Mycorrhization of Fagaceae Forests Within Mediterranean Ecosystems

  • Francisca Reis
  • Rui M. Tavares
  • Paula Baptista
  • Teresa Lino-NetoEmail author


Mediterranean Fagaceae forests are valuable due to their ecological and socioeconomic aspects. Some profitable plant species, such as Castanea (timber and chestnut), Quercus (timber and cork), and Fagus (timber), encounter in this habitat the excellent edaphoclimatic conditions to develop. All Fagaceae plants are commonly associated to ECM fungal species, which are found in these forests in quite stable communities, mainly enriched in Russulaceae and Telephoraceae species. Currently, the Mediterranean Basin is considered as one of the global biodiversity hotspots, since many of their endemic plant species are not found elsewhere and are now under threat. Due to climate changing and introduction of disease agents, Fagaceae forests are facing an adaptation challenge to both biotic and abiotic threats. Although ECM communities are highly disturbed by climate factors and tree disease incidence, they could play an important role in increasing water availability to the plant and also improving plant tree defense against pathogens. Recent advances, namely, on genomics and transcriptomics, are providing tools for increasing the understanding of Fagaceae mycorrhization process and stress responses to biotic and abiotic stresses. Such studies can provide new information for the implementation of the most adequate management policies for protecting threaten Mediterranean forests.


Arbuscular Mycorrhizal Fruit Body Mediterranean Forest American Chestnut Chestnut Blight 
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.


  1. Acácio V, Holmgren M, Rego F, Moreira F, Mohren GMJ (2009) Are drought and wildfires turning Mediterranean cork oak forests into persistent shrublands? Agrofor Syst 76:389–400. doi: 10.1007/s10457-008-9165-y CrossRefGoogle Scholar
  2. Agerer R (2001) Exploration types of ectomycorrhizae—a proposal to classify ectomycorrhizal myce-lial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  3. Amaral Franco J (1990) Quercus. In: Castroviejo S (ed) Flora Iberica, vol 2. Real Jardín Botánico de Madrid, CSIC, Madrid, pp 15–36Google Scholar
  4. Anagnostakis SL (1987) Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:23–27CrossRefGoogle Scholar
  5. Aponte C, García LV, Marañón T, Gardes M (2010) Indirect host effect on ectomycorrhizal fungi: leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Biol Biochem 42:788–796. doi: 10.1016/j.soilbio.2010.01.014 CrossRefGoogle Scholar
  6. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robins N, Herrer EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aryantha IP, Cross R, Guest DI (2000) Suppression of Phytophthora cinnamomi in potting mixes amended with uncomposted and composted animal manures. Phytopathology 90:775–782. doi: 10.1094/PHYTO.2000.90.7.775 PubMedCrossRefGoogle Scholar
  8. Azul AM, Sousa JP, Agerer R, Martín MP, Freitas H (2010) Land use practices and ectomycorrhizal fungal communities from oak woodlands dominated by Quercus suber L. considering drought scenarios. Mycorrhiza 20:73–88. doi: 10.1007/s00572-009-0261-2 PubMedCrossRefGoogle Scholar
  9. Baptista P, Martins A, Tavares RM, Lino-Neto T (2010) Diversity and fruiting pattern of macrofungi associated with chestnut (Castanea sativa) in the Trás-os-Montes region (Northeast Portugal). Fungal Ecol 3:9–19. doi: 10.1016/j.funeco.2009.06.002 CrossRefGoogle Scholar
  10. Baptista P, Reis F, Pereira E, Tavares RM, Santos P, Richard F, Selosse MA, Lino-Neto T (2015) Soil DNA pyrosequencing and fruitbody surveys reveal contrasting diversity for various fungal ecological guilds in chestnut orchards. Environ Microbiol Rep 7:946–954. doi: 10.1111/1758-2229.12336 PubMedCrossRefGoogle Scholar
  11. Bauman JM, Keiffer CH, Hiremath S, Mccarthy BC (2013) Soil preparation methods promoting ectomycorrhizal colonization and American chestnut Castanea dentata establishment in coal mine restoration. J Appl Ecol 50:721–729. doi: 10.1111/1365-2664.12070 CrossRefGoogle Scholar
  12. 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
