RNA silencing in the model mycorrhizal fungus Laccaria bicolor: Gene knock-down of nitrate reductase results in inhibition of symbiosis with Populus

Environmental Microbiology

Volumn 11, Issue 7, 2009, Pages 1878-1896

  Kemppainen, Minna ^a,b   Duplessis, Sébastien ^c   Martin, Francis ^c   Pardo, Alejandro G ^a,b  

^a UNIVERSIDAD NACIONAL DE QUILMES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; NITRATE; NITRATE REDUCTASE; NITROGEN;

ARTICLE; ASPEN; BIOSYNTHESIS; CHEMISTRY; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LACCARIA; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; RHIZOBIUM; RNA INTERFERENCE; SYMBIOSIS;

CULTURE MEDIA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKDOWN TECHNIQUES; LACCARIA; MYCORRHIZAE; NITRATE REDUCTASE; NITRATES; NITROGEN; POPULUS; RHIZOBIUM; RNA INTERFERENCE; SYMBIOSIS; TRANSFORMATION, GENETIC;

AGROBACTERIUM; FUNGI; LACCARIA; LACCARIA BICOLOR; POPULUS; RHIZOBIUM;

EID: 67649979510     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01912.x     Document Type: Article

References (54)

1. Bailly, J., Debaud, J.C., Verner, M.C., Plassard, C., Chalot, M., Marmeisse, R. Fraissinet-Tachet, L. (2007) How does symbiotic fungus modulate expression of its host-plant nitrite reductase? New Phytol 175 : 155 165. (Pubitemid 46854914)
2. Baulcombe, D. (2004) RNA silencing in plants. Nature 431 : 356 363. (Pubitemid 39265676)
3. Bohse, M.L. Woods, J.P. (2007) RNA interference-mediated silencing of the YPS3 gene of Histoplasma capsulatum reveals virulence defects. Infect Immun 75 : 2811 2817. (Pubitemid 46870161)
4. Cardoza, R.E., Vizcaino, J.A., Hermosa, M.R., Sousa, S., Gonzalez, F.J., Llobell, A., et al. (2006) Cloning and characterization of the erg1 of Trichoderma harzianum: effect of the erg1 silencing on ergosterol biosynthesis and resistance to terbinafine. Fungal Genet Biol 43 : 164 178. (Pubitemid 43357967)
5. Chaveroche, M.K., Ghigo, J.M. D'Enfert, C. (2000) A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28 : E97.
6. Chen, X., Stone, M., Schlagnhaufer, C. Romaine, C.P. (2000) A fruiting body tissue method for efficient Agrobacterium-mediated transformation of Agaricus bisporus. Appl Environ Microbiol 66 : 4510 4513. (Pubitemid 30768553)
7. Codon, A.C., Lee, Y.S. Russo, V.E. (1997) Novel pattern of DNA methylation in Neurospora crassa transgenic for the foreign gene hph. Nucleic Acids Res 25 : 2409 2416. (Pubitemid 27303701)
8. Colot, H.V., Parks, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., et al. (2006) A high-throughput gene knockout procedure for Neurospora crassa reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103 : 10353 10357.
9. Combier, J.P., Melayah, D., Raffier, C., Gay, G. Marmeisse, R. (2003) Agrobacterium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum. FEMS Microbiol Lett 220 : 141 148. (Pubitemid 36324333)
10. Combier, J.P., Melayah, D., Raffier, C., Pépin, R., Marmeisse, R. Gay, G. (2004) Nonmycorrhizal (myc-) mutants of Hebeloma cylindrosporum obtained through insertional mutagenesis. Mol Plant-Microbe Interact 17 : 1029 1038. (Pubitemid 39098891)
11. Di Battista, C., Selosse, M.A., Bouchard, D., Stenström, E. Le Tacon, F. (1996) Variation in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S238. Mycol Res 100 : 1315 1324.
12. Duplessis, S., Courty, P.E., Tagu, D. Martin, F. (2005) Transcript patterns associated with ectomycorrhizal development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165 : 599 611. (Pubitemid 40177968)
13. Gong, X., Fu, Y., Jiang, D., Li, G., Yi, X. Peng, Y. (2007) 1-arginine is essential for conidiation in the filamentous fungus Coniothyrium minitans. Fungal Genet Biol 44 : 1368 1379. (Pubitemid 350046360)
