; POLYMERASE CHAIN REACTION; PROTEIN;

ARTICLE; ASCOMYCETES; CARBOHYDRATE METABOLISM; ENZYMOLOGY; FRUITING BODY; FUNGAL GENE; FUNGAL GENOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MYCELIUM; MYCORRHIZA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ASCOMYCOTA; BETA-FRUCTOFURANOSIDASE; CARBOHYDRATE METABOLISM; CITRATES; FRUITING BODIES, FUNGAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENOME, FUNGAL; MYCELIUM; MYCORRHIZAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

ASCOMYCOTA; FUNGI; MYCELIUM (GENUS); TUBER (TRUFFLE); TUBER MELANOSPORUM;

EID: 78651283138     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03520.x     Document Type: Article

References (62)

1. Abbà S, Balestrini R, Benedetto A, Rottensteiner H, De Lucas JR, Bonfante P. 2007. The role of the glyoxylate cycle in the symbiotic fungus Tuber borchii: expression analysis and subcellular localization. Current Genetics 52: 159-170.
2. Agostini D, Polidori E, Palma F, Ceccaroli P, Saltarelli R, Tonelli D, Stocchi V. 2001. Cloning, expression, and characterization of the hxk-1 gene from the white truffle Tuber borchii Vittad.: a first step toward understanding sugar metabolism. Fungal Genetics and Biology 33: 15-23.
3. Bernardo SMH, Gray K-A, Todd RB, Cheetham BF, Katz ME. 2007. Characterization of regulatory non-catalytic hexokinases in Aspergillus nidulans. Molecular Genetics and Genomics 277: 519-532.
4. nd edn Berlin-Heidelberg, Germany: Springer Verlag, 291-332.
5. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N et al. 2004. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiology and Molecular Biology Reviews 68: 1-108.
6. Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
7. Brock M, Fischer R, Linder D, Buckel W. 2000. Methylcitrate synthase from Aspergillus nidulans: implications for propionate as an antifungal agent. Molecular Microbiology 35: 961-973.
8. Buckel W. 1999. Anaerobic energy metabolism. In: Lengeler JW, Drews G, Schlegel HG, eds. Biology of the Procaryotes. Oxford, UK: Blackwell Science, 278-326.
9. Ceccaroli P, Saltarelli R, Buffalini M, Piccoli G, Stocchi V. 1999. Three different forms of hexokinase are identified during Tuber borchii mycelium growth. Molecular and Cellular Biochemistry 194: 71-77.
10. 13C NMR study. Fungal Genetics and Biology 39: 168-175.
11. Ceccaroli P, Saltarelli R, Cesari P, Zambonelli A, Stocchi V. 2001. Effects of different carbohydrate sources on the growth of Tuber borchii Vittad. mycelium strains in pure culture. Molecular and Cellular Biochemistry 218: 65-70.
12. Ceccaroli P, Saltarelli R, Guescini M, Polidori E, Buffalini M, Menotta M, Pierleoni R, Barbieri E, Stocchi V. 2007. Identification and characterization of the Tuber borchii D-mannitol dehydrogenase which defines a new subfamily within the polyol-specific medium chain dehydrogenases. Fungal Genetics and Biology 44: 965-978.
13. Deveau A, Kohler A, Frey-Klett P, Martin F. 2008. The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N. New Phytologist 180: 379-390.
14. Dulermo T, Rascle C, Billon-Grand G, Gout E, Bligny R, Cotton P. 2010. Novel insights into mannitol metabolism in the fungal plant pathogen Botrytis cinerea. Biochemical Journal 427: 323-332.
15. Dulermo T, Rascle C, Chinnici G, Gout E, Bligny R, Cotton P. 2009. Dynamic carbon transfer during pathogenesis of sunflower by the necrotrophic fungus Botrytis cinerea: from plant hexoses to mannitol. New Phytologist 183: 1149-1162.
16. Eis C, Albert M, Dax K, Nidetzky B. 1998. The stereochemical course of the reaction mechanism of trehalose phosphorylase from Schizophyllum commune. FEBS Letters 440: 440-443.
17. Felsenstein J. 2004. PHYLIP (Phylogeny Interference Package) Version 3.63. Department of Genome Sciences, the University of Washington, Seattle.
18. Flores CL, Rodriguez C, Petit T, Gancedo C. 2000. Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiology Review 24: 507-529.