  13. Blom JM, Vannini A, Vettraino AM, Hale MD, Godbold DL (2009) Ectomycorrhizal community structure in a healthy and a Phytophthora-infected chestnut (Castanea sativa Mill.) stand in central Italy. Mycorrhiza 20:25–38. doi: 10.1007/s00572-009-0256-z PubMedCrossRefGoogle Scholar
  14. Blondel J, Aronson J, Bodiou JY, Boeuf G (2010) The Mediterranean region: biological diversity in space and time. Oxford, Oxford University PressGoogle Scholar
  15. Blumenstein K, Macaya-Sanz D, Martín JA, Albrectsen BR, Witzell J (2015) Phenotype microarrays as a complementary tool to next generation sequencing for characterization of tree endophytes. Front Microbiol 6:1033. doi: 10.3389/fmicb.2015.01033 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Boa E (2004) Wild edible fungi a global overview of their use and importance to people. Google Scholar
  17. Branzanti MB, Rocca E, Pisi A (1999) Effect of ectomycorrhizal fungi on chestnut ink disease. Mycorrhiza 9:103–109CrossRefGoogle Scholar
  18. Brasier CM (1996) Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change. Ann Sci For 53:347–358. doi: 10.1051/forest:19960217 CrossRefGoogle Scholar
  19. Brasier CM (2000) The role of Phytophthora pathogens in forests and semi-natural communities in Europe and Africa. In: Hansen EM, Sutton W (eds) Phytophthora diseases of forest trees. First International Meeting on Phytophthoras in Forest and Wildland Ecosystems. Forest Research Laboratory, Oregon State UniversityGoogle Scholar
  20. Brasier F, Ferraz JFP, Robredo CM (1993) Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathol 42:140–145. doi: 10.1111/j.1365-3059.1993.tb01482.x CrossRefGoogle Scholar
  21. Brasier CM, Denman S, Brown A, Webber J (2004) Sudden oak death (Phytophthora ramorum) discovered on trees in Europe. Mycol Res 108:1108–1110. doi: 10.1017/S0953756204221244 CrossRefGoogle Scholar
  22. Breda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644. doi:10.1051/forest: 2006042CrossRefGoogle Scholar
  23. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  24. Brunet J, Fritz Ö, Richnau G (2010) Biodiversity in European beech forests—a review with recommendations for sustainable forest management. Ecol Bull 53:77–94Google Scholar
  25. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. doi: 10.3389/fpls.2015.00547 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. Plant Sci 4:107–138. doi: 10.5772/52570 Google Scholar
  27. Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245. doi: 10.1007/s00572-004-0313-6 PubMedCrossRefGoogle Scholar
  28. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–445PubMedCrossRefGoogle Scholar
  29. Buscardo E, Rodriguez-Echeverria S, Martin MP, De Angelis P, Pereira JS, Freitas H (2010) Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol 114:628–636. doi: 10.1016/j.funbio.2010.05.004 PubMedCrossRefGoogle Scholar
  30. Bussotti F, Ferrini F, Pollastrini M, Fini A (2013) The challenge of Mediterranean sclerophyllous vegetation under climate change: from acclimation to adaptation. Environ Exp Bot 103:80–98. doi: 10.1016/j.envexpbot.2013.09.013 CrossRefGoogle Scholar
  31. Camilo-Alves C, da Clara MIE, de Almeida Ribeiro NMC (2013) Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. Eur J For Res 132:411–432. doi: 10.1007/s10342-013-0688-z CrossRefGoogle Scholar
  32. Causin R, Montecchio L, Accordi SM (1996) Probability of ectomycorrhizal infection in a declining stand of common oak. Ann For Sci 53:743–752. doi: 10.1051/forest:19960250 CrossRefGoogle Scholar
  33. Chaturvedi S, Tewari V, Sharma S, Oehl F, Wiemken A, Prakash A, Sharma AK (2012) Diversity of arbuscular mycorrhizal fungi in oak-pine forests and agricultural land prevalent in the Kumaon Himalayan Hills. Br Microbiol Res J 2:82–96. doi: 10.9734/BMRJ/2012/1136 CrossRefGoogle Scholar
  34. Choupina AB, Estevinho L, Martins I (2014) Scientifically advanced solutions for chestnut ink disease. Appl Microbiol Biotechnol 98:3905–3909. doi: 10.1007/s00253-014-5654-2 PubMedCrossRefGoogle Scholar
  35. Coince A, Cael O, Bach C, Lengelle J, Cruaud C, Gavory F, Morin E, Murat C, Marcais B, Buee M (2013) Below-ground fine-scale distribution and soil versus fine root detection of fungal and soil oomycete communities in a French beech forest. Fungal Ecol 6:223–235CrossRefGoogle Scholar
