14 Genetic Diversity and Functional Aspects of Ericoid Mycorrhizal Fungi

Chapter
Part of the The Mycota book series (MYCOTA, volume 9)

Abstract

Ericoid mycorrhizal (ERM) fungi are a diverse assemblage of symbiotic fungi that features culturable ascomycetes in the Helotiales and Onygenales, but also so far unculturable basidiomycetes in the Sebacinales. They form a distinct endomycorrhizal association with some plant genera in the Ericaceae. ERM plants dominate in heathlands characterised by very poor nutrient status and considerable edaphic stress, and their success in these harsh environments is ascribed to the functional traits of their symbiotic fungi. ERM fungi are able to exploit recalcitrant organic substrates thanks to an arsenal of extracellular enzymes. They also display adaptive mechanisms of stress tolerance and are able to withstand high concentrations of toxic compounds such as heavy metals. ERM plants are also commonly found as understorey vegetation in woodland habitats, and molecular investigations on the genetic diversity of ERM fungi, together with cross-inoculation experiments under gnotobiotic conditions, indicate the potential networking ability of these fungi in mixed plant communities.

Keywords

Hair Root Mycorrhizal Fungus Mycorrhizal Root Dark Septate Endophyte Heavy Metal Tolerance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abbà S, Khouja HR, Martino E, Archer DB, Perotto S (2009) SOD1-Targeted gene disruption in the ericoid mycorrhizal fungus Oidiodendron maius reduces conidiation and the capacity for mycorrhization. Mol Plant Microbe Interact 22:1412–1421PubMedCrossRefGoogle Scholar
  2. Abbà S, Vallino M, Daghino S, Di Vietro L, Borriello R, Perotto S (2011) A PLAC8-containing protein from an endomycorrhizal fungus confers cadmium resistance to yeast cells by interacting with Mlh3p. Nucleic Acids Res 39:7548–7563PubMedCrossRefGoogle Scholar
  3. Abuarghub SM, Read DJ (1988) The biology of mycorrhizal in the Ericaceae. XI. The distribution of nitrogen in soil of a typical upland callunetum with special reference to the free amino-acids. New Phytol 108:425–431CrossRefGoogle Scholar
  4. Abuzinadah RA, Read DJ (1989) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. V. Nitrogen transfer in birch (Betula pendula) grown in association with mycorrhizal and non-mycorrhizal fungi. New Phytol 112:61–68CrossRefGoogle Scholar
  5. Adriaensen K, Vrålstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper adapted Suillus luteus, a symbiotic solution for pines colonising Cu mine spoil. Appl Environ Microbiol 11:7279–7284CrossRefGoogle Scholar
  6. Alberton O, Kuyper TW, Summerbell RC (2009) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470CrossRefGoogle Scholar
  7. 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
  8. Bajwa R, Read DJ (1986) Utilization of mineral and amino N sources by the ericoid mycorrhizal endophyte Hymenoscyphus ericae and by mycorrhizal and non-mycorrhizal seedlings of Vaccinium. Trans Br Mycol Soc 87:269–277CrossRefGoogle Scholar
  9. Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17:185–193PubMedCrossRefGoogle Scholar
  10. Barrett V, Dixon RK, Lemke PA (1990) Genetic transformation of a mycorrhizal fungus. Appl Microbiol Biotechnol 33:313–316CrossRefGoogle Scholar
  11. Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181PubMedCrossRefGoogle Scholar
  12. Bending GD, Read DJ (1996a) Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1595–1602CrossRefGoogle Scholar
  13. Bending GD, Read DJ (1996b) Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1603–1612CrossRefGoogle Scholar
  14. Bending GD, Read DJ (1997) Lignin and soluble-phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol Res 101:1348–1354CrossRefGoogle Scholar
  15. Berch SM, Allen TR, Berbee ML (2002) Molecular detection, community structure and phylogeny of ericoid mycorrhizal fungi. Plant Soil 244:55–66CrossRefGoogle Scholar
  16. Bergero R, Perotto S, Girlanda M, Vidano G, Luppi AM (2000) Ericoid mycorrhizal fungi are common root associates of a Mediterranean ectomycorrhizal plant (Quercus ilex). Mol Ecol 9:1639–1649PubMedCrossRefGoogle Scholar
  17. Bidartondo MI, Bruns TD, Weiss M, Sergio C, Read DJ (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proc Biol Sci R Soc 270:835–842CrossRefGoogle Scholar
  18. Bills SN, Richter DL, Podila GK (1995) Genetic transformation of the ectomycorrhizal fungus Paxillus involutus by particle bombardment. Mycol Res 99:557–561CrossRefGoogle Scholar
  19. Bills SN, Podila GK, Hiremath S (1999) Genetic engineering of an ectomycorrhizal fungus Laccaria bicolor for use as a biological control agent. Mycologia 91:237–242CrossRefGoogle Scholar
  20. Blaudez D, Chalot M (2011) Characterization of the ER-located zinc transporter ZnT1 and identification of a vesicular zinc storage compartment in Hebeloma cylindrosporum. Fungal Genet Biol 48:496–503PubMedCrossRefGoogle Scholar
  21. Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117PubMedGoogle Scholar
