Current Genetics

, Volume 52, Issue 2, pp 77–85

Interaction with mycorrhiza helper bacterium Streptomyces sp. AcH 505 modifies organisation of actin cytoskeleton in the ectomycorrhizal fungus Amanita muscaria (fly agaric)

  • Silvia D. Schrey
  • Vanamo Salo
  • Marjatta Raudaskoski
  • Rüdiger Hampp
  • Uwe Nehls
  • Mika T. Tarkka
Research Article

Abstract

The actin cytoskeleton (AC) of fungal hyphae is a major determinant of hyphal shape and morphogenesis, implicated in controlling tip structure and secretory vesicle delivery. Hyphal growth of the ectomycorrhizal fungus Amanita muscaria and symbiosis formation with spruce are promoted by the mycorrhiza helper bacterium Streptomyces sp. AcH 505 (AcH 505). To investigate structural requirements of growth promotion, the effect of AcH 505 on A. muscaria hyphal morphology, AC and actin gene expression were studied. Hyphal diameter and mycelial density decreased during dual culture (DC), and indirect immunofluorescence microscopy revealed that the dense and polarised actin cap in hyphal tips of axenic A. muscaria changes to a loosened and dispersed structure in DC. Supplementation of growth medium with cell-free bacterial supernatant confirmed that reduction in hyphal diameter and AC changes occurred at the same stage of growth. Transcript levels of both actin genes isolated from A. muscaria remained unaltered, indicating that AC changes are regulated by reorganisation of the existing actin pool. In conclusion, the AC reorganisation appears to result in altered hyphal morphology and faster apical extension. The thus improved spreading of hyphae and increased probability to encounter plant roots highlights a mechanism behind the mycorrhiza helper effect.