  36. Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39CrossRefGoogle Scholar
  37. Compant S, van der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214PubMedGoogle Scholar
  38. Condé S, Richard D, Liamine N (2005) European Environment Agency Europe’ s biodiversity The Mediterranean biogeographical region. In: EEA Europe’s Biodiversity, Alpine, pp 1–54Google Scholar
  39. Corcobado T, Vivas M, Moreno G, Solla A (2014) Ectomycorrhizal symbiosis in declining and non-declining Quercus ilex trees infected with or free of Phytophthora cinnamomi. For Ecol Manage 324:72–80. doi: 10.1016/j.foreco.2014.03.040 CrossRefGoogle Scholar
  40. Courty P, Franc A, Pierrat J, Garbaye J, Fore R (2008) Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Appl Environ Microbiol 74:5792–5801. doi: 10.1128/AEM.01592-08 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dawe AL, Nuss DL (2001) Hypoviruses and chestnut blight: exploiting viruses to understand and modulate fungal pathogenesis. Annu Rev Genet 35:1–29. doi: 10.1146/annurev.genet.35.102401.085929 PubMedCrossRefGoogle Scholar
  42. De Román M, de Miguel AM (2005) Post-fire, seasonal and annual dynamics of the ectomycorrhizal community in a Quercus ilex L. forest over a 3-year period. Mycorrhiza 15:471–482. doi: 10.1007/s00572-005-0353-6 PubMedCrossRefGoogle Scholar
  43. Di Pietro M, Churin JL, Garbaye J (2007) Differential ability of ectomycorrhizas to survive drying. Mycorrhiza 17:547–555. doi: 10.1007/s00572-007-0113-x PubMedCrossRefGoogle Scholar
  44. Diamandis S, Perlerou C (2001) The mycoflora of the chestnut ecosystems in Greece. For Snow Landsc Res 76:499–504Google Scholar
  45. DiLeo MV, Bostock RM, Rizzo DM (2009) Phytophthora ramorum does not cause physiologically significant systemic injury to California bay laurel, its primary reservoir host. Phytopathology 99:1307–1311. doi: 10.1094/PHYTO-99-11-1307 PubMedCrossRefGoogle Scholar
  46. Ding Q, Liang Y, Legendre P, He X, Pei K, Du X, Ma K (2011) Diversity and composition of ectomycorrhizal community on seedling roots: the role of host preference and soil origin. Mycorrhiza 21:669–680. doi: 10.1007/s00572-011-0374-2 PubMedCrossRefGoogle Scholar
  47. Dixon RK, Wright GM, Behrns GT, Tesky RO, Hinckley TM (1980) Water deficits and root growth of ectomycorrhizal white oak seedlings. Can J For Res 10:545–548CrossRefGoogle Scholar
  48. Dulmer KM, Leduc SD, Horton TR (2014) Ectomycorrhizal inoculum potential of northeastern US forest soils for American chestnut restoration: results from field and laboratory bioassays. Mycorrhiza 24:65–74. doi: 10.1007/s00572-013-0514-y PubMedCrossRefGoogle Scholar
  49. Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483. doi: 10.1093/jxb/erm009 PubMedCrossRefGoogle Scholar
  50. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194. doi: 10.1038/nature10947 PubMedCrossRefGoogle Scholar
  51. Franceschini A, Maddau L, Marras F (2002) Osservazioni sull’incidenza di funghi endofiti associati al deperimento di Quercus suber e Q. pubescens. In: Franceschi-ni A, Marras F (eds) L’Endofitismo di Funghi e Batteri Patogeni in Piante Arboree e Arbustive. Sassari-Tempio Pausania, Italy, pp 313–325Google Scholar
  52. Gebhardt S, Neubert K, Wöllecke J, Münzenberger B, Hüttl RF (2007) Ectomycorrhiza communities of red oak (Quercus rubra L.) of different age in the Lusatian lignite mining district, East Germany. Mycorrhiza 17:279–290. doi: 10.1007/s00572-006-0103-4 PubMedCrossRefGoogle Scholar
  53. Heiniger U, Rigling D (1994) Biological control of chestnut blight in Europe. Annu Rev Phytopathol 32:581–599. doi: 10.1146/ CrossRefGoogle Scholar
  54. Herrmann S (2007) Cross talks at the morphogenetic, physiological and gene regulation levels between the mycobiont Piloderma croceum and oak microcuttings (Quercus robur) during formation of ectomycorrhizas. Phytochemestry 68:52–67. doi: 10.1016/j.phytochem.2006.09.028 CrossRefGoogle Scholar
  55. Herzog C, Peter M, Pritsch K, Gu MS (2012) Drought and air warming affects abundance and exoenzyme profiles of Cenococcum geophilum associated with Quercus. Plant Biol 15:230–237. doi: 10.1111/j.1438-8677.2012.00614.x PubMedCrossRefGoogle Scholar
