Abstract
Developing the production of ectomycorrhizal (ECM) mushrooms in forest has become a challenge. Only a few ECM species are currently cultivable. Controlled mycorrhization practices offer promising advance to produce currently uncultivable ECM mushrooms. The persistence of the production of edible species, either cultivated or wild, depends on both the tree and the ecological environment (fungal communities, climate, soil, tree development). Developing adapted forest management practices appears to be means to improve production of edible ECM mushrooms. This review summarises current knowledge on the development of a science-based mycosilviculture for the production of edible ECM mushrooms.
Similar content being viewed by others
References
Águeda B, Parladé J, Fernández-Toirán L, Cisneros O, de Miguel AM, Modrego MP, Martínez-Peña F, Pera J (2008) Mycorrhizal synthesis between Boletus edulis species complex and rockroses (Cistus sp.). Mycorrhiza 18:443–449
Arnolds E (1991) Decline of ectomycorrhizal fungi in Europe. Agric Ecosyst Environ 35:209–244
Aspray TJ, Jones EJ, Whipps JM, Bending GD (2006) Importance of mycorrhization helper bacteria cell density and metabolite localization for the Pinus sylvestris–Lactarius rufus symbiosis. FEMS Microbiol Ecol 56:25–33
Baar J, Kuyper TW (1998) Restoration of aboveground ectomycorrhizal flora in stands of Pinus sylvestris (Scots pine) in the Netherlands by removal of litter and humus. Restor Ecol 6:227–237
Bonet JA, Fischer CR, Colinas C (2004) The relationship between forest age and aspect on the production of sporocarps of ectomycorrhizal fungi in Pinus sylvestris forests of the central Pyrenees. For Ecol Manage 203:157–175
Bonet JA, Oliach D, Fischer C, Olivera A, Martinez de Aragon J, Colinas C (2007) Cultivation methods of the black truffle, the most profitable Mediterranean non-wood forest product. In: Palahi M, Birot Y, Bravo F, Gorriz E (eds) A State of the Art Review Conference Information: 1st Annual Meeting of the Modelling, Valuing and Managing Mediterranean Forest Ecosystems for Non-Timber Goods and Services, 26–27 October, Palencia, Spain. Book Series: European Forest Institute Proceedings 57:57–71
Bonet JA, Pukkala T, Fischer C, Palahí M, Martínez de Aragon J, Colinas C (2008) Empirical models for predicting the production of wild mushrooms in Scots pine (Pinus sylvestris L.) forests in the Central Pyrenees. Ann For Sci 65(2):206
Bonet JA, Palahí M, Colinas C, Pukkala T, Fischer C, Miina J, Martínez de Aragon J (2010) Modelling the production and species richness of wild mushrooms in pine forests of the Central Pyrenees in northeastern Spain. Can J For Res 40:347–356
Brulé C, Frey-Klett P, Pierrat JC, Courrier S, Gérard F, Lemoin MC, Rousselet JL, Sommer J, Garbaye J (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and effect of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33:1683–1694
Chang ST (1993) Mushroom biology: the impact on mushroom production and mushroom products. In: Chang ST, Buswell JA, Chiu SW (eds) Mushroom biology and mushroom products. The Chinese University Press, Hong-Kong, pp 3–20
Chang ST, Miles PG (1992) Mushroom biology, a new discipline. Mycologist 6:64–65
Courty PE, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698
Danell E (2002) Current research on chanterelle cultivation in Sweden; Edible mycorrhizal mushrooms and their cultivation. In: Hall IR, Wang Y, Danell E, Zambonelli A (eds) Proc. 2nd Int. Conf. Edible Mycorrhizal Mushrooms, New Zealand Inst. Crop & Food Research Limited, Christchurch
Danell E, Camacho FJ (1997) Successful cultivation of the golden chanterelle. Nature 385:303
Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755
Díez J, Manjón JL, Martin F (2002) Molecular phylogeny of the mycorrhizal desert truffles (Terfezia and Tirmania), host specificity and edaphic tolerance. Mycologia 94:247–259
Dighton J, Mason PA (1985) In: Moore D, Casselton LA, Wood DA, Frankland JC (eds) Mycorrhizal dynamics during forest tree development. In Developmental biology of higher fungi. Cambridge University Press, Cambridge, pp 117–140
Donnini D, Baciarelli Falini L, Bencivenga M (2001) Analisi della micorrizazione in tartufaie coltivate di Tuber melanosporum Vittad. impiante da oltre 12 anni in ambient pedoclimatici diversi. Proc. 5th Int. Congress on Science and Cultivation of Truffles, Aix-en-Provence, FFT, Paris, France, pp 437–440
Duñabeitia M, Rodríguez N, Salcedo I, Sarrionandia E (2004) Field mycorrhization and its influence on the establishment and development of the seedlings in a broadleaf plantation in the Basque Country. For Ecol Manage 195:129–139
Duponnois R, Garbaye J (1991) Techniques for controlled synthesis of Douglas-Fir—Laccaria laccata ectomycorrhizal symbiosis. Ann Sci For 48:641–650
Egli S, Ayer F, Peter M, Eilmann B, Rigling A (2010) Is forests mushroom productivity driven by tree growth? Results from a thinning experiment. Ann For Sci 67:509p1–509p9
Fangfuk W, Okada K, Petchang R, To-anun C, Fukuda M, Yamada A (2010) In vitro mycorrhization of edible Astraeus mushrooms and their morphological characterization. Mycoscience 51:234–241
Ford ED, Mason PA, Pelham J (1980) Spatial patterns of sporophore distribution around a young birch tree in three successive years. Trans Br Mycol Soc 75:287–296
Fortas Z, Chevalier G (1992) Effet des conditions de culture sur la mycorrhization de l'Helianthemum guttatum par trios espèces de terfez des genres Terfezia et Tirmania d'Algérie. Can J Bot 70:2453–2460
Founoune H, Duponnois R, Bâ AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL (2002) Mycorrhiza helper bacteria stimulate ectomycorrhizal symbiosis of Accacia holoserica with the Pisolithus albus. New Phytol 153:81–89
Frankland JC (1998) Fungal succession—unraveling the unpredictable. Mycol Res 102:1–15
Frey-Klett P, Pierrat J-C, Garbaye J (1997) Location and survival of mycorrhizal helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Appl Environ Microbiol 63:139–144
Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210
Garbaye J, Duponnois R (1992) Specificity and function of mycorrhization helper bacteria (MHB) associated with the Pseudotsuga menziesii–Laccaria laccata symbiosis. Symbiosis 14:335–344
García-Montero LG, Díaz P, Martín-Fernández S, Casermeiro MA (2008) Soil factors that favour the production of Tuber melanosporum carpophores over other truffle species: a multivariate statistical approach. Acta Agric Scand B Plant Soil Sci 58:322–329
Grente J, Delmas J (1974) Perspectives pour une Trufficulture Moderne, 3rd edn. Inst. Natl. Rech. Agric. Stn. Pathol. Veg., Clermont-Ferrand, 65 pp
Guerin-Laguette A, Plassard C, Mousain D (2000) Effects of experimental conditions on mycorrhizal relationships between Pinus sylvestris and Lactarius deliciosus and unprecedent fruit-body formation of the Saffron milk cap under controlled soiless conditions. Can J Microbiol 46:790–799
Guinberteau J, Ducamp M, Poitou N, Mamoun M, Olivier JM (1989) Ecology of various competitors from an experimental plot of Pinus pinaster inoculated with Suillus granulatus and Lactarius deliciosus. Agric Ecosyst Environ 28:161–165
Hall IR, Wang Y, Amicucci A (2003) Cultivation of edible ectomycorrhizal mushrooms. Trends Biotechnol 21:433–438
