The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N

New Phytologist

Volumn 180, Issue 2, 2008, Pages 379-390

  Deveau, A ^a   Kohler, A ^a   Frey Klett, P ^a   Martin, F ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Annotation; Carbon; Ectomycorrhiza; Laccaria bicolor; Mannitol; Transcriptome; Trehalose

Indexed keywords

CARBON;

CARBON; COMPARATIVE STUDY; ECTOMYCORRHIZA; FUNGUS; GENE EXPRESSION; GENOME; METABOLISM; POLYMERASE CHAIN REACTION; SUGAR;

ARTICLE; CARBOHYDRATE METABOLISM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LACCARIA; METABOLISM; MYCORRHIZA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; SYMBIOSIS;

CARBOHYDRATE METABOLISM; CARBON ISOTOPES; GENE EXPRESSION REGULATION, FUNGAL; LACCARIA; MAGNETIC RESONANCE SPECTROSCOPY; MYCORRHIZAE; SYMBIOSIS; TRANSCRIPTION, GENETIC;

BASIDIOMYCOTA; FUNGI; LACCARIA; LACCARIA BICOLOR;

EID: 52649089240     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02581.x     Document Type: Article

References (56)

1. Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G. 2006. Insights on the evolution of trehalose biosynthesis. BMC Evolutionary Biology 6 : 109 124.
2. Bago B, Pfeffer PE, Douds DD, Brouillette J, Bécard G, Shachar-Hill Y. 1999. Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiology 121 : 263 271.
3. Bell W, Sun W, Hohmann S, Wera S, Reinders A, De Virgilio C, Wiemken A, Thevelein J. 1998. Composition and functional analysis of Saccharomyces cerevisiae trehalose synthase complex. Journal of Biological Chemistry 273 : 33311 33319.
4. 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.
5. 13C NMR study. Fungal Genetics and Biology 39 : 168 175.
6. 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 dehydrogenase. Fungal Genetics and Biology 44 : 965 978.
7. Cullen D. 2008. Fungal symbiosis unearthed. Nature 452 : 42 43.
8. DeSmet KAL, Weston A, Brown IN, Young DB, Robertson BD. 2000. Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146 : 199 208.
9. Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P. 2007. The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytologist 175 : 243 255.
10. Di Battista C, Selosse M-A, Bouchard D, Senström E, Le Tacon F. 1996. Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S238. Mycological Research 100 : 1315 1324.
11. Duplessis S, Courty PE, Tagu D, Martin F. 2005. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytologist 165 : 599 611.
12. Eis C, Nidetzky B. 1999. Characterization of trehalose phosphorylase from Schizophyllum commune. Biochemistry Journal 341 : 385 393.
13. Elbein AD, Pan YT, Pastuszak I, Caroll D. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology 13 : 17R 27R.
14. Elzainy TA, Hassan MM, Allam AM. 1973. New pathway for nonphosphorylated degradation of gluconate by Aspergillus niger. Journal of Bacteriology 114 : 457 459.
15. Finlay RD, Söderström B. 1992. Mycorrhiza and carbon flow to the soil. In : Allen M, ed. Mycorrhiza Functioning. London, UK : Chapman & Hall, 134 160.
16. Frey-Klett P, Pierrat JC, Garbaye J. 1997. Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Applied and Environmental Microbiology 63 : 139 144.
17. Hampp R, Schaeffer C. 1995. Mycorrhiza carbohydrate and energy metabolism. In : Varma A, Hock B, eds. Mycorrhiza: structure, function, molecular biology and biotechnology. Berlin, Germany : Springer-Verlag, 267 289.
18. 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.
19. 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 882 : 607 612.
20. Hult K, Veide A, Gatenbeck S. 1980. The distribution of the NAPDH regenerating mannitol cycle among fungal species. Archives of Microbiology 128 : 253 255.
21. Ineichen K, Wiemken V. 1992. Changes in the fungus-specific, soluble-carbohydrate pool during rapid and synchronous ectomycorrhiza formation of Picea abies with Pisolithus tinctorius. Mycorrhiza 2 : 1 7.
22. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23, 403 405.
23. Johansson T, Le Quéré A, Ahren D, Söderström B, Erlandsson R, Lundeberg J, Uhlen M, Tunlid A. 2004. Transcriptional response of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Molecular Plant-Microbe Interactions 17 : 202 215.
24. Jorge JA, Polizeli MTM, Thevelein JM, Terenzi HF. 1997. Trehalases and trehalose hydrolysis in fungi. FEMS Microbiology Letters 154 : 165 171.
25. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 : 97 101.
26. Kitamoto Y, Osaki N, Tanaka H, Sasaki H, Mori N. 1998. Purification and properties of α-glucose 1-phosphate-forming trehalose phosphorylase from the basidiomycete Pleurotus ostreatus. Mycoscience 41 : 607 613.
27. Koide R, Sharda JN, Herr JR, Malcolm GM. 2008. Ectomycorrhizal fungi and the biotrophy-saprotrophy continuum. New Phytologist 178 : 230 233.