  22. Bolchi A, Ruotolo R, Marchini G, Vurro E, Sanità di Toppi L, Kohler A, Tisserant E, Martin F, Ottonello S (2011) Genome-wide inventory of metal homeostasis-related gene products including a functional phytochelatin synthase in the hypogeous mycorrhizal fungus Tuber melanosporum. Fungal Genet Biol 48:573–584PubMedCrossRefGoogle Scholar
  23. Bonfante-Fasolo P (1980) Occurrence of a basidiomycetes in living cells of mycorrhizal hair roots of Calluna vulgaris. Trans Br Mycol Soc 75:320–325CrossRefGoogle Scholar
  24. Bonfante-Fasolo P, Gianinazzi-Pearson V (1979) Ultrastructural aspects of endomycorrhiza in the Ericaceae. I. Naturally infected hair roots of Calluna vulgaris L. Hull. New Phytol 83:739–744CrossRefGoogle Scholar
  25. Bougoure DS, Cairney JWG (2005a) Assemblages of ericoid mycorrhizal and other root-associated fungi from Epacris pulchella (Ericaceae) as determined by culturing and direct DNA extraction from roots. Environ Microbiol 7:819–827PubMedCrossRefGoogle Scholar
  26. Bougoure DS, Cairney JWG (2005b) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ Microbiol 7:1743–1754PubMedCrossRefGoogle Scholar
  27. Bougoure DS, Cairney JWG (2006) Chitinolytic activities of ericoid mycorrhizal and other root-associated fungi from Epacris pulchella (Ericaceae). Mycol Res 110:328–334PubMedCrossRefGoogle Scholar
  28. Bougoure DS, Parkin PI, Cairney JWG, Alexander IJ, Anderson IC (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Mol Ecol 16:4624–4636PubMedCrossRefGoogle Scholar
  29. Bradley R, Burt AJ, Read DJ (1981) Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature 292:335–337CrossRefGoogle Scholar
  30. Bradley R, Burt AJ, Read DJ (1982) The biology of mycorrhiza in the Ericaceae VIII. The role of the mycorrhizal infection in heavy metal resistance. New Phytol 91:197–209CrossRefGoogle Scholar
  31. Braun-Lüllemann A, Hüttermann A, Majcherczyk A (1999) Screening of ectomycorrhizal fungi for degradation of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 53:127–132CrossRefGoogle Scholar
  32. Brown SH, Yarden O, Gollop N, Chen S, Zveibil A, Belausov E, Freeman S (2008) Differential protein expression in Colletotrichum acutatum: changes associated with reactive oxygen species and nitrogen starvation implicated in pathogenicity on strawberry. Mol Plant Pathol 9:171–190PubMedCrossRefGoogle Scholar
  33. Burke RM, Cairney JWG (1997a) Carbohydrolase production by the ericoid mycorrhizal fungus Hymenoscyphus ericae under solid state fermentation conditions. Mycol Res 101:1135–1139CrossRefGoogle Scholar
  34. Burke RM, Cairney JWG (1997b) Purification and characterisation of a β-1,4-endoxylanase from the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol 135:345–352CrossRefGoogle Scholar
  35. Burke RM, Cairney JWG (1998) Carbohydrate oxidases in ericoid and ectomycorrhizal fungi: a possible source of Fenton radicals during the degradation of lignocellulose. New Phytol 139:637–645CrossRefGoogle Scholar
  36. Burke RM, Cairney JWG (2002) Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 12:105–116PubMedCrossRefGoogle Scholar
  37. Cairney JWG, Burke RM (1998) Extracellular enzyme activities of the ericoid mycorrhizal endophyte Hymenoscyphus ericae (Read) Korf & Kernan: their likely roles in decomposition of dead plant tissue in soil. Plant Soil 205:181–192CrossRefGoogle Scholar
  38. Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740CrossRefGoogle Scholar
  39. Cairney JWG, Sawyer NA, Sharples JM, Meharg AA (2000) Intraspecific variation in nitrogen source utilisation by isolates of the ericoid mycorrhizal fungus Hymenoscyphus Ericae (Read) Korf and Kernan. Soil Biol Biotechnol 32:1319–1322CrossRefGoogle Scholar
  40. Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44PubMedCrossRefGoogle Scholar
  41. Chambers SM, Williams PG, Seppelt RD, Cairney JWG (1999) Molecular identification of Hymenoscyphus sp. From rhizoids of the leafy liverwort Cephaloziella exiliflora (Tayl.) Steph. In Australia and Antarctica. Mycol Res 103:286–288CrossRefGoogle Scholar
  42. Chambers SM, Liu G, Cairney JWG (2000) ITS rDNA sequence comparison of ericoid mycorrhizal endophytes from Woollsia pungens. Mycol Res 104:168–174CrossRefGoogle Scholar
  43. Chambers SM, Curlevski NJ, Cairney JWG (2008) Ericoid mycorrhizal fungi are common root inhabitants of non-Ericaceae plants in a south-eastern Australian sclerophyll forest. FEMS Microbiol Ecol 65:263–270PubMedCrossRefGoogle Scholar
  44. Chen A, Chambers SM, Cairney JWG (1999) Utilisation of organic nitrogen and phosphorus sources by mycorrhizal endophytes of Woollsia pungens (Cav.) F. Muell. (Epacridaceae). Mycorrhiza 8:181–187CrossRefGoogle Scholar
  45. Chongpraditnun P, Mori S, Chino M (1992) Excess copper induces a cytosolic Cu, Zn-superoxide dismutase in soybean root. Plant Cell Physiol 33:239–244Google Scholar
  46. Colpaert JV, Muller LAH, Lambaerts M, Adriaensen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of suilloid fungi. New Phytol 162:549–559CrossRefGoogle Scholar
  47. Colpaert JV, Wevers JHL, Krznaric E, Adriaensen K (2011) How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Ann For Sci 68:17–24CrossRefGoogle Scholar
  48. Combier JP, 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 220:141–148PubMedCrossRefGoogle Scholar