  56. Jany JL, Garbaye J, Martin F (2002) Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytol 154:651–659. doi: 10.1046/j.1469-8137.2002.00408.x CrossRefGoogle Scholar
  57. Jönsson-Belyazio U, Rosengren U (2006) Can Phytophthora quercina have a negative impact on mature pedunculate oaks under field conditions? Ann For Sci 63:661–672. doi: 10.1051/forest:2006047 CrossRefGoogle Scholar
  58. Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D (2006) Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland. Soil Biol Biochem 38:2448–2246. doi: 10.1016/j.soilbio.2006.02.021 CrossRefGoogle Scholar
  59. Kasai K, Usami T, Lee J, Ishikawa SI, Oikawa T (2000) Responses of ectomycorrhizal colonization and morphotype assemblage of Quercus myrsinaefolia seedlings to elevated air temperature and elevated atmospheric CO2. Microbes Environ 15:197–207CrossRefGoogle Scholar
  60. Keen B, Vancov T (2010) Phytophthora cinnamomi suppressive soils. In: Curent research, technology and education topics in applied microbiology and microbial biotechnology. FORMATEX, pp 239–250Google Scholar
  61. Keenan RJ (2015) Climate change impacts and adaptation in forest management: a review. Ann For Sci 72:145–167. doi: 10.1007/s13595-014-0446-5 CrossRefGoogle Scholar
  62. Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457. doi: 10.3732/ajb.1200558 PubMedCrossRefGoogle Scholar
  63. Kremer A, Abbott AG, Carlson JE, Manos PS, Plomion C, Sisco P, Staton ME, Ueno S, Vendramin GG (2012) Genomics of Fagaceae. Tree Genet Genomes 8:583–610. doi: 10.1007/s11295-012-0498-3 CrossRefGoogle Scholar
  64. Kuikka K, Härmä E, Markkola AM, Rautio P, Roitto M, Saikkonen K, Ahonen-Jonnarth U, Finlay R, Tuomi J (2003) Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology 84:2051–2061. doi: 10.1890/02-0359 CrossRefGoogle Scholar
  65. Kurth F, Feldhahn L, Bönn M, Herrmann S, Buscot F, Tarkka MT (2015) Large scale transcriptome analysis reveals interplay between development of forest trees and a beneficial mycorrhiza helper bacterium. BMC Genomics 16:1–13. doi: 10.1186/s12864-015-1856-y CrossRefGoogle Scholar
  66. Kurz-Besson C, Otieno D, Lobo Do Vale R, Siegwolf R, Schmidt M, Herd A, Nogueira C, David TS, David JS, Tenhunen J, Pereira JS, Chaves M (2006) Hydraulic lift in cork oak trees in a savannah-type Mediterranean ecosystem and its contribution to the local water balance. Plant Soil 282:361–378. doi: 10.1007/s11104-006-0005-4 CrossRefGoogle Scholar
  67. Laganà A, Salerni E, Barluzzi C, Perini C, De Dominicis V (2002) Macrofungi as long-term indicators of forest health and management in central Italy. Cryptogam Mycol 23:39–50Google Scholar
  68. Lancellotti E, Franceschini A (2013) Studies on the ectomycorrhizal community in a declining Quercus suber L. stand. Mycorrhiza 23:533–542. doi: 10.1007/s00572-013-0493-z PubMedCrossRefGoogle Scholar
  69. Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90. doi: 10.1007/s00572-010-0348-9 PubMedCrossRefGoogle Scholar
  70. Lesur I, Le Provost G, Bento P, Silva C, Leplé JC, Murat F, Ueno F, Bartholomé J, Lalanne C, Ehrenmann C, Plomion C (2015) The oak gene expression atlas: insights into Fagaceae genome evolution and the discovery of genes regulated during bud dormancy release. BMC Genomics 16:112. doi: 10.1186/s12864-015-1331-9 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lindner M, Fitzgerald JB, Zimmermann NE, Reyer C, Delzon S, van der Maaten E, Hanewinkel M (2014) Climate change and European forests: what do we know, what are the uncertainties, and what are the implications for forest management? J Environ Manage 146:69–83. doi: 10.1016/j.jenvman.2014.07.030 PubMedCrossRefGoogle Scholar
  72. Lumaret R, Mir C, Michaud H, Raynal V (2002) Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.) Mol Ecol 11:2327–2336. doi: 10.1046/j.1365-294X.2002.01611.x PubMedCrossRefGoogle Scholar
  73. Magalhães AP, Verde N, Reis F, Martins I, Costa D, Lino-Neto T, Castro PH, Tavares PH, Azevedo H (2016) RNA-Seq and gene network analysis uncover activation of an ABA-dependent signalosome during the cork oak root response to drought. Front Plant Sci 6:1195. doi: 10.3389/fpls.2015.01195 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Malajczuk N (1979) Biological suppression of Phytophthora cinnamomi in eucalyptus and avocados in Australia. In: Schippers B, Gams W (eds) Soil-borne plant pathogens. Academic, LondonGoogle Scholar
