Mycorrhiza

, Volume 26, Issue 5, pp 429–440 | Cite as

Is the root-colonizing endophyte Acremonium strictum an ericoid mycorrhizal fungus?

Original Article

Abstract

In previous investigations, we found that Acremonium strictum (strain DSM 100709) developed intracellular structures with similarity to mycelia of ericoid mycorrhizal fungi in the rhizodermal cells of flax plants and in hair roots of Rhododendron plantlets. A. strictum had also been isolated from roots of ericaceous salal plants and was described as an unusual ericoid mycorrhizal fungus (ERMF). As its mycorrhizal traits were doubted, we revised the hypothesis of a mycorrhizal nature of A. strictum. A successful synthesis of mycorrhiza in hair roots of inoculated ericaceous plants was a first step of evidence, followed by fluorescence microscopy with FUN®1 cell stain to observe the vitality of the host cells at the early infection stage. In inoculation trials with in vitro-raised mycorrhiza-free Rhododendron plants in axenic liquid culture and in greenhouse substrate culture, A. strictum was never observed in living hair root cells. As compared to the ERMF Oidiodendron maius and Rhizoscyphus ericae that invaded metabolically active host cells and established a symbiotic unit, A. strictum was only found in cells that were dead or in the process of dying and in the apoplast. In conclusion, A. strictum does not behave like a common ERMF—if it is one at all. A comparison of A. strictum isolates from ericaceous and non-ericaceous hosts could reveal further identity details to generalize or specify our findings on the symbiotic nature of A. strictum. At least, the staining method enables to discern between true mycorrhizal and other root endophytes—a tool for further studies.

Keywords

Ericoid mycorrhiza Root endophyte Cell vitality Microscopy Fluorescence test FUN®1 cell stain 