  49. Combier JP, Melayah D, Raffier C, Pepin R, Marmeisse R, Gay G (2004) Nonmycorrhizal (Myc-) mutants of Hebeloma cylindrosporum obtained through insertional mutagenesis. Mol Plant Microbe Interact 17:1029–1038PubMedCrossRefGoogle Scholar
  50. Cosgrove DJ (1967) Metabolism of organic phosphates in soil. In: McLaren AD, Peterson GH (eds) Soil biochemistry. Dekker, New York, pp 216–228Google Scholar
  51. Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417PubMedCrossRefGoogle Scholar
  52. Couture M, Fortin JA, Dalpé Y (1983) Oidiodendron griseum Robak: an endophyte of ericoid mycorrhiza in Vaccinium spp. New Phytol 95:375–380CrossRefGoogle Scholar
  53. Cox GM, Harrison TS, McDade HC, Taborda CP, Heinrich G, Casadevall A, Perfect JR (2003) Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 71:173–180PubMedCrossRefGoogle Scholar
  54. Curlevski NJA, Chambers SM, Anderson IC, Cairney JWG (2009) Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiol Ecol 67:411–420PubMedCrossRefGoogle Scholar
  55. Dalpé Y (1986) Axenic synthesis of ericoid mycorrhiza in Vaccinium angustifolium Ait. by Oidiodendron species. New Phytol 103:391–396CrossRefGoogle Scholar
  56. Dalpé Y (1989) Ericoid mycorrhizal fungi in the Myxotrichaceae and Gymnoascaceae. New Phytol 113:523–527CrossRefGoogle Scholar
  57. Dalpé Y, Litten W, Sigler L (1989) Scytalidium vaccinii sp. nov., an ericoid endophyte of Vaccinium angustifolium roots. Mycotaxon 35:371–377Google Scholar
  58. Denny HJ, Ridge I (1995) Fungal slime and its role in the mycorrhiza amelioration of zinc toxicity to higher plants. New Phytol 130:251–257CrossRefGoogle Scholar
  59. Devevre O, Garbaye J, Botton B (1996) Release of complexing organic acids by rhizosphere fungi as a factor in Norway Spruce yellowing in acidic soils. Mycol Res 100:1367–1374CrossRefGoogle Scholar
  60. Dighton J, Thomas ED, Latter PM (1987) Interactions between tree roots, mycorrhizas, a saprotrophic fungus and the decomposition of organic substrates in a microcosm. Biol Fertil Soils 4:145–150CrossRefGoogle Scholar
  61. Dos Santos Utmazian MN, Schweiger P, Sommer P, Gorfer M, Strauss J (2007) Influence of Cadophora finlandica and other microbial treatments on cadmium and zinc uptake in willows grown on polluted soil. Plant Soil Environ 53:158–166Google Scholar
  62. Duckett JG, Read DJ (1995) Ericoid mycorrhizas and rhizoid-ascomycete associations in liverworts share the same mycobiont: isolation of the partners and resynthesis of the associations in vitro. New Phytol 129:439–447CrossRefGoogle Scholar
  63. Duddridge J, Read DJ (1982) An ultrastructural analysis of the development of mycorrhizas in Rhododendron pontium. Can J Bot 60:2345–2356CrossRefGoogle Scholar
  64. Eaton GK, Ayres MP (2002) Plasticity and constraint in growth and protein mineralization of ectomycorrhizal fungi under simulated nitrogen deposition. Mycologia 94:921–932PubMedCrossRefGoogle Scholar
  65. Egger KN (2006) The surprising diversity of ascomycetous mycorrhizas. New Phytol 170:421–423PubMedCrossRefGoogle Scholar
  66. Egger KN, Sigler L (1993) Relatedness of the ericoid endophytes Scytalidium vaccinii and Hymenoscyphus ericae inferred from analysis of ribosomal DNA. Mycologia 85:219–230CrossRefGoogle Scholar
  67. Englander L, Hull RJ (1980) Reciprocal transfer of nutrients between ericaceous plants and a Clavaria sp. New Phytol 84:661–667CrossRefGoogle Scholar
  68. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126PubMedCrossRefGoogle Scholar
  69. Fishel R, Kolodner RD (1995) Identification of mismatch repair genes and their role in the development of cancer. Curr Opin Genet Dev 5:382–395PubMedCrossRefGoogle Scholar
  70. Fomina M, Charnock JM, Hillier S, Alvarez R, Gadd GM (2007) Fungal transformations of uranium oxides. Environ Microbiol 9:1696–1710PubMedCrossRefGoogle Scholar
  71. Forbes PJ, Millian S, Hooker JE, Harrier LA (1998) Transformation of the arbuscolar mycorrhiza Gigaspora rosea by particle bombardment. Mycol Res 102:497–501CrossRefGoogle Scholar
  72. Fridovich I (1995) Superoxide radicals and superoxide dismutase. Annu Rev Biochem 5:321–324Google Scholar
  73. Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60CrossRefGoogle Scholar
  74. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643PubMedCrossRefGoogle Scholar
  75. Genney DR, Alexander IJ, Hartley SE (2000) Exclusion of grass roots from soil organic layers by Calluna: the role of ericoid mycorrhizas. J Exp Bot 51:1117–1125PubMedCrossRefGoogle Scholar
  76. Gibson BR, Mitchell DT (2004) Nutritional influences on the solubilization of metal phosphate by ericoid mycorrhizal fungi. Mycol Res 108:947–954PubMedCrossRefGoogle Scholar
  77. Gibson BR, Mitchell DT (2005) Phosphatases of ericoid mycorrhizal fungi: kinetic properties and the effect of copper on activity. Mycol Res 109:478–486PubMedCrossRefGoogle Scholar
  78. Girlanda M, Selosse MA, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F, Cozzolino S, Perotto S (2006) Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Mol Ecol 15:491–504PubMedCrossRefGoogle Scholar
  79. González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335PubMedCrossRefGoogle Scholar