  75. Malajczuk N, McComb A (1979) The microflora of unsubersied roots of Eucalyptus calophylla R. Br. and Eucalytpus marginata Donn ex Sm. seedlings grown in soils suppressive and conducive to Phytophthora cinnamomi Rands. I. Rhizosphere bacteria, actinomycetes and fungi. Aust J Bot 27:235–254CrossRefGoogle Scholar
  76. Malcolm GM, López-Gutiérrez JC, Koide RT, Eissenstat DM (2008) Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi. Glob Chang Biol 14:1169–1180. doi: 10.1111/j.1365-2486.2008.01555.x CrossRefGoogle Scholar
  77. Manos CH, Oh SH (2008) Phylogenetic relationships and taxonomic status of the paleoendemic Fagaceae of Western North America: recognition of a new genus. Madroño 55:181–190. doi: 10.3120/0024-9637-55.3.181 CrossRefGoogle Scholar
  78. Manos PS, Zhou ZK, Cannon CH (2001) Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. Int J Plant Sci 162:1361–1379CrossRefGoogle Scholar
  79. Markkola AM, Kuikka K, Rautio P, Härmä E, Roitto M, Tuomi J (2004) Defoliation increases carbon limitation in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140:234–240. doi: 10.1007/s00442-004-1587-2 PubMedCrossRefGoogle Scholar
  80. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92. doi: 10.1038/nature06556 PubMedCrossRefGoogle Scholar
  81. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038. doi: 10.1038/nature08867 PubMedCrossRefGoogle Scholar
  82. Marx D (1972) Ectomycorrhizal and nonmycorrhizal shortleaf pine seedlings in soil with Phytophthora cinnamomi. Annu Rev Phytopathol 10:1472–1473CrossRefGoogle Scholar
  83. Milgroom MG, Wang KR, Zhou Y, Lipari SE, Kaneko S (1996) Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88:179–190. doi: 10.2307/3760921 CrossRefGoogle Scholar
  84. Mohan V, Nivea R, Menon S (2015) Evaluation of ectomycorrhizal fungi as potential bio-control agents against selected plant pathogenic fungi. J Acad Ind Res 3:408–412Google Scholar
  85. Montecchio L, Causin R, Rossi S, Mutto Acordi S (2004) Changes in ectomycorrhizal diversity in a declining Quercus ilex coastal forest. Phytopathol Mediterr 43:26–34. doi:10.14601/Phytopathol_Mediterr-1721Google Scholar
  86. Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98:380–386. doi: 10.1094/PHYTO-98-4-0380 PubMedCrossRefGoogle Scholar
  87. Moricca S, Ginetti B, Ragazzi A (2012) Species- and organ-specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol Mediterr 51:587–598. doi:10.14601/Phytopathol_Mediterr-11705Google Scholar
  88. Moricca S, Franceschini A, Ragazzi A, Linaldeddu BT, Lancellotti E (2014) Studies on communities of endophytic (end) and ectomycorrhizal (ecm) fungi associated with oaks in pure and mixed stands. In: Pirttilä AM, Sorvari S (eds) Prospects and applications for plant-associated microbes, a laboratory manual: Part B: FungiGoogle Scholar
  89. Myers N, Mittermeier RA, Mittermeier CG, Fonseca G, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. doi: 10.1038/35002501 PubMedCrossRefGoogle Scholar
  90. Nardini A, Salleo S, Tyree MT, Vertovec M (2000) Influence of the ectomycorrhizas formed by Tuber melanosporum Vitt. on hydraulic conductance and water relations of Quercus ilex L. seedlings. Ann For Sci 57:305–312. doi: 10.1051/forest:2000121 CrossRefGoogle Scholar
  91. Nardini A, Lo Gullo MA, Trifilò P, Salleo S (2014) The challenge of the Mediterranean climate to plant hydraulics: responses and adaptations. Environ Exp Bot 103:68–79. doi: 10.1016/j.envexpbot.2013.09.018 CrossRefGoogle Scholar
  92. Nixon KC, Crepet WL (1989) Trigonobalanus (Fagaceae): taxonomy status and phylogenetic relashionship. Am J Bot 76:826–841CrossRefGoogle Scholar
  93. Nuche P, Komac B, Camarero JJ, Alados CL (2014) Developmental instability as an index of adaptation to drought stress in a Mediterranean oak. Ecol Indic 40:68–75. doi: 10.1016/j.ecolind.2013.12.023 CrossRefGoogle Scholar