19. Guescini M, Pierleoni R, Palma F, Zeppa S, Vallorani L, Potenza L, Sacconi C, Giomaro G, Stocchi V. 2003. Characterization of the Tuber borchii nitrate reductase gene and its role in ectomycorrhizae. Molecular Genetics and Genomics 269: 807-816.
20. Guidi C, Zeppa S, Annibalini G, Pierleoni R, Guescini M, Buffalini M, Zambonelli A, Stocchi V. 2006. The isoprenoid pathway in the ectomycorrhizal fungus Tuber borchii Vittad.: cloning and characterisation of the tbhmgr, tbfpps and tbsqs genes. Current Genetics 50: 393-404.
21. Han SE, Kwon HB, Lee SB, Yi BY, Murayama I, Kitamoto Y, Byun MO. 2003. Cloning and characterization of a gene encoding trehalose phosphorylase TP from Pleurotus sajor-caju. Protein Expression and Purification 30: 194-202.
22. Hult K, Gatenbeck S. 1978. Production of NADPH in the mannitol cycle and its relation to polyketide formation in Alternaria alternata. European Journal of Biochemistry 88: 607-612.
23. Iotti M, Barbieri E, Stocchi V, Zambonelli A. 2005. Morphological and molecular characterisation of mycelia of ectomycorrhizal fungi in pure culture. Fungal Diversity 19: 51-68.
24. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23: 403-405.
25. Jiang H, Ouyang H, Zhou H, Jin C. 2008. GDP-mannose pyrophosphorylase is essential for cell wall integrity, morphogenesis and viability of Aspergillus fumigatus. Microbiology 154: 2730-2739.
26. Jordy MN, Azémar-Lorentz S, Brun A, Botton B, Pargney JC. 1998. Cytolocalization of glycogen, starch, and other insoluble polysaccharides during ontogeny of Paxillus involutus-Betula pendula ectomycorrhizas. New Phytologist 140: 331-341.
27. Jorge JA, Polizeli ML, Thevelein JM, Terenzi HF. 1997. Trehalases and trehalose hydrolysis in fungi. FEMS Microbiology Letters 154: 165-171.
28. Jules M, Guillou V, François J, Parrou J-L. 2004. Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Applied and Environmental Microbiology 70: 2771-2778.
29. Kleinschmidt R, Hentschke I, Rothe GM. 1998. Effect of season and soil treatments on carbohydrate concentrations in Norway spruce (Picea abies) mycorrhizae. Tree Physiology 18: 325-332.
30. Lacourt I, Duplessis S, Abbà S, Bonfante P, Martin F. 2002. Isolation and characterization of differentially expressed genes in the mycelium and fruit body of Tuber borchii. Applied and Environmental Microbiology 68: 4574-4582.
31. Lee SH, Han YK, Yun SH, Lee YW. 2009. Roles of the glyoxylate and methylcitrate cycles in sexual development and virulence in the cereal pathogen Gibberella zeae. Eukaryotic Cell 8: 1155-1164.
32. Liu QN, Liu RS, Wang YH, Mi ZY, Li DS, Zhong JJ, Tang YJ. 2009. Fed-batch fermentation of Tuber melanosporum for the hyperproduction of mycelia and bioactive Tuber polysaccharides. Bioresource Technology 100: 3644-3649.
33. López MF, Männer P, Hampp R, Nehls U. 2007. Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytologist 174: 389-398.
34. Lussier M, Sdicu AM, Bussereau F, Jacquet M, Bussey H. 1997. The Ktr1p, Ktr3p, and Kre2p/Mnt1p mannosyltransferases participate in the elaboration of yeast O- and N-linked carbohydrate chains. The Journal of Biological Chemistry 272: 15527-15531.
35. Mamoun M, Olivier JM. 1991. Influence du substrat carboné et de la forme d'azote minéral sur la croissance de Tuber melanosporum (Vitt.) en culture pure. Application à la production de biomasse mycélienne. Physiologie Végétale 11: 521-527.
36. Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92.
37. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
38. Munro CA, Bates S, Buurman ET, Hughes B, MacCallum DM, Bertram G, Atrih A, Ferguson MAJ, Bain JM, Brand A et al. 2005. Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1, 2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. Journal of Biological Chemistry 280: 1051-1060.