  80. Gorfer M, Persak H, Berger H, Brynda S, Bandian D, Strauss J (2009) Identification of heavy metal regulated genes from the root associated ascomycete Cadophora finlandica using a genomic microarray. Mycol Res 113:1377–1388PubMedCrossRefGoogle Scholar
  81. Grelet GA, Meharg AA, Alexander IJ (2005) Carbon availability affects nitrogen source utilisation by Hymenoscyphus ericae. Mycol Res 109:469–477PubMedCrossRefGoogle Scholar
  82. Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009a) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366CrossRefGoogle Scholar
  83. Grelet GA, Meharg AA, Duff EI, Anderson IC, Alexander IJ (2009b) Small genetic differences between ericoid mycorrhizal fungi affect nitrogen uptake by Vaccinium. New Phytol 181:708–718PubMedCrossRefGoogle Scholar
  84. Grelet GA, Johnson D, Vrålstad T, Alexander IJ, Anderson IC (2010) New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytol 188:210–222PubMedCrossRefGoogle Scholar
  85. Griffiths RP, Caldwell BA (1992) Mycorrhizal mat communities in forest soils. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 98–105Google Scholar
  86. Grimaldi B, de Raaf MA, Filetici P, Ottonello S, Ballario P (2005) Agrobacterium-mediated gene transfer and enhanced green fluorescent protein visualization in the mycorrhizal ascomycete Tuber borchii: a first step towards truffle genetics. Curr Genet 48:69–74PubMedCrossRefGoogle Scholar
  87. Guelfi A, Azevedo RA, Lea PJ, Molina SMG (2003) Growth inhibition of the filamentous fungus Aspergillus nidulans by cadmium: an antioxidant enzyme approach. J Gen Appl Microbiol 49:63–73PubMedCrossRefGoogle Scholar
  88. Gunther H, Perner B, Gramss G (1998) Activities of phenol oxidizing enzymes of ectomycorrhizal fungi in axenic culture and in symbiosis with Scots pine (Pinus sylvestris L.). J Basic Microbiol 38:197–206CrossRefGoogle Scholar
  89. Hambleton S, Currah RS (1997) Fungal endophytes from the roots of alpine and boreal Ericaceae. Can J Bot 75:1570–1581CrossRefGoogle Scholar
  90. Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27CrossRefGoogle Scholar
  91. Hambleton S, Egger KN, Currah RS (1998) The genus Oidiodendron: species delimitation and phylogenetic relationships based on nuclear ribosomal DNA analysis. Mycologia 90:854–868CrossRefGoogle Scholar
  92. Hanif M, Pardo A, Gorfer M, Raudaskoski M (2002) T-DNA transfer and integration in the ectomycorrhizal fungus Suillus bovinus using hygromycin B as a selectable marker. Curr Genet 41:183–188PubMedCrossRefGoogle Scholar
  93. Hartwig A (1995) Current aspects in metal genotoxicity. Biometals 8:3–11PubMedCrossRefGoogle Scholar
  94. Helber N, Requena N (2008) Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscolar mycorrhizal fungus Glomus intraradices. New Phytol 177:537–548PubMedGoogle Scholar
  95. Heupel S, Roser B, Kuhn H, Lebrun MH, Villalba F, Requena N (2010) Erl1, a novel Era-Like GTPase from Magnaporthe oryzae, is required for full root virulence and is conserved in the mutualistic symbiont Glomus intraradices. Mol Plant Microbe Interact 23:67–81PubMedCrossRefGoogle Scholar
  96. Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–569PubMedCrossRefGoogle Scholar
  97. Hutchison LJ (1990) Studies on the systematics of ectomycorrhizal fungi in axenic culture. III. Patterns of polyphenol oxidase activity. Mycologia 82:424–435CrossRefGoogle Scholar
  98. Hutton BJ, Dixon KW, Sivasithamparam K (1994) Ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytol 127:557–566CrossRefGoogle Scholar
  99. Hwang CS, Rhie GE, Oh JH, Huh WK, Yim HS, Kang SO (2002) Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148:3705–3713PubMedGoogle Scholar
  100. Jacob C, Courbot M, Brun A, Steinman HM, Jacquot J-P, Botton B, Chalot M (2001) Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. Eur J Biochem 268:3223–3232PubMedCrossRefGoogle Scholar
  101. Jalal MAF, Read DJ (1983) The organic acid composition of Calluna heathland soil with special reference to phyto- and fungi-toxicity. I. Isolation and identification of organic acids. Plant Soil 70:257–272CrossRefGoogle Scholar
  102. Janssens TKS, Mariën J, Cenijn P, Legler J, van Straalen NM, Dick RD (2007) Recombinational micro-evolution of functionally different metallothionein promoter alleles from Orchesella cincta. BMC Evol Biol 7:88–107PubMedCrossRefGoogle Scholar
  103. Jin YH, Clark AB, Slebos RJC, Al-Refai H, Taylor JA, Kunkel TA, Resnick MA, Gordenin DA (2003) Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat Genet 34:326–329PubMedCrossRefGoogle Scholar
  104. Jongmans AG, van Breemen N, Lundström US, van Hees PAW, Finlay RD, Srinivasan M, Unestam T, Giesler R, Melkerud P-A, Olsson M (1997) Rock-eating fungi. Nature 389:682–683CrossRefGoogle Scholar
  105. Jumpponen A (2001) Dark septate endophytes – are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  106. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310CrossRefGoogle Scholar
  107. Kemppainen M, Circosta A, Tagu D, Martin F, Pardo A (2005) Agrobacterium-mediated transformation of the ectomycorrhizal symbiont Laccaria bicolor S238N. Mycorrhiza 16:19–22PubMedCrossRefGoogle Scholar
