Abstract
Ectomycorrhizal formation is a highly regulated process involving the molecular reorganization of both partners during symbiosis. An analogous molecular process also occurs during the pre-symbiotic phase, when the partners exchange molecular signals in order to position and prepare both organisms for the establishment of symbiosis. To gain insight into genetic reorganization in Tuber borchii during its interaction with its symbiotic partner Tilia americana, we set up a culture system in which the mycelium interacts with the plant, even though there is no actual physical contact between the two organisms. The selected strategies, suppressive subtractive hybridisation and reverse Northern blots, allowed us to identify, for the first time, 58 cDNA clones differentially expressed in the pre-symbiotic phase. Sequence analysis of the expressed sequence tags showed that the expressed genes are involved in several biochemical pathways: secretion and apical growth, cellular detoxification, general metabolism and both mutualistic and symbiotic features.
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Brummer MH, Kivinen KJ, Jantti J, Toikkanen J, Soderlund H, Keranen S (2001) Characterization of the sec1-1 and sec1-11 mutations. Yeast 18:1525–1536
Brun A, Chalot M, Finlay RD, Soderstorm B (1995) Structure and function of the ectomycorrhizal association between Paxillus involutus (Batsch) Fr. & Betula pendula Roth. I. Dynamics of mycorrhizae formation. New Phytol 129:487–493
Burgess T, Laurent P, Dell B, Malajczuk N, Martin F (1995) Effect of the fungal isolate aggressivity on the biosynthesis of symbiosis—related polypeptides in differentiating eucalypt ectomycorrhiza. Planta 195:408–417
Calabrese D, Bille J, Sanglard D (2000) A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology 146:2743–2754
Chen XY, Hampp R (1993) Sugar uptake by protoplast of the ectomycorrhizal fungus Amanita muscaria (L Ex Fr) Hooker. New Phytol 125:1883–1887
Cullen D (1997) Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol 53:273–289
De Bernardis F, Muhlschlegel FA, Cassone A, Fonzi WA (1998) The pH of the host niche controls gene expression and virulence of Candida albicans. Infect Immun 66:3317–3325
Duchesne LC, Peterson RL, Ellis BE (1989) The time course of disease suppression and antibiosis by the ectomycorrhizal fungus Paxillus involutus. New Phytol 111:693–698
Ghannoum MA, Spellberg B, Saporito-Irwin SM, Fonzi WA (1995) Reduced virulence of Candida albicans PHR1 mutants. Infect Immun 63:4528–4530
Gianinazzi-Pearson V, Brechenmacher L, Tamasloukht M, Bécard G, La Camera S, Gianinazzi S, Franken P (2002) Functional genomics of fungal–plant communication in the arbuscolar mycorrhizal symbiosis. Int Mycol Congr 7:11–17
Hall RI, Yun W, Amicucci A (2003) Cultivation of edible ectomycorrhizal mushrooms. Trends Biotechnol 21:433–438
Hirozumi K, Nakajima H, Machida M, Yamaguchi M, Takeo K, Kitamoto K (1999) Cloning and characterization of a gene (arpA) from Aspergillus oryzae encoding an actin-related protein required for normal nuclear distribution and morphology of conidiophores. Mol Gen Genet 262:758–767
Kersten PJ, Witek C, Wymelenberg AV, Cullen D (1995) Phanerochaete chrysosporium glyoxal oxidase is encoded by two allelic variants: structure, genomic organization, and heterologous expression of glx1 and glx2. J Bacteriol 177:6106–6110
Kim SJ, Zheng J, Hiremath ST, Podila GK (1998) Cloning and characterization of a symbiosis-related gene from an ectomycorrhizal fungus Laccaria bicolour. Gene 222:203–212
Lamb D, Kelly D, Kelly S (1999) Molecular aspects of azole antifungal action and resistance. Drug Resist Updates 2:390–402
Laurent P, Voiblet C, Tagu D, de Carvalho D, Nehls U, De Bellis R, Balestrini R, Bauw G, Bonfante P, Martin F (1999) A novel class of ectomycorrhiza-regulated cell wall polypeptides in Pisolithus tinctorius. Mol Plant Microbe Interact 12:862–871
Martin F, Lapeyrie F, Tagu D (1997) Altered gene expression during ectomycorrhiza development in the mycota. In: Lemke P, Caroll G (eds) Plant Relationship, vol VI. Springer, Berlin Heidelberg New York, pp 223–242