Hortal S, Pera J, Parladé J (2009) Field persistence of the edible ectomycorrhizal fungus Lactarius deliciosus: effect of inoculation strain, initial colonization level, and site characteristics. Mycorrhiza 19:167–177
Ishida TA, Nara K, Tanaka M, Kinoshita A, Hogetsu T (2008) Germination and infectivity of ectomycorrhizal fungal spores in relation to their ecological traits during primary succession. New Phytol 180:491–500
Kataoka R, Taniguchi T, Futai K (2009) Fungal selectivity of two mycorrhiza helper bacteria on five mycorrhizal fungi associated with Pinus thunbergii. World J Microbiol Biotechnol 25:1815–1819
Kendrick B (1985) The fifth kingdom. Mycologue, Waterloo, p 364
Kües U, Liu Y (2000) Fruiting body production in basidiomycetes. Appl Micriobol Biotechnol 54:141–152
Last FT, Natarajan K, Mohan V, Mason PA (1992) Sequences of sheathing (ecto-) mycorrhizal fungi associated with man-made forests, temperate and tropical. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 214–219
Le Tacon F, Alvarez IF, Bouchard D, Henrion B, Jackson RM, Luff S, Parlade JI, Pera J, Sternström E, Villeneuve N, Walker C (1992) Variations in field responses of forest trees to nursery ectomycorrhizal inoculation in Europe. In: Read DJ, Lewis DH, Lewis AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 119–134
Lotti M, Lancellotti E, Hall I, Zambonelli A (2010) The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiol Ecol 72:250–260
Malençon G (1938) Les truffes européennes. Rev Mycol 3:1–92
Mamoun M, Olivier JM (1996) Receptivity of cloned hazels to artificial ectomycorrhizal infection by Tuber melanosporum and symbiotic competitors. Mycorrhiza 6:15–19
Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury J-M, Ballario P, Bolchi A, Brenna A, Brun A, Buée M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marçais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun M-H, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038
Martínez de Aragón J, Bonet JA, Fischer CR, Colinas C (2007) Productivity of ectomycorrhizal and selected edible saprotrophic fungi in pine forests of the pre-Pyrenees mountains, Spain: predictive equations for forest management of mycological resources. For Ecol Manage 252:239–256
Mello A, Miozzi L, Vizzini A, Napoli C, Kowalchuk G, Bonfante P (2010) Bacterial and fungal communities associated with Tuber magnatum-productive niches. Plant Biosyst 144:323–332
Meotto F, Pellegrino S, Bounous G (1999) Evolution of Amanita caesarea (Scop.:Fr.) and Boletus edulis Bull.:Fr. synthetic ectomycorrhizae on European chestnut (Castanea sativa Mill.) seedlings under field conditions. Acta Hortic 494:201–206
Morte A, Lovisolo C, Schubert A (2000) Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense–Terfezia claveryi. Mycorrhiza 10:115–119
Olivier JM (2000) Progress in the cultivation of truffles. In: Van Griensven LJLD (ed) Science and cultivation of edible fungi. A.A. Balkema, Rotterdam, pp 937–942
Olivier J-M, Guinberteau J, Rondet J, Mamoun M (1997) Vers l'inoculation contrôlée des cèpes et bolets comestibles? Rev For Fr Special Issue 222–234
Oria-de-Rueda JA, Martin-Pinto P, Olaizola J (2008) Bolete productivity of cistaceous scrublands in Northwestern Spain. Econ Bot 62:323–330
Oria-de-Rueda JA, Hernández-Rodríguez M, Martín-Pinto P, Pando V, Olaizola J (2010) Could artificial reforestations provide as much production and diversity of fungal species as natural forest stands in marginal Mediterranean areas? For Ecol Manage 260:171–180
Otha A (1994) Production of fruit-bodies of a mycorrhizal fungus, Lyophyllum shimeji. Mycoscience 35:83–87
Parladé J, Pera J, Luque J (2004) Evaluation of mycelial inocula of edible Lactarius species for the production of Pinus pinaster and P. sylvestris mycorrhizal seedlings under greenhouse conditions. Mycorrhiza 14:171–176