  108. Kemppainen M, Duplessis S, Martin F, Pardo AG (2009) RNA silencing in the model mycorrhizal fungus Laccaria bicolor: gene knock-down of nitrate reductase results in inhibition of symbiosis with Populus. Environ Microbiol 11:1878–1896PubMedCrossRefGoogle Scholar
  109. Kerley SJ, Read DJ (1995) The biology of mycorrhiza in the Ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host plant. New Phytol 131:369–375CrossRefGoogle Scholar
  110. Kerley SJ, Read DJ (1997) The biology of mycorrhiza in the Ericaceae. XIX. Fungal mycelium as a nitrogen source for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host plants. New Phytol 136:691–701CrossRefGoogle Scholar
  111. Kernan MJ, Finocchio F (1983) A new discomycetes associated with the roots of Monotropa uniflora (Ericaceae). Mycologia 75:916–920CrossRefGoogle Scholar
  112. Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383CrossRefGoogle Scholar
  113. Kjøller R, Olsrud M, Michelsen A (2010) Co-existing ericaceous plant species in a subarctic mire community share fungal root endophytes. Fungal Ecol 3:205–214CrossRefGoogle Scholar
  114. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209PubMedCrossRefGoogle Scholar
  115. Kosola KR, Workmaster BAA, Spada PA (2007) Inoculation of cranberry (Vaccinium macrocarpon) with the ericoid mycorrhizal fungus Rhizoscyphus ericae increases nitrate influx. New Phytol 176:184–196PubMedCrossRefGoogle Scholar
  116. 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 68:335–423CrossRefGoogle Scholar
  117. Krznaric E, Wevers JHL, Cloquet C, Vangronsveld J, Vanhaecke F, Colpaert JV (2009) Zn pollution counteracts Cd toxicity in metal-tolerant ectomycorrhizal fungi and their host plant, Pinus sylvestris. Environ Microbiol 12:2133–2141PubMedGoogle Scholar
  118. Lacourt I, Girlanda M, Perotto S, Del Pero M, Zuccon D, Luppi AM (2002) Nuclear ribosomal sequence analysis of Oidiodendron: towards a redefinition of ecologically relevant species. New Phytol 149:565–576CrossRefGoogle Scholar
  119. Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67PubMedCrossRefGoogle Scholar
  120. Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330PubMedCrossRefGoogle Scholar
  121. Leake JR, Miles W (1996) Phosphodiesters as mycorrhizal P sources. I. Phosphodiesterase production and the utilization of DNA as a phosphorus source by the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol 132:435–443CrossRefGoogle Scholar
  122. Leake JR, Read DJ (1989) The effect of phenolic compounds on nitrogen mobilisation by ericoid mycorrhizal systems. Agric Ecosyst Environ 29:225–236CrossRefGoogle Scholar
  123. Leake JR, Read DJ (1990a) Chitin as a nitrogen source for mycorrhizal fungi. Mycol Res 94:993–995CrossRefGoogle Scholar
  124. Leake JR, Read DJ (1990b) Proteinase activity in mycorrhizal fungi. I. The effect of extracellular pH on the production and activity of proteinase by ericoid endophytes from soils of contrasted pH. New Phytol 115:243–250CrossRefGoogle Scholar
  125. Leake JR, Read DJ (1990c) Proteinase activity in mycorrhizal fungi. II. The effects of mineral and organic nitrogen sources on induction of extracellular proteinase in Hymenoscyphus ericae (Read) Korf and Kernan. New Phytol 116:123–128CrossRefGoogle Scholar
  126. Leake JR, Read DJ (1991) Experiments with ericoid mycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology, vol 23. Elsevier, Oxford, pp 435–459Google Scholar
  127. Leake JR, Read DJ (1997) Mycorrhizal fungi in terrestrial habitats. In: Wicklow D, Söderström B (eds) The mycota IV: environmental and microbial relationships. Springer, Berlin Heidelberg New York, pp 281–301Google Scholar
  128. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153CrossRefGoogle Scholar
  129. Liu G, Chambers SM, Cairney JWG (1998) Molecular diversity of ericoid mycorrhizal endophytes isolated from Woollsia pungens. New Phytol 140:145–153CrossRefGoogle Scholar
  130. Lundström US, Van Breemen N, Bain D (2000) The podzolization process. A review. Geoderma 94:91–107CrossRefGoogle Scholar
  131. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189CrossRefGoogle Scholar
  132. Marmeisse R, Gay G, Debaud JC, Casselton LA (1992) Genetic transformation of the symbiotic basidiomycete fungus Hebeloma cylindrosporum. Curr Genet 22:41–45PubMedCrossRefGoogle Scholar
  133. Martin F, Selosse M-A (2008) The Laccaria genome: a symbiont blueprint decoded. New Phytol 180:296–310PubMedCrossRefGoogle Scholar
  134. Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92PubMedCrossRefGoogle Scholar
  135. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038PubMedCrossRefGoogle Scholar
  136. Martino E, Turnau K, Girlanda M, Bonfante P, Perotto S (2000a) Ericoid mycorrhizal fungi from heavy metal polluted soils: their identification and growth in the presence of zinc ions. Mycol Res 104:338–344CrossRefGoogle Scholar
  137. Martino E, Coisson JD, Lacourt I, Favaron F, Bonfante P, Perotto S (2000b) Influence of heavy metals on production and activity of pectinolytic enzymes in ericoid mycorrhizal fungi. Mycol Res 104:825–833CrossRefGoogle Scholar
  138. Martino E, Franco B, Piccoli G, Stocchi V, Perotto S (2002) Influence of zinc ions on protein secretion in a heavy metal tolerant strain of the ericoid mycorrhizal fungus Oidiodendron maius. Mol Cell Biochem 231:179–185PubMedCrossRefGoogle Scholar
