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The Co-occurrence and Morphological Continuum Between Ericoid Mycorrhiza and Dark Septate Endophytes in Roots of Six European Rhododendron Species

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Abstract

Ericaceae associate with a wide spectrum of root mycobionts, but the most common are ascomycetous ericoid mycorrhizal fungi and dark septate endophytes (DSE), followed by basidiomycetous fungi and glomeracean arbuscular mycorrhizal fungi. We investigated distribution and morphological diversity of ericoid mycorrhizae (ErM), DSE associations, ectomycorrhizae (EcM) and arbuscular mycorrhizae (AM) in hair roots of six European native Rhododendron species and found that i) while EcM and AM were absent, ErM and DSE associations were simultaneously present in all screened plants; ii) their levels were negatively correlated, suggesting Ericaceae preference for certain root-fungus association in certain habitats; iii) the highest ErM colonization occurred at sites in southern and central Europe, while the highest DSE colonization was found in a subarctic site in northern Finland and in a subalpine site in the Carpathians, suggesting a latitudinal/altitudinal shift in Ericaceae root-fungus associations; iv) some mycelia could simultaneously form structures corresponding to ErM and DSE association, which occasionally resulted in a unique ectendomycorrhizal colonization comprising an intercellular parenchymatous net and intracellular hyphal coils. These results indicate frequent interactions between ErM fungi and DSE in roots of European rhododendrons and a morphological continuum between ErM and DSE associations. The new ectendomycorrhizal type deserves further investigation.

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References

  • 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 160:255–272

    Article  CAS  Google Scholar 

  • Bonfante-Fasolo P (1980) Occurrence of a basidiomycete in living cells of mycorrhizal hair roots of Calluna vulgaris. Trans Brit Mycol Soc 75:320–325

    Article  Google Scholar 

  • Bougoure DS, Cairney JWG (2005) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environm Microbiol 7:1743–1754

    Article  CAS  Google Scholar 

  • Bougoure DS, Parkin PI, Cairney JWG, Alexander IJ, Anderson IC (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Molec Ecol 16:4624–4636

    Article  CAS  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR Monograph 32, Canberra

  • Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that expoits harsh edaphic conditions. Eur J Soil Sci 54:735–740

    Article  Google Scholar 

  • Chambers SM, Curlevski 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 65:263–270

    Article  PubMed  CAS  Google Scholar 

  • Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi associated with central Himalayan rhododendrons. Forest Ecol Managem 207:315–324

    Article  Google Scholar 

  • Currah RS, Tsuneda A, Murakami S (1993a) Conidiogenesis in Oidiodendron periconioides and ultrastructure of ericoid mycorrhizas formed with Rhododendron brachycarpum. Canad J Bot 71:1481–1485

    Article  Google Scholar 

  • Currah RS, Tsuneda A, Murakami S (1993b) Morphology and ecology of Phialocephala fortinii in roots of Rhododendron brachycarpum. Canad J Bot 71:1639–1644

    Article  Google Scholar 

  • Dighton J, Coleman DC (1992) Phosphorus relations of roots and mycorrhizas of Rhododendron maximum L. in the southern Appalachians, North Carolina. Mycorrhiza 1:175–184

    Article  Google Scholar 

  • Dostálková A (1981) Rododendrony (Rhododendrons). Academia, Prague

    Google Scholar 

  • Douglas GC, Heslin MC, Reid C (1989) Isolation of Oidiodendron maius from Rhododendron and ultrastructural characterization of synthesized mycorrhizas. Canad J Bot 67:2206–2212

    Article  Google Scholar 

  • Duddridge JA, Read DJ (1982) Ultrastructural analysis of the development of mycorrhizas in Rhododendron ponticum. Canad J Bot 60:2345–2356

    Article  Google Scholar 

  • Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture. Canad J Bot 74:1071–1078

    Article  Google Scholar 

  • Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366

    Article  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4(1). Available at: http://palaeo-electronica.org/

  • Haselwandter K (1979) Mycorrhizal status of ericaceous plants in alpine and subalpine areas. New Phytol 83:427–431

    Article  Google Scholar 

  • Haselwandter K, Read DJ (1980) Fungal associations of roots of dominant and sub-dominant plants in high-alpine vegetation systems with special reference to mycorrhiza. Oecologia 45:57–62

    Article  Google Scholar 

  • Jones MD, Grenon F, Peat H, Fitzgerald M, Holt L, Philip LJ, Bradley R (2009) Differences in N-15 uptake amongst spruce seedlings colonized by three pioneer ectomycorrhizal fungi in the field. Fungal Ecol 2:110–120

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310

    Article  Google Scholar 

  • Koske RE, Gemma JN, Englander L (1990) Vesicular-arbuscular mycorrhizae in Hawaiian Ericales. Amer J Bot 77:64–68

    Article  Google Scholar 

  • Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: Molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • Leake JR, Shaw C, Read DJ (1989) The role of ericoid mycorrhizas in the ecology of ericaceous plants. Agric Ecosyst Environm 29:237–250

    Article  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  • Massicotte HB, Melville LH, Peterson RL (2005) Structural characteristics of root-fungal interactions for five ericaceous species in eastern Canada. Canad J Bot 83:1057–1064

    Article  Google Scholar 

  • Moore-Pankhurst S, Englander L (1981) A method for the synthesis of mycorrhizal association between Pezizella ericae and Rhododendron maximum seedlings growing in a defined medium. Mycologia 73:994–997

