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

Volumn 175, Issue 4, 2007, Pages 743-755

  Deveau, A ^a   Palin, B ^a   Delaruelle, C ^a   Peter, M ^a   Kohler, A ^a   Pierrat, J C ^b   Sarniguet, A ^c   Garbaye, J ^a   Martin, F ^a   Frey Klett, P ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b LERFoB   (France)

^c AGROCAMPUS OUEST   (France)

Author keywords

Fungal bacterial interactions; Laccaria bicolor S238N; Mycorrhiza helper bacteria; Rhizobacteria; Transcriptome

Indexed keywords

FUNGAL DNA; FUNGAL PROTEIN; FUNGAL RNA;

BIOASSAY; ECTOMYCORRHIZA; FUNGUS; GENE EXPRESSION; GROWTH RATE; MORPHOLOGY; RHIZOBACTERIUM;

ARTICLE; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCELIUM; MYCORRHIZA; PHYSIOLOGY; PSEUDOMONAS FLUORESCENS;

DNA, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MYCELIUM; MYCORRHIZAE; PSEUDOMONAS FLUORESCENS; RNA, FUNGAL; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); FUNGI; LACCARIA; LACCARIA BICOLOR; PSEUDOMONAS FLUORESCENS; RHIZOBIALES;

EID: 34547650367     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2007.02148.x     Document Type: Article

References (48)