14. Guescini, M., Pierleoni, R., Palma, F., Zeppa, S., Vallorani, L., Potenza, L., et al. (2003) Characterization of the Tuber borchii nitrate reductase gene and its role in ectomycorrhizae. Mol Gen Genomics 269 : 807 816. (Pubitemid 37214937)
15. Guescini, M., Zeppa, S., Pierleoni, R., Sisti, D., Stocchi, L. Stocchi, V. (2007) The expression profile of the Tuber borchii nitrite reductase suggest its positive contribution to the host-plant nitrogen nutrition. Curr Genet 51 : 31 41. (Pubitemid 44873608)
16. Heller, G., Adomas, A., Li, G., Osborne, J., van Zyl, L., Sederoff, R., et al. (2008) Transcriptional analysis of Pinus sylvestris roots challenged with the ectomycorrhizal fungus Laccaria bicolor. BMC Plant Biol 8 : 1 13.
17. Johansson, T., Le Quéré, A., Ahren, D., Söderström, B., Erlandsson, R., Lundeberg, J., et al. (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant-Microbe Interact 17 : 202 215. (Pubitemid 38391001)
18. de Jong, J.F., Deelstra, H.J., Wösten, H.A.B. Lugones, L.G. (2006) RNA-mediated gene silencing in monokaryons and dikaryons of Schizophyllum commune. Appl Environ Mircrobiol 72 : 1267 1269. (Pubitemid 43271235)
19. Kaldorf, M., Schmelzer. E. Bothe, H. (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol Plant-Microbe Interact 11 : 439 448. (Pubitemid 28244569)
20. Kemppainen, M., Circosta, A., Tagu, D., Martin, F. Pardo, A.G. (2005) Agrobacterium-mediated transformation of the ectomycorrhizal symbiont Laccaria bicolor S238N. Mycorrhiza 16 : 19 22. (Pubitemid 41618813)
21. Kemppainen, M., Duplessis, S., Martin, F. Pardo, A.G. (2008) T-DNA insertion, plasmid rescue and integration analysis in the model mycorrhizal fungus Laccaria bicolor. Microbial Biotechnol 1 : 258 269.
22. 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. Mol Plant-Microbe Interact 18 : 659 673. (Pubitemid 40832033)
23. Liu, G., Casqueiro, J., Bañuelos, O., Cardoza, R.E., Gutiérrez, S. Martín, J.F. (2001) Targeted inactivation of the mecB gene, encoding cystathione-gamma-lyase, shows that the reverse transsulfuration pathway is required for high-level cephalosporin biosíntesis in Acremonium chysogenum C10 but not for methionine induction of the cephalosporin genes. J Bacteriol 183 : 1765 1772. (Pubitemid 32172321)
24. Liu, H., Cottrell, T.R., Pierini, L.M., Goldman, W.E. Doering, T.L. (2002) RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160 : 463 470. (Pubitemid 34194522)
25. Liu, Y.G., Mitsukawa, L.N., Oosumi, T. Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8 : 457 463.
26. McDonald, T., Brown, D., Keller, N.P. Hammond, T.M. (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant-Microbe Interact 18 : 539 545. (Pubitemid 40728007)
27. Marmeisse, R., Jargeat, P., Wagner, F., Gay, G. Debaud, J.C. (1998) Isolation and characterization of nitrate reductase deficient mutants of the ectomycorrhizal fungus Hebeloma cylindrosporum. New Phytol 140 : 311 318. (Pubitemid 28501787)
28. Martin, F. Selosse, M.A. (2008) The Laccaria genome: a symbiont blueprint decoded. New Phytol 180 : 296 310.
29. Martin, F., Kholer, A. Duplessis, S. (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10 : 204 210. (Pubitemid 46330109)
30. Martin, F., Aerts, A., Ahrén, D., Brun, A., Danchin, E.G., Duchaussoy, F., et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452 : 88 92. (Pubitemid 351355085)
31. Marzluf, G.A. (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiol Mol Biol Rev 61 : 17 32. (Pubitemid 27290922)
32. Matzke, M.A., Matzke, A.J.M. Kooter, J.M. (2001) RNA: guiding gene silencing. Science 293 : 1080 1083. (Pubitemid 32758078)
33. Mello, C. Conte, D. (2004) Revealing the world of RNA interference. Nature 431 : 338 342. (Pubitemid 39265673)