    Article  Google Scholar 

  • O’Dell TE, Massicotte HB, Trappe JM (1993) Root colonization of Lupinus latifolius Agardh. and Pinus concorta Dougl. by Phialocephala fortinii Wang & Wilcox. New Phytol 124:93–100

    Article  Google Scholar 

  • Perotto S, Girlanda M, Martino E (2002) Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Pl Soil 244:41–53

    Article  CAS  Google Scholar 

  • Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa

    Google Scholar 

  • Peterson RL, Wagg C, Pautler M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 86:445–456

    Article  CAS  Google Scholar 

  • Peterson TA, Mueller WC, Englander L (1980) Anatomy and ultrastructure of a Rhododendron root-fungus association. Canad J Bot 58:2421–2433

    Article  Google Scholar 

  • Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot (Oxford) 77:365–374

    Article  CAS  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions – the role of mutualisms. Biol Rev Cambridge Philos Soc 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Ruotsalainen AL, Väre H, Oksanen J, Tuomi J (2004) Root fungus colonization along an altitudinal gradient in North Norway. Arctic Antarct Alpine Res 36:239–243

    Article  Google Scholar 

  • Schulz B, Boyle C, Sieber T (eds) (2006) Microbial root endophytes. Springer Verlag, Berlin

    Google Scholar 

  • Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    Article  PubMed  CAS  Google Scholar 

  • Setaro S, Weiß M, Oberwinkler F, Kottke I (2006) Sebacinales form ectendomycorrhizas with Cavendishia nobilis, a member of the Andean clade of Ericaceae, in the mountain rain forest of southern Ecuador. New Phytol 169:355–365

    Article  PubMed  CAS  Google Scholar 

  • Seviour RJ, Willing RR, Chilvers GA (1973) Basidiocarps associated with ericoid mycorrhizas. New Phytol 72:381–385

    Article  Google Scholar 

  • Smith JE, Molina R, Perry DA (1995) Occurrence of ectomycorrhizas on ericaceous and coniferous seedlings grown in soils from the Oregon Coast Range. New Phytol 129:73–81

    Article  Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis. Ed. 3. Academic Press, London

  • Smith SE, Smith FA (1990) Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol 114:1–38

    Article  CAS  Google Scholar 

  • Stoyke G, Currah RS (1991) Endophytic fungi from the mycorrhizae of alpine ericoid plants. Canad J Bot 69:347–352

    Article  Google Scholar 

  • Usuki F, Narisawa K (2005) Formation of structures resembling ericoid mycorrhizas by the root endophytic fungus Heteroconium chaetospira within roots of Rhododendron obsutum var. kaempferi. Mycorrhiza 15:61–64

    Article  PubMed  Google Scholar 

  • Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184

    Article  PubMed  CAS  Google Scholar 

  • Usuki F, Junichi AP, Kakishima M (2003) Diversity of ericoid mycorrhizal fungi isolated from hair roots of Rhododendron obtusum var. kaempferi in a Japanese red pine forest. Mycoscience 44:97–102

    Article  Google Scholar 

  • Väre H, Vestberg M, Ohtonen R (1997) Shifts in mycorrhiza and microbial activity along an oroarctic altitudinal gradient in northern Fennoscandia. Arctic Alpine Res 29:93–104

    Article  Google Scholar 

  • Vohník M, Albrechtová J, Vosátka M (2005) The inoculation with Oidiodendron maius and Phialocephala fortinii alters phosphorus and nitrogen uptake, foliar C:N ratio and root biomass distribution in Rhododendron cv. Azurro. Symbiosis 40:87–96

    Google Scholar 

  • Vohník M, Fendrych M, Albrechtová J, Vosátka M (2007) Intracellular colonization of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiol (Prague) 52:407–414

    Article  Google Scholar 

  • Vohník M, Lukančič S, Bahor E, Regvar M, Vosátka M, Vodnik D (2003) Inoculation of Rhododendron cv. Belle-Heller with two strains of Phialocephala fortinii in two different substrates. Folia Geobot 38:191–200

    Article  Google Scholar 

  • Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol 164:7–10

    Article  Google Scholar 

  • Wurzburger N, Bledsoe CS (2001) Comparison of ericoid and ectomycorrhizal colonization and ectomycorrhizal morphotypes in mixed conifer and pygmy forests on the northern California coast. Canad J Bot 79:1202–1210

    Article  CAS  Google Scholar 

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Acknowledgement

This study is a part of the research project AV0Z60050516 of the Institute of Botany ASCR and SVV 261209/2010 of Charles University in Prague. MV wishes to thank M. Vosátka for general supervision, and D. Vodnik, S. Lukančič, M.-M. Kytoviita, T. Kojola, R. Partanen, J.A. Mejías and M. Fendrych for help with collecting the root samples. Inspiring comments of three anonymous reviewers are also acknowledged.

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  1. Department of Mycorrhizal Symbioses, Institute of Botany ASCR, Lesní 323, CZ-252 43, Průhonice, Czech Republic

    Martin Vohník & Jana Albrechtová

  2. Department of Experimental Plant Biology, Faculty of Science, Charles University, Viničná 5, CZ-128 44, Prague, Czech Republic

    Martin Vohník & Jana Albrechtová

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  1. Martin Vohník
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Correspondence to Martin Vohník.

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Vohník, M., Albrechtová, J. The Co-occurrence and Morphological Continuum Between Ericoid Mycorrhiza and Dark Septate Endophytes in Roots of Six European Rhododendron Species. Folia Geobot 46, 373–386 (2011). https://doi.org/10.1007/s12224-011-9098-5

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