Keywords

Actin cytoskeleton Hyphal tip growth Mycorrhiza helper bacterium 

Supplementary material

References

  1. Aktories K, Barbieri JT (2005) Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 3:397–410PubMedCrossRefGoogle Scholar
  2. Duplessis S, Courty PE, Tagu D, Martin F (2005) Transcript pattern associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus tinctorius. New Phytol 165:599–611PubMedCrossRefGoogle Scholar
  3. Frankel S, Mooseker MS (1996) The actin-related proteins. Curr Opin Cell Biol 8:30–37PubMedCrossRefGoogle Scholar
  4. Founoune H, Duponnois R, Ba AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL (2002) Mycorrhiza helper bacteria stimulated ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus alba. New Phytol 153:81–89CrossRefGoogle Scholar
  5. Garbaye J (1994) Mycorrhiza helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  6. Garbaye J, Bowen GD (1989) Stimulation of mycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388CrossRefGoogle Scholar
  7. Gorfer M, Tarkka MT, Hanif M, Pardo AG, Laitainen E, Raudaskoski M (2001) Characterisation of small GTPases Cdc42 and Rac and the relationship between Cdc42 and actin cytoskeleton in vegetative and ectomycorrhizal hyphae of Suillus bovinus. Mol Plant Microbe Interact 14:135–144PubMedCrossRefGoogle Scholar
  8. Hampp R, Maier A (2004) Interaction between soil bacteria and ectomycorrhiza-forming fungi. In: Varma A, Abbot LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 197–210Google Scholar
  9. Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M (2005) Polarisome meets spitzenkörper: microscopy, genetics and genome converge. Eukaryot Cell 4:225–229PubMedCrossRefGoogle Scholar
  10. Heath IB (1990) The role of actin in tip growth of fungi. Int Rev Cytol 123:95–127Google Scholar
  11. Horio T, Oakley BR (2005) The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol Biol Cell 16:918–926PubMedCrossRefGoogle Scholar
  12. Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  13. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405PubMedCrossRefGoogle Scholar
  14. Kottke I, Oberwinkler F (1987) The cellular structure of the Hartig net: coenocytic and transfer cell-like organisation. Nord J Bot 7:85–95CrossRefGoogle Scholar
  15. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759Google Scholar
  16. Maier A (2003) Einfluss bakterieller Stoffwechselprodukte auf Wachstum und Proteom des Ektomykorrhizapilzes Amanita muscaria. Dissertation, University of TuebingenGoogle Scholar
  17. Maier A, Riedlinger J, Fiedler HP, Hampp R (2004) Actinomycetales bacteria from a spruce stand: characterisation and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture. Mycol Progress 3:129–136CrossRefGoogle Scholar
  18. Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387PubMedCrossRefGoogle Scholar
  19. Molina R, Palmer JG (1982) Isolation, maintenance and pure culture manipulation of ectomycorrhizal fungi. In: Schenk NC (ed) Methods and principles of mycorrhizal research. The American Phytopathological Society, St. Paul pp 115–129Google Scholar
  20. Nehls U, Wiese J, Guttenberger M, Hampp R (1998) Carbon allocation in ectomycorrhizas: identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol Plant Microbe Interact 11:167–176PubMedCrossRefGoogle Scholar
  21. Nehls U, Bock A, Ecke E, Hampp R (2001) Differential expression of the hexose-regulated fungal genes AmPAL and AmMst1 within Amanita/Populus ectomycorrhizas. New Phytol 150:583–589CrossRefGoogle Scholar
  22. Niini S, Raudaskoski M (1998) Growth patterns in non-mycorrhizal and mycorrhizal short roots of Pinus sylvestris. Symbiosis 25:101–114Google Scholar
  23. Poch O, Winsor B (1997) Who’s who among the Saccharomyces cerevisiae actin-related proteins? A classification and nomenclature proposal for a large family. Yeast 13:1053–1058PubMedCrossRefGoogle Scholar
  24. Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestris–Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:743–751CrossRefGoogle Scholar
  25. Rambaut A, Drummond A (2003) Tracer, version 1.0. Department of Zoology, University of Oxford, Oxford. http://evolve.zoo.ox.ac.uk/software.htmlGoogle Scholar
  26. Raudaskoski M, Rupeš I, Timonen S (1991) Immunofluorescence microscopy of the cytoskeleton in filamentous fungi after quick freezing and low temperature fixation. Exp Mycol 15:167–173CrossRefGoogle Scholar
  27. Raudaskoski M, Tarkka M, Niini S (2004) Mycorrhizal development and cytoskeleton. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 293–330Google Scholar
  28. Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler HP (2006) Auxofuran, a novel metabolite that stimulates the growth of fly agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 72:3550–3557PubMedCrossRefGoogle Scholar
  29. Runeberg P, Raudaskoski M, Virtanen I (1985) Cytoskeletal elements in the hyphae of the homobasidiomycete Schizophyllum commune visualized by indirect immunofluorescence and NBC-phallacidin. Eur J Cell Biol 41:25–32Google Scholar
  30. Rupeš I, Mao WZ, Åström H, Raudaskoski M (1995) Effects of nocodazole and brefeldin A on microtubule cytoskeleton and membrane organization in the homobasidiomycete Schizophyllum commune. Protoplasma 185:212–221CrossRefGoogle Scholar
  31. Salo V, Ninii SS, Virtanen I, Raudaskoski M (1989) Comparative immunocytochemistry of the cytoskeleton in filamentous fungi with dikaryotic and multinucleate hyphae. J Cell Sci 94:11–24Google Scholar
  32. Sambrook J, Fritsch EF, Maniatis TA (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  33. Sampson K, Heath IB (2005) The dynamic behaviour of microtubules and their contributions to hyphal tip growth in Aspergillus nidulans. Microbiology 151:1543–1555PubMedCrossRefGoogle Scholar
  34. Schaeffer C, Johann P, Nehls U, Hampp R (1996) Evidence for an up-regulation of the host and down-regulation of the fungal phosphofructokinase activity in ectomycorrhizas of Norway spruce and fly agaric. New Phytol 134:697–702CrossRefGoogle Scholar
  35. Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216PubMedCrossRefGoogle Scholar
  36. Schuchardt I, Assmann D, Thines E, Schuberth C, Steinberg G (2005) Myosin-V, kinesin-1, and kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol Biol Cell 16:5191–5201PubMedCrossRefGoogle Scholar
  37. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340CrossRefGoogle Scholar
  38. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  39. Tarkka MT, Vasara R, Gorfer M, Raudaskoski M (2000) Molecular characterisation of actin genes from homobasidiomycetes: two different actin genes from Schizophyllum commune and Suillus bovinus. Gene 251:27–35PubMedCrossRefGoogle Scholar
  40. Tarkka MT, Schrey SD, Nehls U (2006) The a-tubulin gene AmTuba1: a marker for rapid mycelial growth in the ectomycorrhizal basidiomycete Amanita muscaria. Curr Genet 49:294–301PubMedCrossRefGoogle Scholar
  41. Tinsley JH, Lee IH, Minke PF, Plamann M (1998) Analysis of actin and actin-related protein 3 (ARP3) gene expression following induction of hyphal tip formation and apolar growth in Neurospora. Mol Gen Genet 259:601–609PubMedCrossRefGoogle Scholar
  42. Torralba S, Raudaskoski M, Pedregosa AM, Laborda F (1998) Effect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology 144:45–53PubMedCrossRefGoogle Scholar
  43. Virag A, Griffiths AJ (2004) A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet Biol 41:213–25PubMedCrossRefGoogle Scholar
  44. Walther A, Wendland J (2004) Apical localisation of actin patches and vacuolar dynamics in Ashbya gossypii depend on the WASP homolog Wal1p. J Cell Sci 117:4947–4958PubMedCrossRefGoogle Scholar
  45. Weber M, Salo V, Uuskallio M, Raudaskoski M (2005) Ectopic expression of a constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genet Biol 42:624–637PubMedCrossRefGoogle Scholar
  46. Wright DP, Johansson T, Le Quere A, Söderström B, Tunlid A (2005) Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula) seedlings in soil microcosms. New Phytol 167:579–596PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Silvia D. Schrey
    • 1
  • Vanamo Salo
    • 2
  • Marjatta Raudaskoski
    • 3
  • Rüdiger Hampp
    • 1
  • Uwe Nehls
    • 1
  • Mika T. Tarkka
    • 1
    • 4
  1. 1.Faculty of Biology, Institute of Botany, Physiological Ecology of PlantsUniversity of TuebingenTuebingenGermany
  2. 2.Plant Biology, Department of Biological and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  3. 3.Department of BiologyUniversity of TurkuTurkuFinland
  4. 4.Department of Soil EcologyUFZ, Helmholtz-Centre for Environmental ResearchHalleGermany

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