28. Le Quéré A, Wright D, Söderström B, Tunlid A, Johansson T. 2005. Global patterns of gene regulation associated with the development of ectomycorrhiza between birch Betula pendula Roth. and Paxillus involutus Batsch fr. Molecular Plant-Microbe Interactions 18 : 659 673.
29. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P. 2004. SMART 4.0: towards genomic data integration. Nucleic Acids Research 32 : 142 144.
30. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA et al. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307 : 1321 1324.
31. López MF, Dietz S, Grunze N, Bloschies J, Weiß M, Nehls U. 2008. The sugar porter gene family of Laccaria bicolor: function in ectomycorrhizal symbiosis and soil growing hyphae. New Phytologist 180 : 365 378.
32. López MF, Männer P, Hampp R, Nehls U. 2007. Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas. New Phytologist 174 : 389 398.
33. Luster J, Finlay R. 2006. Microbial growth and visualisation of bacteria and fungi. In : Luster J, Finlay RD, eds. Handbook of methods used in rhizosphere research. Birmensdorf, Switzerland : Swiss Federal Research Institute WSL, 399 400.
34. Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, 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.
35. Martin F, Boiffin V, Pfeffer PE. 1998. Carbohydrate and amino acid metabolism in the Eucalyptus globules-Pisolithus tinctorius ectomycorrhizal during glucose utilization. Plant Physiology 118 : 627 635.
36. 13C nuclear magnetic resonance. Physiologie Végétale 242 : 209 218.
37. 13C nuclear magnetic resonance study of mannitol cycle and trehalose synthesis during glucose utilization by the ectomycorrhizal ascomycete Cenococcum graniforme. Plant Physiology 77 : 499 502.
38. Martin F, Ramstedt M, Söderhäll K. 1987. Carbon and nitrogen metabolism in ectomycorrhizal fungi and ectomycorrhizas. Biochimie 69 : 569 581.
39. Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F et al. 2004. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nature Biotechnology 22 : 695 700.
40. Moran NA. 2007. Symbiosis as an adaptative process and source of phenotypic complexity. Proceedings of the National Academy of Sciences, USA 104 : 8627 8633.
41. Moreno F, Herrero P. 2002. The hexokinase 2-dependent glucose signal transduction pathway of Saccharomyces cerevisiae. FEMS Micobiology Reviews 26 : 83 90.
42. Nehls U, Grunze N, Willmann M, Reich M, Küster H. 2007. Sugar for my honey: carbohydrate partitioning in ectomycorrhizal symbiosis. Phytochemistry 68 : 82 91.
43. Nehls U, Mokolajewski S, Magel E, Hampp R. 2001. Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytologist 150 : 533 541.
44. Parrou J-L, Jules M, Beltran G, François J. 2005. Acid trehalase in yeasts and filamentous fungi: localization, regulation and physiological function. FEMS Yeast Research 5 : 503 511.
45. 13C NMR study. Agriculture, Ecosystems & Environment 28 : 409 414.
46. 13C-NMR study of exudation and storage of carbohydrates and amino acids in the ectomycorrhizal edible mushroom Cantharellus cibarius. Mycologia 94 : 190 199.
47. Saito K, Yamazaki H, Ohnishi Y, Fujimoto S, Takahashi E, Horinouchi S. 1998. Production of trehalose synthase from a basidiomycete, Grifola frondosa, in Escherichia coli. Applied Microbiology Biotechnology 50 : 193 198.
48. Stambuk BU, de Araujo PS. 2001. Kinetics of active α-glucoside transport in Saccharomyces cerevisiae. FEMS Yeast Research 1 : 73 78.
49. Stoop JMH, Mooibroek H. 1998. Cloning and characterization of NADP-mannitol dehydrogenase cDNA from the button mushroom, Agaricus bisporus, and its expression in response to NaCl stress. Applied Environmental Microbiology 64 : 4689 4696.
50. Swofford DL. 1999. paup*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA, USA : Sinauer Associates.
51. Voegele RT, Hahn M, Lohaus G, Link T, Heiser I, Mendgen K. 2005. Possible roles for mannitol and mannitol dehydrogenase in the biotrophic plant pathogen Uromyces fabae. Plant Physiology 137 : 190 198.
52. Voiblet C, Duplessis S, Encelot N, Martin F. 2001. Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant Journal 25 : 181 191.
53. Wannet WJ, Op den Camp HJ, Wisselink HW, van der Drift C, van Griensven LJ, Vogels GD. 1998. Purification and characterization of trehalose phosphorylase from the commercial mushroom Agaricus bisporus. Biochimica Biophysica Acta 14251 : 177 188.
54. Wiemken V. 2007. Trehalose synthesis in ectomycorrhizas - a driving force of carbon gain for fungi. New Phytologist 174 : 228 230.
55. Wiese J, Kleber R, Hampp R, Nehls U. 2001. Functional characterization of the Amanita muscaria monosaccharide transporter Ammst1. Plant Biology 2 : 1 5.
56. Zdobnov EM, Apweiler R 2001. InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17 : 847 848.