  94. Núñez JAD, Serrano JS, Barreal JAR, de Omeñaca González JAS (2006) The influence of mycorrhization with Tuber melanosporum in the afforestation of a Mediterranean site with Quercus ilex and Quercus faginea. For Ecol Manage 231:226–233. doi: 10.1016/j.foreco.2006.05.052 CrossRefGoogle Scholar
  95. Oh S, Manos PS (2008) Molecular phylogenetics and cupule evolution in Fagaceae as inferred from nuclear CRABS CLAW sequences. Taxon 57:434–451Google Scholar
  96. Oliveira RS, Franco AR, Vosátka M, Castro PML (2010) Management of nursery practices for efficient ectomycorrhizal fungi application in the production of Quercus ilex. Symbiosis 52:125–131. doi: 10.1007/s13199-010-0092-0 CrossRefGoogle Scholar
  97. Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonising arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790. doi: 10.1111/j.1365-2745.2006.01136.x CrossRefGoogle Scholar
  98. Orgiazzi A, Lumini E, Nilsson RH, Girlanda M, Vizzini A, Bonfante P, Bianciotto V (2012) Unravelling soil fungal communities from different mediterranean land-use backgrounds. PLoS One 7:1–9. doi: 10.1371/journal.pone.0034847 CrossRefGoogle Scholar
  99. Orgiazzi A, Dunbar MB, Panagos P, de Groot GA, Lemanceau P (2015) Soil biodiversity and DNA barcodes: opportunities and challenges. Soil Biol Biochem 80:244–250. doi: 10.1016/j.soilbio.2014.10.014 CrossRefGoogle Scholar
  100. Ortega A, Lorite J (2007) Macrofungi diversity in cork-oak and holm-oak forests in Andalusia (southern Spain); an efficient parameter for establishing priorities for its evaluation and conservation. Cent Eur J Biol 2:276–296. doi: 10.2478/s11535-007-0015-0 Google Scholar
  101. Palmer J, Lindner D, Volk T (2008) Ectomycorrhizal characterization of an American chestnut (Castanea dentata)-dominated community in western Wisconsin. Mycorrhiza 19:27–36. doi: 10.1007/s00572-008-0200-7 PubMedCrossRefGoogle Scholar
  102. Peintner U, Iotti M, Klotz P, Bonuso E, Zambonelli A (2007) Soil fungal communities in a Castanea sativa (chestnut) forest producing large quantities of Boletus edulis sensu lato (porcini): where is the mycelium of porcini? Environ Microbiol 9:880–889. doi: 10.1111/j.1462-2920.2006.01208.x PubMedCrossRefGoogle Scholar
  103. Pereira-Leal JB, Abreu IA, Alabaça CS, Almeida MH, Almeida P, Almeida T et al (2014) A comprehensive assessment of the transcriptome of cork oak (Quercus suber) through EST sequencing. BMC Genomics 15:371. doi: 10.1186/1471-2164-15-371 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Pietras M, Rudawska M, Leski T, Karliński L (2013) Diversity of ectomycorrhizal fungus assemblages on nursery grown European beech seedlings. Ann For Sci 70:115–121. doi: 10.1007/s13595-012-0243-y CrossRefGoogle Scholar
  105. Plomion C, Bastien C, Bogeat-Triboulot MB, Bouffier L, Déjardin A, Duplessis S, Vacher C (2015) Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci 73:77–103. doi: 10.1007/s13595-015-0488-3 CrossRefGoogle Scholar
  106. Querejeta JI, Egerton-Warburton LM, Allen MF (2007) Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California Oak savanna. Soil Biol Biochem 39:409–417. doi: 10.1016/j.soilbio.2006.08.008 CrossRefGoogle Scholar
  107. Ragazzi A, Moricca S, Capretti P, Dellavalle I, Mancini F, Turco E (2001) Endophytic fungi in Quercus cerris: isolation frequency in relation to phenological phase, tree health and the organ affected. Phytopathol Mediterr 40:165–171. doi:10.14601/Phytopathol_Mediterr-1598Google Scholar
  108. Ragazzi A, Moricca S, Capretti P, Dellavalle I, Turco E (2003) Differences in composition of endophytic mycobiota in twigs and leaves of healthy and declining Quercus species in Italy. For Pathol 33:31–38. doi: 10.1046/j.1439-0329.2003.3062003.x Google Scholar
  109. Ragazzi A, Moricca S, Dellavalle I (2004) Endophytism in forest trees. Accademia Italiana di Scienze Forestali, FirenzeGoogle Scholar
  110. Ramirez-Valiente JA, Lorenzo Z, Soto A, Valladares F, Gil L, Aranda I (2009) Elucidating the role of genetic drift and natural selection in cork oak differentiation regarding drought tolerance. Mol Ecol 18:3803–3815. doi: 10.1111/j.1365-294X.2009.04317.x PubMedCrossRefGoogle Scholar
  111. Ramirez-Valiente JA, Valladares F, Huertas AD, Granados S, Aranda I (2011) Factors affecting cork oak growth under dry conditions: local adaptation and contrasting additive genetic variance within populations. Tree Genet Genomes 7:285–295. doi: 10.1007/s11295-010-0331-9 CrossRefGoogle Scholar