  139. Martino E, Perotto S, Parsons R, Gadd GM (2003) Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biotechnol 35:133–141CrossRefGoogle Scholar
  140. Martino E, Murat C, Vallino M, Bena A, Perotto S, Spanu P (2007) Imaging mycorrhizal fungal transformants that express EGFP during ericoid endosymbiosis. Curr Genet 52:65–75PubMedCrossRefGoogle Scholar
  141. Massicotte HB, Melville LH, Peterson RL (2005) Structural characteristics of root-fungal interactions for five ericaceous species in Eastern Canada. Can J Bot 83:1057–1064CrossRefGoogle Scholar
  142. McKendrick SL, Leake JR, Read DJ (2000) Symbiotic germination and development of myco-heterotrophic plants in nature: transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytol 145:539–548CrossRefGoogle Scholar
  143. McLean CB, Cunnington JH, Lawrie AC (1999) Molecular diversity within and between ericoid endophytes from the Ericaceae and Epacridaceae. New Phytol 144:351–358CrossRefGoogle Scholar
  144. Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112CrossRefGoogle Scholar
  145. Midgley DJ, Chambers SM, Cairney JWG (2004a) Inorganic and organic substrates as sources of nitrogen and phosphorus for multiple genotypes of two ericoid mycorrhizal fungal taxa from Woollsia pungens Cav. (Muell.) and Leucopogon parviflorus (Andr.) Lindl. (Ericaceae). Austral J Bot 52:63–71CrossRefGoogle Scholar
  146. Midgley DJ, Chambers SM, Cairney JWG (2004b) Utilisation of carbon substrates by multiple genotypes of ericoid mycorrhizal fungal endophytes from eastern Australian Ericaceae. Mycorrhiza 14:245–251PubMedCrossRefGoogle Scholar
  147. Midgley DJ, Chambers SM, Cairney JWG (2004c) Distribution of ericoid mycorrhizal endophytes and root-associated fungi in neighbouring Ericaceae plants in the field. Plant Soil 259:137–151CrossRefGoogle Scholar
  148. Midgley DJ, Jordan LA, Saleeba JA, McGee PA (2006) Utilisation of carbon substrates by orchid and ericoid mycorrhizal fungi from Australian dry sclerophyll forests. Mycorrhiza 16:175–182PubMedCrossRefGoogle Scholar
  149. Mitchell DT, Gibson BR (2006) Ericoid mycorrhizal association: ability to adapt to a broad range of habitats. Mycologist 20:2–9CrossRefGoogle Scholar
  150. Mitchell DT, Read DJ (1981) Utilization of inorganic and organic phosphates by the mycorrhizal endophytes of Vaccinium macrocarpon and Rhododendron ponticum. Trans Br Mycol Soc 76:255–260CrossRefGoogle Scholar
  151. Mitchell DT, Sweeney M, Kennedy A (1992) Chitin degradation by Hymenoscyphus ericae and the influence of H. ericae on the growth of ectomycorrhizal fungi. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 246–251Google Scholar
  152. Monreal M, Berch SM, Berbee M (1999) Molecular diversity of ericoid mycorrhizal fungi. Can J Bot 77:1580–1594CrossRefGoogle Scholar
  153. Morel M, Kohler A, Martin F, Gelhaye E, Rouhier N (2008) Comparison of the thiol-dependent antioxidant systems in the ectomycorrhizal Laccaria bicolor and the saprotrophic Phanerochaete chrysosporium. New Phytol 180:391–407PubMedCrossRefGoogle Scholar
  154. Murat C, Zampieri E, Vallino M, Daghino S, Perotto S, Bonfante P (2011) Genomic suppression subtractive hybridization as a tool to identify differences in mycorrhizal fungal genomes. FEMS Microbiol Lett 318:115–120PubMedCrossRefGoogle Scholar
  155. Myers MD, Leake JR (1996) Phosphodiesters as mycorrhizal P sources. II. Ericoid mycorrhiza and the utilization of nuclei as a phosphorus source by Vaccinium macrocarpon. New Phytol 132:445–451CrossRefGoogle Scholar
  156. Nehls U, Kleber R, Wiese J, Hampp R (1999) Isolation and characterization of a general amino acid permease from the ectomycorrhizal fungus Amanita muscaria. New Phytol 144:343–349CrossRefGoogle Scholar
  157. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20CrossRefGoogle Scholar
  158. Nikolaou E, Stumpf M, Quinn J, Stansfield I, Brown AJP (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9:44–53PubMedCrossRefGoogle Scholar
  159. Ohtaka N, Narisawa K (2008) Molecular characterization and endophytic nature of the root-associated fungus Meliniomyces variabilis (LtVB3). J Gen Plant Pathol 74:24–31CrossRefGoogle Scholar
  160. Pardo AG, Hanif M, Raudaskoski M, Gorfer M (2002) Genetic transformation of ectomycorrhizal fungi mediated by Agrobacterium tumefaciens. Mycol Res 106:132–137CrossRefGoogle Scholar
  161. Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421PubMedCrossRefGoogle Scholar
  162. Pearson V, Read DJ (1973a) The biology of mycorrhizae in the Ericaceae. I. The isolation of the endophyte and synthesis of mycorrhizas in aseptic culture. New Phytol 72:371–379CrossRefGoogle Scholar
  163. Pearson V, Read DJ (1973b) Biology of mycorrhiza in Ericaceae. II. Transport of carbon and phosphorus by endophyte and mycorrhiza. New Phytol 72:1325–1331CrossRefGoogle Scholar
  164. Perotto R, Bettini V, Bonfante P (1993) Evidence of two polygalacturonases produced by a mycorrhizal ericoid fungus during saprotrophic growth. FEMS Microbiol Lett 114:85–92CrossRefGoogle Scholar