Martin F, Duplessis S, Dintengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Development of cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154
Menotta M, Gioacchini AM, Buffalini M, Amicucci A, Sisti D, Stocchi V (2004) Headspace solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system. Rapid Commun Mass Spectrom 18:206–210
Mouyana I, Fontaine T, Vai M, Monod M, Fonzi WA, Diaquin M, Popolo L, Hartland RP, Latge JP (2000) Glycosylphosphatidylinoisotl-anchored gluconyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275:14882–14889
Muhlschlegel FA, Fonzi WA (1997) PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol Cell Biol 17:5960–5967
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nehls U, Weise J, Guttenberger M, Hampp R (1998) Carbon allocation in ectomycorrhizae: identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol Plant Microbe Interact 11:167–176
Nehls U, Ecke M, Hampp R (1999) Sugar and nitrogen-dependent regulation of an Amanita muscaria phenylalanine ammonium lyase gene. J Bacteriol 181:1931–1933
Peng R, Gallwitz D (2002) Sly1 protein bound to Golgi syntaxin Sed5p allows assembly and contributes to specificity of SNARE fusion complexes. J Cell Biol 157:645–655
Perez-Moreno J, Read DJ (2000) Mobilization and transfer of nutrients from litter to tree seedling via the vegetative mycelium of ectomycorrhizal plants. New Phytol 145:301–309
Podila GK, Zheng S, Balasubramanian S, Sundaram S, Hiremath S, Brand JH, Hymes MJ (2002) Fungal gene expression in early symbiotic interaction between Laccaria bicolor and red pine. Plant Soil 244:117–128
Polidori E, Agostini D, Zeppa S, Potenza L, Palma F, Sisti D, Stocchi V (2002) Identification of differentially expressed cDNA clones in Tilia Platyphyllos–Tuber borchii ectomycorrhizae using differential screening approach. Mol Genet Genomics 266:858–864
Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient adsorbing surface of pine. New Phytol 128:639–644
Salzer P, Hager A (1991) Sucrose utilization of ectomycorrhizal fungi Amanita muscaria and Hebeloma crustuliniforme depends on the cell wall-bound invertase activity of their host Picea abies. Bot Acta 104:439–444
Saporito-Irwin SM, Birse CE, Sypherd PS, Fonzi WA (1995) PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol Cell Biol 15:601–613
Seo KW, Park M, Kim JG, Kim TW, Kim HJ (2000) Effects of benzothiazole on the xenobiotic metabolizing enzymes and metabolism of acetaminophen. J Appl Toxicol 20:427–430
Sundaram S, Kim SJ, Suzuki H, Mcquattie CJ, Hiremath ST, Podila GK (2001) Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol Plant Microbe Interact 14:628
Suwanchaichinda C, Brattsten LB (2002) Induction of microsomal cytochrome P450s by tire-leachate compounds, habitat components of Aedes albopictus mosquito larvae. Arch Insect Biochem Physiol 49:71–79
Tagu D, Phyton M, Cretin C, Martin F (1993) Cloning symbiosis related cDNAs from eucalypt ectomycorrhizal by PCR assisted differential screening. New Phytol 125:339–343
Voiblet C, Duplessis S, Encelot N, Martin F (2001) Identification of symbiosis regulated genes in Eucaliptus globus–Pisolithus tinctorius ectomycorrhizal by differential hybridization of arrayed cDNA. Plant J 25:181–191
Weig M, Haynes K, Rogers TR, Kurzai O, Frosch M, Muhlschlegel FA (2001) A GAS-like gene family in the pathogenic fungus Candida glabrata. Microbiology 147:2007–2019
Xiang X, Morris NR (1999) Hyphal tip growth and nuclear migration. Curr Opin Microbiol 2:636–640
Sisti D, Zambonelli A, Giomaro G, Rossi I, Ceccaroli P, Citterio B, Benedetti PA, Stocchi V (1998) In vitro mycorrhizal synthesis of micropropagated Tilia platyphyllos Scop. plantlets with Tuber borchii Vittad. mycelium in pure culture. Acta Hortic 457:379–387
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Menotta, M., Amicucci, A., Sisti, D. et al. Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad. and Tilia americana L.. Curr Genet 46, 158–165 (2004). https://doi.org/10.1007/s00294-004-0518-4
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DOI: https://doi.org/10.1007/s00294-004-0518-4