Notes

Acknowledgments

We thank Mrs. Natalie Roeder for competent technical assistance in preparing the experiments, and we gratefully appreciate the support by Mrs. Pamella Ogada to improve the English language of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13CrossRefGoogle Scholar
  2. Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272CrossRefGoogle Scholar
  3. Anjum T, Akram W (2014) First record of Acremonium wilt in tomato from Pakistan. Plant Dis Dis Notes 98:155CrossRefGoogle Scholar
  4. Bargmann C (1993) Zur Resistenzinduktion von Tomatenpflanzen (Lycopersicon lycopersicum L.) gegenüber Welkekrankheiten durch Acremonium kiliense Grütz. Dissertation, Universität Hannover, GermanyGoogle Scholar
  5. Berch SM, Allen TR, Berbee ML (2002) Molecular detection, community structure and phylogeny of ericoid mycorrhizal fungi. Plant Soil 244:55–66CrossRefGoogle Scholar
  6. Bougoure D, Parkin PI, Cairney JWG, Alexander IJ, Anderson IC (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Mol Ecol 16:4624–4636CrossRefPubMedGoogle Scholar
  7. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. Tansley review no 134. New Phytol 154:275–304CrossRefGoogle Scholar
  8. Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 281–298CrossRefGoogle Scholar
  9. Bruzone MC, Fontenla SB, Vohník M (2015) Is the prominent ericoid mycorrhizal fungus Rhizoscyphus ericae absent in the Southern Hemisphere’s Ericaceae? A case study on the diversity of root mycobionts in Gaultheria spp. from northwest Patagonia, Argentina. Mycorrhiza 25:25–40CrossRefPubMedGoogle Scholar
  10. Cairney JWG (2006) Ericoid mycorrhizal and other fungal root endophytes of epacrids (Ericaceae) in the southern hemisphere. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 247–260CrossRefGoogle Scholar
  11. Chalfoun NR, Grellet-Bournonville CF, Martínez-Zamora MG, Díaz-Perales A, Castagnaro AP, Díaz-Ricci JC (2013) Purification and characterization of AsES protein. A subtilisin secreted by Acremonium strictum is a novel plant defense elicitor. J Biol Chem 288:14098–14113. doi: 10.1074/jbc.M112.429423 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chambers SM, Williams PG, Seppelt RD, Cairney JWG (1999) Molecular identification of Hymenoscyphus sp. from rhizoids of the leafy liverwort Cephaloziella exiliflora in Australia and Antarctica. Mycol Res 103:286–288CrossRefGoogle Scholar
  13. Chambers SM, Curlevaki NJA, Cairney JWG (2008) Ericoid mycorrhizal fungi are common root inhabitants of non-Ericaceae plants in a south-eastern Australian sclerophyll forest. FEMS Microbiol Ecol 65:263–270CrossRefPubMedGoogle Scholar
  14. Chase AR, Munnecke DE (1980) Shasta daisy vascular wilt incited by Acremonium strictum. Phytopathology 70:834–838CrossRefGoogle Scholar
  15. Dugassa-Gobena D, Raps A, Vidal S (1998) Influence of fungal endophytes on allelochemicals of their host plants and the behavior of insects. Meded Fac Landbouw Biol Wetensch Univ Gent 63:333–337Google Scholar
  16. Gams W (1971) Cephalosporium-artige Schimmelpilze (Hyphomycetes). Gustav-Fischer-Verlag Stuttgart, GermanyGoogle Scholar
  17. Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88:369–383CrossRefGoogle Scholar
  18. Goswamy J, Pandey RK, Tewari JP, Goswamy BK (2008) Management of root knot nematode on tomato through application of fungal antagonists, Acremonium strictum and Trichoderma harzianum. J Environ Sci Health Part B 43:237–240CrossRefGoogle Scholar
  19. Grunewaldt-Stöcker G, von Alten H (2003) Plant health effects of Acremonium root endophytes compared to those of arbuscular mycorrhiza. In Abe J (ed) Roots: the dynamic interface between plants and the earth. Kluwer Academic Publishers, Nordrecht, NL: Developments in plant and soil sciences 101:445- 454Google Scholar
  20. Grunewaldt-Stöcker G, Riediger N, Dietrich C (2007) Suitability of GFP-transformed isolates of the fungal root endophyte Acremonium strictum W. Gams for studies on induced Fusarium-wilt resistance in flax. Plant Root 1:46–56. doi: 10.3117/plantroot.1.46 CrossRefGoogle Scholar
  21. Grunewaldt-Stöcker G, von den Berg C, Knopp J, von Alten H (2013) Interactions of ericoid mycorrhizal fungi and root pathogens in Rhododendron: in vitro tests with plantlets in sterile liquid culture. Plant Root 7:33–48. doi: 10.3117/plantroot.7.33 CrossRefGoogle Scholar
  22. Hazard C, Gosling P, Mitchell TD, Doohan FM, Bending GD (2014) Diversity of fungi associated with hair roots of ericaceous plants is affected by land use. FEMS Microbiol Ecol 87:586–600CrossRefPubMedGoogle Scholar
  23. Hua SST, Brandl M, Eng JG (2007) Fluorescent microscopic studies in the interactions of Pichia anomala and Aspergillus flavus. Bull OILB/SROP 6(1):165–169Google Scholar
  24. Jaber LR, Vidal S (2009) Interactions between an endophytic fungus, aphids and extrafloral nectaries: do endophytes induce extrafloral-mediated defences in Vicia faba? Funct Ecol 23:707–714CrossRefGoogle Scholar