  165. Perotto S, Actis Perino E, Perugini J, Bonfante P (1996) Molecular diversity of fungi from ericoid mycorrhizal roots. Mol Ecol 5:123–131CrossRefGoogle Scholar
  166. Perotto S, Coisson JD, Perugini I, Cometti V, Bonfante P (1997) Production of pectin-degrading enzymes by ericoid mycorrhizal fungi. New Phytol 135:151–162CrossRefGoogle Scholar
  167. Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot 82:1074–1088CrossRefGoogle Scholar
  168. Peterson TAW, Mueller C, Englander L (1980) Anatomy and ultrastructure of a Rhododendron root–fungus association. Can J Bot 58:2421–2433CrossRefGoogle Scholar
  169. Piercey MM, Thormann MN, Currah RS (2002) Saprotrophic characteristics of three fungal taxa from ericalean roots and their association with the roots of Rhododendron groenlandicum and Picea mariana in culture. Mycorrhiza 12:175–180PubMedCrossRefGoogle Scholar
  170. Ramesh G, Podila GK, Gay G, Marmeisse R, Reddy MS (2009) Different patterns of regulation for the copper and cadmium metallothioneins of the ectomycorrhizal fungus Hebeloma cylindrosporum. Appl Environ Microbiol 75:2266–2274PubMedCrossRefGoogle Scholar
  171. Rasmussen HN, Rasmussen FN (2009) Orchid mycorrhiza: implications of a mycophagous life style. Oikos 118:334–345CrossRefGoogle Scholar
  172. Read DJ (1974) Pezizella ericae sp. nov., the perfect state of a typical mycorrhizal endophyte of the Ericaceae. Trans Br Mycol Soc 63:381–383CrossRefGoogle Scholar
  173. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391CrossRefGoogle Scholar
  174. Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374CrossRefGoogle Scholar
  175. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  176. Read DJ, Leake JR, Langdale AR (1989) The nitrogen nutrition of mycorrhizal fungi and their host plants. In: Boddy L, Marchant R, Read DJ (eds) Nitrogen, phosphorus and sulphur utilization by fungi. Cambridge University Press, Cambridge, pp 181–204Google Scholar
  177. Roberts P, Jones D (2008) Critical evaluation of methods for determining total protein in soil solution. Soil Biol Biochem 40:1485–1495CrossRefGoogle Scholar
  178. Rodriguez-Tovar AV, Ruiz-Medrano R, Herrera-Martinez A, Barrera-Figueroa BE, Hidalgo-Lara ME, Reyes-Marquez BE, Cabrera-Ponce JL, Valdes M, Xoconostle-Cazares B (2005) Stable genetic transformation of the ectomycorrhizal fungus Pisolithus tinctorius. J Microbiol Methods 63:45–54PubMedCrossRefGoogle Scholar
  179. Rutherford JC, Bird AJ (2004) Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3:1–13PubMedCrossRefGoogle Scholar
  180. Ruytinx J, Craciun AR, Verstraelen K, Vangronsveld J, Colpaert JV, Verbruggen N (2011) Transcriptome analysis by cDNA-AFLP of Suillus luteus Cd-tolerant and Cd-sensitive isolates. Mycorrhiza 21:145–154PubMedCrossRefGoogle Scholar
  181. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  182. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  183. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefGoogle Scholar
  184. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedCrossRefGoogle Scholar
  185. Scott B, Eaton CJ (2008) Role of reactive oxygen species in fungal cellular differentiations. Curr Opin Microbiol 11:488–493PubMedCrossRefGoogle Scholar
  186. Selosse MA, Weiß M, Jany JL, Tillier A (2002) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L.C.M. Rich. and neighbouring tree ectomycorrhizae. Mol Ecol 11:1831–1844PubMedCrossRefGoogle Scholar
  187. Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbiol Ecol 47:416–426CrossRefGoogle Scholar
  188. Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878PubMedCrossRefGoogle Scholar
  189. 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 169:355–365PubMedCrossRefGoogle Scholar
  190. Sharples JM, Chambers SM, Meharg AA, Cairney JWG (2000a) Genetic diversity of root-associated fungal endophytes from Calluna vulgaris at contrasting field sites. New Phytol 148:153–162CrossRefGoogle Scholar
  191. Sharples JM, Meharg AA, Chambers SM, Cairney JWG (2000b) Mechanism of arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. Plant Physiol 124:1327–1334PubMedCrossRefGoogle Scholar
  192. Sharples JM, Meharg AA, Chambers SM, Cairney JWG (2001) Arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol 151:265–270CrossRefGoogle Scholar
  193. Silver S, Phung LT (2009) Heavy metals, bacterial resistance. In: Schaechter M (ed) Encyclopedia of microbiology. Elsevier, Oxford, pp 220–227CrossRefGoogle Scholar
  194. Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582CrossRefGoogle Scholar
  195. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, LondonGoogle Scholar
  196. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  197. Sokolovski SG, Meharg AA, Maathuis FJM (2002) Calluna vulgaris root cells show increased capacity for amino acid uptake when colonized with the mycorrhizal fungus Hymenoscyphus ericae. New Phytol 155:525–530CrossRefGoogle Scholar
  198. Straker CJ (1996) Ericoid mycorrhiza: ecological and host specificity. Mycorrhiza 6:215–225CrossRefGoogle Scholar
  199. Straker CJ, Mitchell DT (1986) The activity and characterization of acid phosphatase in endomycorrhizal fungi of the Ericaceae. New Phytol 104:243–256CrossRefGoogle Scholar