34. Menotta, M., Amicucci, A., Sisti, D., Gioacchini, A.M. Stocchi, V. (2004) Differential gene expression during pre-symbiotic interaction between Tuber borchii Vitad. & Tilia americana L. Curr Genet 46 : 158 165. (Pubitemid 39307204)
35. Montanini, B., Gabella, S., Abbà, S., Peter, M., Kohler, A., Bonfante, P., et al. (2006a) Gene expression profiling of the nitrogen starvation stress response in the mycorrhizal ascomycete Tuber borchii. Fungal Genet Biol 43 : 630 641. (Pubitemid 44175876)
36. Montanini, B., Viscomi, A.R., Bolchi, A., Martin, Y., Siverio, J.M., Balestrini, R., et al. (2006b) Functional properties and differential mode of regulation of the nitrate transporter from a plant symbiotic ascomycete. Biochem J 394 : 125 134. (Pubitemid 43259662)
37. Morris, K.V., Chan, S.W., Jacobsen, S.E. Looney, D.J. (2004) Small interfering RNA-induced transcriptional gene silencing in human cells. Science 305 : 1289 1292. (Pubitemid 39129233)
38. Mullins, E.D., Chen, X., Romaine, C.P., Raina, R., Geiser, D.M. Kang, S. (2001) Agrobacterium-mediated transformation of Fusarium oxysporum: an efficient tool for insertional mutagenesis and gene transfer. Phytopathology 91 : 173 180. (Pubitemid 32106557)
39. Nakayashiki, H. Kadotani, N.S.M. (2006) Evolution and diversification of RNA silencing proteins in fungi. J Mol Evol 63 : 127 135. (Pubitemid 43992011)
40. Nakayashiki, H., Hanada, S., Nguyen, B.Q., Kadotani, N., Tosa, Y. Mayama, S. (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet Biol 42 : 275 283. (Pubitemid 40321142)
41. Namekawa, S.H., Iwabata, K., Sugawara, H., Hamada, F.N., Koshiyama, A., Chiku, H., et al. (2005) Knockdown of LIM/DMC1 in the mushroom Coprinus cinereus by double-stranded RNA-mediated gene silencing. Microbiology 151 : 3669 3678. (Pubitemid 41632077)
42. Nygren, C.M.R., Eberhardt, U., Karlsson, M., Parrent, J., Lindhal, B.J. Taylor, A.F.S. (2008) Growth on nitrate and occurrence of nitrate reductase-encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi. New Phytol 180 : 875 889.
43. Peter, M., Courty, P.E., Kohler, A., Delaruelle, C., Martin, D., Tagu, D., et al. (2003) Analysis of expressed sequence tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus microcarpus. New Phytol 159 : 117 129. (Pubitemid 36738344)
44. Podila, G.K., Zheng, J., Balasubramanian, S., Sundaram, S., Hiremath, S., Brend, J.H. Hymes, M.J. (2002) Fungal gene expression in early symbiotic interaction between Laccaria bicolor and red pine. Plant Soil 244 : 117 128.
45. Pöggeler, S. Kück, U. (2006) Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378 : 1 10. (Pubitemid 44108460)
46. 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 a differential screening approach. Mol Genet Genomics 266 : 858 864.
47. Rappleye, C.A., Engle, J.T. Coldman, W.E. (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53 : 153 165. (Pubitemid 38901387)
48. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY, USA : Cold Spring Harbor Laboratory.
49. Sawyer, N.A., Chambers, S.M. Cairney, J.W.G. (2003) Variation in nitrogen source utilization by nine Amanita muscaria genotypes from Australian Pinus radiata plantations. Mycorrhiza 13 : 217 221. (Pubitemid 37084237)
50. Smith, S.E. Read, D.J. (1997) Mycorrhizal Symbiosis. London, UK : Academic Press.
51. Tuschl, T. (2001) RNA interference and small interfering RNAs. Chembiochem 2 : 239 245. (Pubitemid 33722551)
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 J 25 : 181 191. (Pubitemid 32122752)
53. Wälti, M.A., Villalba, C., Buser, R.M., Grünler, A., Aebi, M. Künzler, M. (2006) Targeted gene silencing in the model mushroom Coprinus cinerea (Coprinus cinereus) by expression of homologous hairpin RNAs. Euk Cell 5 : 732 744.
54. Zofall, M. Grewal, S.I. (2006) RNAi-mediated heterochromatin assembly in fission yeast. Cold Spring Harbor Symp Quant Biol 71 : 487 496.