  25. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  26. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310CrossRefGoogle Scholar
  27. Lenc L, Kwaśa H, Sadowski C, Grabowski A (2015) Microbiota in wheat roots, rhizosphere and soil in crops grown in organic and other production systems. J Phytopathol 163:245–263CrossRefGoogle Scholar
  28. Millard PJ, Roth BL, Thi HP, Yue ST, Haugland RP (1997) Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl Environ Microbiol 63:2897–2905PubMedPubMedCentralGoogle Scholar
  29. Monreal M, Berch SM, Berbee M (1999) Molecular diversity of ericoid mycorrhizal fungi. Can J Bot 77:1580–1594CrossRefGoogle Scholar
  30. Perotto S, Peretto R, Faccio A, Schubert A, Varma A, Bonfante P (1995) Ericoid mycorrhizal fungi: cellular and molecular bases of their interactions with the host plant. Can J Bot 73(Suppl):S557–S568CrossRefGoogle Scholar
  31. Peterson TA, Mueller WC, Englander L (1980) Anatomy and ultrastructure of a Rhododendron root-fungus association. Can J Bot 58:2421–2433CrossRefGoogle Scholar
  32. Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Press Ottawa, Ontario, Canada; NRC No. 46325, ISBN 0-660-19087-7Google Scholar
  33. Peterson RL, Wagg C, Pautler M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 86:445–456CrossRefGoogle Scholar
  34. Pina-Vaz C, Sansonetty F, Rodrigues AG, Costa-de-Oliveira S, Martinez-de-Oliveira J, Fonseca AF (2001) Susceptibility to fluconazole of Candida clinical isolates determined by FUN-1 staining with flow cytometry and epifluorescence microscopy. J Med Microbiol 50:375–382CrossRefPubMedGoogle Scholar
  35. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315CrossRefPubMedGoogle Scholar
  36. Rempe-Verspermann N, Grunewaldt-Stöcker G, von Alten H (2014) Histological characterization of browning and glassiness—quality deficiencies of white asparagus spears (Asparagus officinalis L.). J Pl Dis Protect 121:250–259CrossRefGoogle Scholar
  37. Rice AV, Currah RS (2006) Oidiodendron maius: saprobe in sphagnum peat, mutualist in ericaceous roots? In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil microbiology, vol 9. Springer, Berlin, pp 227–246CrossRefGoogle Scholar
  38. Rodriguez R, White J, Arnold AE, Redman R (2009) Fungal endophytes: diversity and ecological roles. New Phytol 182:314–330CrossRefPubMedGoogle Scholar
  39. Sharples JM, Chambers SM, Meharg AA, Cairney JWG (2000) Genetic diversity of root-associated fungal endophytes from Calluna vulgaris at contrasting field sites. New Phytol 148:153–162CrossRefGoogle Scholar
  40. Straker CJ (1996) Ericoid mycorrhiza: ecological and host specificity. Mycorrhiza 6:215–225CrossRefGoogle Scholar
  41. Summerbell RC, Gueidan C, Schroers H-J, deHoog GS, Starink M, Arocha Rosete Y, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68:139–162CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sun L, Pei K, Wang F, Ding Q, Bing Y, Gao B, Zheng Y, Liang Y, Ma K (2012) Different distribution patterns between putative ericoid mycorrhizal and other fungal assemblages in roots of Rhododendron decorum in the Southwest of China. PLoS ONE 7(11), e49867CrossRefPubMedPubMedCentralGoogle Scholar
  43. Tagne A, Neergaar E, Hansen HJ, The C (2002) Studies of host—pathogen interaction between maize and Acremonium strictum from Cameroon. Eur J Plant Pathol 108:93–102CrossRefGoogle Scholar
  44. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol Plant 125:393–404Google Scholar
  45. Vohník M, Albrechtová J (2011) The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six European Rhododendron species. Folia Geobotanica 46:373–386CrossRefGoogle Scholar
  46. Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata—the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563CrossRefGoogle Scholar
  47. Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  48. Wurzburger N, Higgins BP, Hendrick RL (2012) Ericoid mycorrhizal root fungi and their multicopper oxidases from a temperate forest shrub. Ecol Evol 2(65–792):65–79CrossRefPubMedPubMedCentralGoogle Scholar
  49. Xiao G (1994) The role of root-associated fungi in the dominance of Gaultheria shallon. Dissertation, University of British Columbia, Vancouver, CanadaGoogle Scholar
  50. Xiao G, Berch M (1996) Diversity and abundance of ericoid mycorrhizal fungi of Gaultheria shallon on forest clearcuts. Can J Bot 74:337–346CrossRefGoogle Scholar
  51. Xiao G, Berch M (1999) Organic nitrogen use by salal ericoid mycorrhizal fungi from northern Vancouver Island and its impacts on growth in vitro of Gaultheria shallon. Mycorrhiza 9:145–149CrossRefGoogle Scholar
  52. Yuan Z, Zhang C, Lin F (2010) Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. J Plant Growth Regul 29:116–126CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Gisela Grunewaldt-Stöcker
    • 1
  • Henning von Alten
    • 1
  1. 1.Institute of Horticultural Production Systems, Section PhytomedicineGottfried Wilhelm Leibniz Universität HannoverHannoverGermany

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