  112. Richard F, Moreau PA, Selosse MA, Gardes M (2004) Diversity and fruiting patterns of ectomycorrhizal and saprobic fungi in an old-growth Mediterranean forest dominated by Quercus ilex L. Can J Bot 82:1711–1729. doi: 10.1139/B04-128 CrossRefGoogle Scholar
  113. Richard F, Millot S, Gardes M, Selosse M-A (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166:1011–1023. doi: 10.1111/j.1469-8137.2005.01382.x PubMedCrossRefGoogle Scholar
  114. Richard F, Roy M, Shahin O, Sthultz C, Duchemin M, Joffre R, Selosse MA (2011) Ectomycorrhizal communities in a Mediterranean forest ecosystem dominated by Quercus ilex: seasonal dynamics and response to drought in the surface organic horizon. Ann For Sci 68:57–68. doi: 10.1007/s13595-010-0007-5 CrossRefGoogle Scholar
  115. Robin C, Heiniger U (2001) Chestnut blight in Europe: diversity of Cryphonectria parasitica, hypovirulence and biocontrol. For Snow Landsc Res 76:361–367Google Scholar
  116. Robin C, Smith I, Hansen EM (2012) Phythophthora cinnamomi. For Phytophthoras 2(1). doi: 10.5399/osu/fp.2.1.3041
  117. Rocheta M, Sobral R, Magalhães J, Amorim MI, Ribeiro T, Pinheiro M, Egas C, Morais-Cecílio L, Costa MM (2014) Comparative transcriptomic analysis of male and female flowers of monoecious Quercus suber. Front Plant Sci 6:599. doi: 10.3389/fpls.2014.00599 Google Scholar
  118. Saravesi K, Markkola AM, Rautio P, Roitto M, Tuomi J (2008) Defoliation causes parallel temporal responses in a host tree and its fungal symbionts. Oecologia 156:117–123. doi: 10.1007/s00442-008-0967-4 PubMedCrossRefGoogle Scholar
  119. Savoie J, Largeteau ML (2011) Production of edible mushrooms in forests: trends in development of a mycosilviculture. Appl Microbiol Biotechnol 89:971–979. doi: 10.1007/s00253-010-3022-4 PubMedCrossRefGoogle Scholar
  120. Schmitz S, Zini J, Chandelier A (2006) Involvement of Phytophthora species in the decline of beech Fagus sylvatica in Wallonia (Belgium). Commun Agric Appl Biol Sci 72(4):879–885Google Scholar
  121. Sebastiana M, Figueiredo A, Acioli B, Sousa L, Pessoa F, Baldi A, Pais MS (2009) Identification of plant genes involved on the initial contact between ectomycorrhizal symbionts (Castanea sativa—European chestnut and Pisolithus tinctorius). Eur J Soil Biol 45:275–282. doi: 10.1016/j.ejsobi.2009.02.001 CrossRefGoogle Scholar
  122. Sebastiana M, Pereira VT, Alcântara A, Pais MS, Silva AB (2013) Ectomycorrhizal inoculation with Pisolithus tinctorius increases the performance of Quercus suber L. (cork oak) nursery and field seedlings. New For 44:937–949. doi: 10.1007/s11056-013-9386-4 CrossRefGoogle Scholar
  123. Sebastiana M, Vieira B, Lino-Neto T, Monteiro F, Figueiredo A, Sousa L, Pais MS, Tavares R, Paulo O (2014) Oak root response to ectomycorrhizal symbiosis establishment: RNA-Seq derived transcript identification and expression profiling. PLoS One 9:98376. doi: 10.1371/journal.pone.0098376 CrossRefGoogle Scholar
  124. Serrazina S, Santos C, Machado H, Pesquita C, Vicentini R, Pais MS, Costa R (2015) Castanea root transcriptome in response to Phytophthora cinnamomi challenge. Tree Genet Genomes 11:1–19. doi: 10.1007/s11295-014-0829-7 CrossRefGoogle Scholar
  125. Shi L, Guttenberger M, Kottke I, Hampp R (2002) The effect of drought on mycorrhizas of beech (Fagus sylvatica L.) changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza 12:303–311PubMedCrossRefGoogle Scholar
  126. Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21:1794–1805. doi: 10.1111/j.1365-294X.2012.05538.x PubMedCrossRefGoogle Scholar
  127. Smit E, Veenman C, Baar J (2003) Molecular analysis of ectomycorrhizal basidiomycete communities in a Pinus sylvestris L. stand reveals long-term increased diversity after removal of litter and humus layers. FEMS Microbiol Ecol 45:49–57. doi: 10.1016/S0168-6496(03)00109-0 PubMedCrossRefGoogle Scholar
  128. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  129. Smith ME, Douhan GW, Rizzo DM (2007) Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytol 174:847–863. doi: 10.1111/j.1469-8137.2007.02040.x PubMedCrossRefGoogle Scholar