  200. Straker CJ, Mitchell DT (1987) Kinetic characterization of dual phosphate uptake system in the endomycorrhizal fungus of Erica hispidula L. New Phytol 106:129–137CrossRefGoogle Scholar
  201. Stribley DP, Read DJ (1974) Biology of mycorrhiza in Ericaceae. 4. Effect of mycorrhizal infection on uptake of N-15 from labeled soil by Vaccinium macrocarpon Ait. New Phytol 73:1149–1155CrossRefGoogle Scholar
  202. Talbot JM, Treseder KK (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53:169–179CrossRefGoogle Scholar
  203. Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11:3166–3178PubMedCrossRefGoogle Scholar
  204. Todorova D, Nedeva D, Abrashev R, Tsekova K (2008) Cd (II) stress response during the growth of Aspergillus niger B 77. J Appl Microbiol 104:178–184PubMedGoogle Scholar
  205. Tomsett BA (1993) Genetic and molecular biology of metal tolerance in fungi. In: Jennings DH (ed) Stress tolerance of fungi. Dekker, New York, pp 69–95Google Scholar
  206. Upson R, Read DJ, Newsham KK (2007) Widespread association between the ericoid mycorrhizal fungus Rhizoscyphus ericae and a leafy liverwort in the maritime and sub-Antarctic. New Phytol 176:460–471PubMedCrossRefGoogle Scholar
  207. Vallino M, Drogo V, Abbà S, Perotto S (2005) Gene expression of the ericoid mycorrhizal fungus Oidiodendron maius in the presence of high zinc concentrations. Mycorrhiza 15:333–344PubMedCrossRefGoogle Scholar
  208. Vallino M, Martino E, Boella F, Murat C, Chiapello M, Perotto S (2009) Cu, Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol Lett 293:48–57PubMedCrossRefGoogle Scholar
  209. Vallino M, Zampieri E, Murat C, Girlanda M, Picarella S, Pitet M, Portis E, Martino E, Perotto S (2011) Specific regions in the Sod1 locus of the ericoid mycorrhizal fungus Oidiodendron maius from metal enriched soils show different sequence polymorphism. FEMS Microbiol Ecol 75:321–331PubMedCrossRefGoogle Scholar
  210. Van Leerdam DM, Williams PA, Cairney JWG (2001) Phosphate solubilising abilities of ericoid mycorrhizal endophytes of Woollsia pungens (Epacridaceae). Austral J Bot 49:75–80CrossRefGoogle Scholar
  211. Van der Wal A, De Boer W, Klein Gunnewiek PJA, van Veen JA (2009) Possible mechanism for Spontaneous establishment of Calluna vulgaris in a recently abandoned agricultural field. Restor Ecol 17:308–313CrossRefGoogle Scholar
  212. Varma A, Bonfante P (1994) Utilisation of cell-wall related carbohydrates by ericoid mycorrhizal endophytes. Symbiosis 16:301–313Google Scholar
  213. Vido K, Spector D, Lagniel G, Lopez S, Toledano MB, Labarre J (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J Biol Chem 276:8469–8474PubMedCrossRefGoogle Scholar
  214. Villarreal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192CrossRefGoogle Scholar
  215. 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 52:407–414CrossRefGoogle Scholar
  216. Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi partof a common guild? New Phytol 164:7–10CrossRefGoogle Scholar
  217. Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata- the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563CrossRefGoogle Scholar
  218. Vrålstad T, Myhre E, Schumacher T (2002a) Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytol 155:131–148CrossRefGoogle Scholar
  219. Vrålstad T, Schumacher T, Taylor AFS (2002b) Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–152CrossRefGoogle Scholar
  220. Weiss M (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010PubMedCrossRefGoogle Scholar
  221. Whittaker SP, Cairney JWG (2001) Influence of amino acids on biomass production by ericoid mycorrhizal endophytes from Woollsia pungens (Epacridaceae). Mycol Res 105:105–111CrossRefGoogle Scholar
  222. Wilcox HE, Wang CJK (1987) Ectomycorrhizal and ectoendomycorrhizal associations of Phialophora finlandia with Pinus resinosa, Picea rubens and Betula alleghaniensis. Can J For Res 17:976–990CrossRefGoogle Scholar
  223. Xiao G, Berch SM (1996) Diversity and abundance of ericoid mycorrhizal fungi of Gaultheria shallon on forest clearcuts. Can J Bot 74:337–346CrossRefGoogle Scholar
  224. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–171CrossRefGoogle Scholar
  225. Yoo HY, Chang MS, Rho HM (1999) Heavy metal-mediated activation of the rat Cu/Zn superoxide dismutase gene via a metal-responsive element. Mol Gen Genet 262:310–313PubMedCrossRefGoogle Scholar
  226. Zhang YH, Zhuang WY (2004) Phylogenetic relationships of some members in the genus Hymenoscyphus (Ascomycetes, Helotiales). Nova Hedwigia 78:475–484CrossRefGoogle Scholar
  227. Zhu H, Dancik BP, Higginbotham KO (1994) Regulation of extracellular proteinase production in an ectomycorrhizal fungus Hebeloma crustuliniforme. Mycologia 86:227–234CrossRefGoogle Scholar
  228. Zijlstra JD, van Hof P, Baar J, Verkley GJM, Summerbell RC, Paradi I, Braakhekke WG, Berendse F (2005) Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass Deschampsia flexuosa. Stud Mycol 53:147–162CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Dipartimento di Scienzedella Vita e Biologia dei Sistemi dell’Università di Torino and Istituto per la Protezione delle Piante del CNRTorinoItaly

Personalised recommendations