39. Nehls U. 2008. Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. Journal of Experimental Botany 59: 1097-1108.
40. Nehls U, Göhringer F, Wittulsky S, Dietz S. 2010. Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biology 12: 292-301.
41. Nehls U, Grunze N, Willmann M, Reich M, Küster H. 2007. Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68: 82-91.
42. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman Ma, Abe K, Archer DB, Bermejo C et al. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151-1156.
43. Parrent JL, James TY, Vasaitis R, Taylor AFS. 2009. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses BMC Evolutionary Biology 9: 148.
44. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: 2002-2007.
45. Polidori E, Ceccaroli P, Saltarelli R, Guescini M, Menotta M, Agostini D, Palma F, Stocchi V. 2007. Hexose uptake in the plant symbiotic ascomycete Tuber borchii Vittadini: biochemical features and expression pattern of the transporter TBHXT1. Fungal Genetics and Biology 44: 187-198.
46. Roos AK, Andersson CE, Bergfors T, Jacobsson M, Karlen A, Unge T, Jones TA, Mowbray SL. 2004. Mycobacterium tuberculosis ribose-5-phosphate isomerase has a known fold, but a novel active site. Journal of Molecular Biology 335: 799-809.
47. Saavedra E, Ramos-Casillas LE, Marin-Hernandez A, Moreno-Sanchez R, Guerra-Sanchez G. 2008. Glycolysis in Ustilago maydis. FEMS Yeast Research 8: 1313-1323.
48. Saltarelli R, Ceccaroli P, Vallorani L, Zambonelli A, Citterio B, Malatesta M, Stocchi V. 1998. Biochemical and morphological modifications during the growth of Tuber borchii mycelium. Mycological Research 102: 403-409.
49. Salzer P, Hager A. 1991. Sucrose utilization of the ectomycorrhizal fungi Amanita muscaria and Hebeloma crustuliniforme depends on the cell wall-bound invertase activity of their host Picea abies. Botanica Acta 104: 439-445.
50. Schaarschmidt S, Roitsch T, Hause B. 2006. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. Journal of Experimental Botany 57: 4015-4023.
51. Schaeffer C, Wallenda T, Guttenberger M, Hampp R. 1995. Acid invertase in mycorrhizal and non-mycorrhizal roots of Norway spruce (Picea abies [L.] Karst.) seedlings. New Phytologist 129: 417-424.
52. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK: Academic Press.
53. Solomon PS, Lee RC, Wilson TJG, Oliver RP. 2004. Pathogenicity of Stagonospora nodorum requires malate synthase. Molecular Microbiology 53: 1065-1073.
54. Solomon PS, Waters ODC, Jörgens CI, Lowe RGT, Rechberger J, Trengove RD, Olivier RP. 2006. Mannitol is required for asexual sporulation in the wheat pathogen Staganospora nodorum (glume blotch). Biochemical Journal 399: 231-239.
55. Solomon PS, Waters ODC, Oliver RP. 2007. Decoding the mannitol enigma in filamentous fungi. Trends in Microbiology 15: 257-262.
56. Suz LM, Martin MP, Colinas C. 2006. Detection of Tuber melanosporum DNA in soil. FEMS Microbiology Letters 254: 251-257.
57. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
58. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Research 25: 4876-4882.
59. Vélëz H, Glassbrook NJ, Daub ME. 2007. Mannitol metabolism in the phytopathogenic fungus Alternaria alternata. Fungal Genetics and Biology 44: 258-268.
60. Wilson RA, Jenkinson JM, Gibson RP, Littlechild JA, Wang Z-Y, Talbot NJ. 2007. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO Journal 26: 3673-3685.
61. Zampieri E, Murat C, Cagnasso M, Bonfante P, Mello A. 2010. Soil analysis reveals the presence of an extended mycelial network in a Tuber magnatum truffle-ground. FEMS Microbiology Ecology 71: 43-49.
62. Zhang RG, Andersson CE, Skarina T, Evdokimova E, Edwards AM, Joachimiak A, Savchenko A, Mowbray SL. 2003. The 2.2 Å resolution structure of RpiB/AlsB from Escherichia coli illustrates a new approach to the ribose-5-phosphate isomerase reaction. Journal of Molecular Biology 332: 1083-1094.