  130. Southworth D, Carrington EM, Frank JL, Gould P, Harrington CA, Devine WD (2009) Mycorrhizas on nursery and field seedlings of Quercus garryana. Mycorrhiza 19:149–158. doi: 10.1007/s00572-008-0222-1 PubMedCrossRefGoogle Scholar
  131. Stark S, Kytöviita M-M (2005) Evidence of antagonistic interactions between rhizosphere microorganisms and mycorrhizal fungi associated with birch (Betula pubescens). Acta Oecol 28:149–155. doi: 10.1016/j.actao.2005.03.007 CrossRefGoogle Scholar
  132. Suz LM, Barsoum N, Benham S, Dietrich H-P, Fetzer KD, Fischer R, Ia PG, Gehrman J, Gofel FK, Mannunger M, Neagu S, Nicolas M, Oldenburger J, Raspe S, Anchez GS, Schrock HW, Schubert A, Verheyen K, Verstraeten A, Bidartondo MI (2014) Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Mol Ecol 23:5628–5644. doi: 10.1111/mec.12947 PubMedCrossRefGoogle Scholar
  133. Tarkka MT, Herrmann S, Wubet T, Feldhahn L, Recht S, Kurth F, Mailänder S, Bönn M, Neef M, Angay O, Buscot F et al (2013) OakContigDF159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis. New Phytol 199:529–540. doi: 10.1111/nph.12317 PubMedCrossRefGoogle Scholar
  134. Taschen E, Sauve M, Taudiere A, Parlade J, Selosse MA, Richard F (2015) Whose truffle is this? Distribution patterns of ectomycorrhizal fungal diversity in Tuber melanosporum brûlés developed in multi-host Mediterranean plant communities. Environ Microbiol 17:2747–2761. doi: 10.1111/1462-2920.12741 PubMedCrossRefGoogle Scholar
  135. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi: 10.1007/s00572-009-0274-x PubMedCrossRefGoogle Scholar
  136. Teixeira RT, Fortes AM, Pinheiro C, Pereira H (2014) Comparison of good- and bad-quality cork: application of high-throughput sequencing of phellogenic tissue. J Exp Bot 65:4887–4905. doi: 10.1093/jxb/eru252 PubMedCrossRefGoogle Scholar
  137. Toju H, Sato H, Tanabe AS (2014) Diversity and spatial structure of belowground plant—fungal symbiosis in a mixed subtropical forest of ectomycorrhizal and arbuscular mycorrhizal plants. PLoS One 9:24–26. doi: 10.1371/journal.pone.0086566 CrossRefGoogle Scholar
  138. Valavanidis A, Vlachogianni T (2011) Ecosystems and biodiversity hotspots in the Mediterranean basin threats and conservation efforts. Sci Adv Environ Toxicol Ecotoxicol Issues 10:1–24Google Scholar
  139. Van der Heijden MGA, Martin FM, Sanders IR (2015) Tansley review Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. doi: 10.1111/nph.13288 PubMedCrossRefGoogle Scholar
  140. Vettraino AM, Barzanti GP, Bianco MC, Ragazzi A, Capretti P, Paoletti E, Luisi N, Anselmi N, Vannini A (2002) Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. For Pathol 32:19–28. doi: 10.1046/j.1439-0329.2002.00264.x Google Scholar
  141. Voříšková J, Brabcová V, Cajthaml T, Baldrian P (2014) Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201:269–278. doi: 10.1111/nph.12481 PubMedCrossRefGoogle Scholar
  142. Wang Q, Gao C, Guo L (2011) Ectomycorrhizae associated with Castanopsis fargesii (Fagaceae) in a subtropical forest. Mycol Prog 10:323–332. doi: 10.1007/s11557-010-0705-2 CrossRefGoogle Scholar
  143. Wheeler N, Sederoff R (2009) Role of genomics in the potential restoration of the American chestnut. Tree Genet Genomes 5:181–187. doi: 10.1007/s11295-008-0180-y CrossRefGoogle Scholar
  144. Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68. doi: 10.1146/annurev-phyto-102313-050222 PubMedCrossRefGoogle Scholar
  145. Yakhlef SB, Kerdouh B, Mousain D, Ducousso M, Duponnois R, Abourouh M (2009) Phylogenetic diversity of Moroccan cork oak woodlands fungi. Biotechnol Agron Soc 13:521–528Google Scholar
  146. Yun W, Hall IA (2004) Edible ectomycorrhizal mushrooms: challenges and achievements. Can J Bot 82(8):1063–1073. doi: 10.1139/b04-051 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Francisca Reis
    • 1
  • Rui M. Tavares
    • 1
  • Paula Baptista
    • 2
  • Teresa Lino-Neto
    • 1
    Email author
  1. 1.BioSystems and Integrative Sciences Institute (BioISI), Plant Functional Biology CentreUniversity of MinhoBragaPortugal
  2. 2.REQUIMTE - School of Agriculture, Polytechnic Institute of BragançaBragançaPortugal

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