1. Akiyama K, Matsuzaki K-I, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435 : 824 827.
2. Allard S, Utley R, Savard J, Clarke A, Grant P, Brandl C, Pillus L, Workman J, Côté J. 1999. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO Journal 18 : 5108 5119.
3. Aspray T, Frey-Klett P, Jones JE, Whipps J, Garbay J, Bending G. 2006. Mycorrhization helper bacteria: a case of specificity for altering ectomycorrhiza architecture but not ectomycorrhiza formation. Mycorrhiza. 16 : 533 541.
4. Becker D, Bagley S, Podila G. 1999. Effects of mycorrhizal-associated streptomycetes on growth of Laccaria bicolor, Cenococcum geophilum, and Armillaria species and on gene expression in Laccaria bicolor. Mycologia 91 : 33 40.
5. Bending G. 2007. What are the mechanisms and specificity of mycorrhization helper bacteria? New Phytologist 174 : 707 710.
6. Bertaux J, Schmid M, Chemidlin Prevost-Boure N, Churin JL, Hartmann A, Garbaye J, Frey-Klett P. 2003. In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Applied and Environmental Microbiology 69 : 4243 4248.
7. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J-C, Roux C, Bécard G, Séjalon-Delmas N. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology 4 : 1239 1247.
8. de Boer W, Leveau J, Kowalschuk G, Klein Gunnewiek P, Abeln E, Figge M, Sjollema K, Janse J, van Veen J. 2004. Collimonas fungivorans General. Nov, sp. Nov, a chitinolytic soil bacterium with the ability to grow on living fungal hyphae. International Journal of Systematic and Evolutionnary Microbiology 54 : 857 864.
9. Bolwerk A, Lagopodi A, Wijfjes A, Lamers G, Chin A Woeng T, Lugtenberg B, Bloemberg G. 2003. Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f. sp. radicis-lycopersci. Molecular Plant-Microbe Interactions 16 : 983 993.
10. Brown C, Howe L, Soussa K, Alley S, Carroza M, Tan S, Workman J. 2001. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra 1 subunit. Sciences 292 : 2333 2337.
11. Brulé C, Frey-Klett P, Pierrat J-C, Courrier S, Gérard F, Lemoin M-C, Roussellet J-L, Sommer J, Garbaye J. 2001. Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and effect of a mycorrhiza helper Pseudomonas fluorescens. Soil Biology and Biochemistry 33 : 1683 1694.
12. Chapon A, Guillerm A-Y, Delalande L, Lebreton L, Sarniguet A. 2002. Dominant colonisation of wheat roots by Pseudomonas fluorescens Pf29A and selection of the indigenous microflora in the presence of the take-all fungus. European Journal of Plant Pathology 108 : 449 459.
13. Cosma MP. 2002. Ordered recruitment: gene-specific mechanism of transcription activation. Molecular Cell 10 : 227 236.
14. Di Battista C, Selosse M-A, Bouchard D, Senström E, Le Tacon F. 1996. Variations in symbiotic efficiency, phenotypic charachters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S238. Mycological Research 100 : 1315 1324.
15. 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.
16. Duponnois R, Garbaye J. 1991. Effect of dual inoculation of Douglas fir with the ectomycorrhizal fungus Laccaria laccata and mycorrhization helper bacteria (MHB) in two bare-root forest nurseries. Plant Soil 138 : 169 176.
17. Duponnois R, Plenchette C. 2003. A mycorrhizal helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13 : 85 91.
18. Founoune H, Duponnois R, Bâ AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL. 2002. Mycorrhiza helper bacteria stimulate ectomycorrhizal symbiosis of Accacia holoserica with the Pisolithus albus. New Phytologist 153 : 81 89.
19. Frey-Klett P, Garbaye J. 2005. Mycorrhiza helper bacteria: a promising model for the genomic analysis of fungal-bacterial interactions. New Phytologist 168 : 4 8.
20. Frey-Klett P, Pierrat J-C, Garbaye J. 1997. Location and survival of mycorrhizal helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Applied and Environmental Microbiology 63 : 139 144.
21. Garbaye J. 1994. Mycorrhiza helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytologist 128 : 197 210.
22. Gasch A, Werner-Washburne M. 2002. The genomics of yeast responses to environmental stress and starvation. Functional & Integrative Genomics 2 : 181 192.
23. Hildebrandt U, Ouziad F, Marner F-J, Bothe H. 2006. The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiology Letters 254 : 258 267.
24. Huh C, Aldrich J, Mottahedeh J, Kwon H, Johnson C, Mrsh R. 1998. Cloning and characterization of Physarum polycepharum tectonins. Homologues of limulus lectin L6. Journal of Biological Chemistry 273 : 6565 6574.
25. Kohler A, Delaruelle C, Martin D, Encelot N, Martin F. 2003. The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Letters 542 : 37 41.
26. Le Quéré A, Eriksen KA, Rajashekar B, Schütznedü bel A, Canbäck B, Johansson T, Tunlid A. 2006. Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Molecular Ecology 15 : 535 550.
27. Livak K, Schmittgen D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods. 25 : 402 408.
28. Maier A, Riedlinger J, Fiedler H-P, Hampp R. 2004. Actinomycetales bacteria from a spruce strand: characterization and effects on growth of root symbiotic, and plant parasitic soil fungi in dual culture. Mycological Progress 3 : 129 136.
29. Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F. 2001. Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytologist 151 : 145 154.
30. Melin P, Schnürer J, Wagner EGH. 2002. Proteome analysis of Aspergillus nidulans reveals proteins associated with the response to the antibiotic concanamycin A, produced by Streptomyces species. Molecular Genetics and Genomics 267 : 695 702.
31. Morel M, Jacob C, Kohler A, Johansson T, Martin F, Chalot M, Brun A. 2005. Identification of genes differentially expressed in extraradical mycelium and ectomycorrhizal roots during Paxillus involutus-Betula pendula ectomycorrhizal symbiosis. Applied and Environmental Microbiology 71 : 382 391.
32. Paschlewski R, Pachlewska J. 1974. Studies on symbiotic properties of mycorrhizal fungi of pine (Pinus sylvestris L.) with the aid of the method of mycorrhizal synthesis in pure cultures on agar. (Translated Into English by Royal Dzieciolowski). Warsaw, Poland : Forest Research Institute.
33. Peter M, Courty P-E, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F. 2003. Analysis of expressed sequenced tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus macrocarpus. New Phytologist 159 : 117 129.
34. Peterson L, Bonfante P. 1994. Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant and Soil 159 : 79 88.
35. Podila G, Zheng J, Balasubramanian S, Sundaram S, Hiremath S, Brand J, Hymes M. 2002. Fungal gene expression in early symbiotic interactions between Laccaria bicolor and red pine. Plant and Soil 244 : 117 128.
36. Poole E, Bending G, Whipps J, Read D. 2001. Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhizal formation in vitro. New Phytologist 151 : 743 751.
37. Pray-Grant M, Schieltz D, McM, Ahon S, Wood J, Cook R, Workman J, Yates J, III. Grant P. 2002. The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Molecular and Cellular Biology 22 : 8774 8786.
38. Requena N, Füller P, Franken P. 1999. Molecular charcterization of GmFOX2 an evolutionary highly conserved gene from the mycorrhizal fungus Glomus mosseae, down regulated during interaction with rhizobacteria. Molecular Plant-Microbe Interactions 12 : 934 942.
39. Riedlinger J, Schrey S, Tarkka M, Hampp R, Kapur M, Fielder H-P. 2006. Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Applied and Environmental Microbiology 72 : 3350 3557.
40. Sambrook J, Fritsch E, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, NY, USA : Cold Spring Harbor Laboratory Press.
41. Schrey S, Schellhammer M, Ecke M, Hampp R, Tarkka M. 2005. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytologist 168 : 205 216.
42. Sen RE-L, Nurmiaho-Lassila K, Haahtela et T, Korhonen. 1994. Attachment of Pseudomonas fluorescense trains to the cell walls of ectomycorrhizal fungi. In : Azcon-Aguilar C, Barea JM, ed. Mycorhizas in integrated systems from genes to plant development. European Commission EUR 16728 EN. Luxembourg, 661 664.
43. Smith S, Read D. 1997. Mycorrhizal symbiosis, 2nd edn. London, UK : Academic Press.
44. Sterner D, Belotserkovskaya R, Berger S. 2002. SALSA, a variant of yeast SAGA, contains truncated Spt7, which correlates with activated transcription. Proceedings of the National Academy of Sciences, USA 99 : 11622 11627.
45. Ström K, Schnürer Melin P. 2005. Co-cultivation of antifungal Lactobacillus plantarum MiLAB 393 and Aspergillus nidulans, evaluation of effects on fungal growth and protein expression. FEMS Microbiology Letters 246 : 119 124.
46. Tachibana C, Yoo J, Tagne J-B, Kacherovsky N, Lee T, Young E. 2005. Combined global localization analysis and transcriptome data to identify genes that are directly coregulated by Adr1 and Cat8. Molecular Cell and Biology 25 : 2138 2146.
47. Wu J, Zhang N, Hayes A, Panoutsopoulou K, Oliver S. 2004. Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth. Proceedings of the National Academy of Sciences, USA 101 : 3148 3153.
48. Xie X, Wilkinson H, Correa A, Lewis Z, Bell-Pederson D, Ebbole D. 2004. Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genetics and Biology 41 : 1104 1119.