Peintner U, Lotti 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
Pilz D, Molina R, Mayo J (2006) Effects of thinning young forests on chanterelle mushroom production. J Forest 104:9–14
Poitou N, Mamoun M, Ducamp M, Delmas J (1984) After Boletus granulatus, Lactarius deliciosus obtained in fructification in the field from mycorrhizal plants. Rev Hortic 244:65–68
Poitou N, Mamoun M, Ducamp M, Guinberteau J, Olivier JM (1989) Controlled mycorrhization and experimental cultivation in the field of Boletus (=Suillus) granulatus and Lactarius deliciosus. Mush Sci 12:551–564
Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestris–Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:743–751
Rana GL, Sisto D, de Gioia T, Ubaldo D (2007) Up-to-date acquirements on hypogeous fungi of Apulia region (southern Italy). Micologia italiana 36:53–57
Rao CS, Sharma GD, Shukla AK (1997) Distribution of ectomycorrhizal fungi in pure stands of different age groups of Pinus kesiya. Can J Microbiol 43:85–91
Riedlinger J, Schrey S, Tarkka M, Hampp R, Kapur M, Fielder HP (2006) Auxofuran, a novel metabolite that stimulate the growth of fly agaric, is produced by the mycorrhiza helper bacterium Steptomyces strain AcH 505. Appl Environ Microbiol 72:3350–3557
Rincon A, Alvarez IF, Pera J (1999) Ectomycorrhizal fungi of Pinus pinea L. in northeastern Spain. Mycorrhiza 8:271–276
Rineau F, Maurice JP, Nys C, Voiry H, Garbaye J (2010) Forest liming durably impact the communities of ectomycorrhizas and fungal epigeous fruiting bodies. Ann For Sci 67:110
Román M, Boa E (2006) The marketing of Lactarius deliciosus in northern Spain. Econ Bot 60:284–290
Rossi MJ, Furigo A, Oliveira VL (2007) Inoculant production of ectomycorrhizal fungi by solid and submerged fermentations. Food Technol Biotechnol 45:277–286
Salerni E, Perini C (2004) Experimental study for increasing productivity of Boletus edulis s.l. in Italy. For Ecol Manag 201:161–170
Schrey S, Schelhammer M, Ecke M, Hampp R, Tarkka M (2005) Mycorrhiza helper bacterium Steptomyces AcH 505 induces diffential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216
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
Smith JE, Molina R, Huso MMP, Luoma DL, McKay D, Castellano MA, Lebel T, Valachovic Y (2002) Species richness, abundance and composition of hypogeous and epigeous ectomycorrhizal fungal sporocarps in young, rotation-age, and old-growth stands of Douglas-fir (Pseudotsuga menziesii) in the Cascade Range of Oregon, USA. Can J Bot 80:186–204
Sourzat P, Sanchez A, Ourzick A, Roux JJ (2001) Analyse du statut mycorhizien de brûlés stériles dans trois régions de France: Midi-Pyrénées (Lot), PACA (Var), Charente-Poitou (Vienne). Proc. 5th Int. Congress on Science and Cultivation of Truffles, Aix-en-Provence, FFT, Paris, France, pp 474–479
Taylor AFS, Alexander IJ (1990) Demography and population dynamics of ectomycorrhizas of Stika spruce fertilised with nitrogen. Agric Ecosyst Environ 28:493–496
Tonkin CM, Malajczuk N, McComb JA (1989) Ectomycorrhizal formation by micropropagated clones of Eucalyptus marginata inoculated with isolates of Pisolithus tinctorius. New Phytol 111:209–214
Torres P, Honrubia M (1994) Ectomycorrhizal associations proven for Pinus halepensis. Isr J Plant Sci 42:51–58
Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447
Van der Heijden EW, Kuyper TW (2001) Does origin of mycorrhizal fungus or mycorrhizal plant influence effectiveness of the mycorrhizal symbiosis? Plant Soil 230:161–174
Van Griensven LJLD (2008) Mushrooms: cause and cure. In: Lelley JI, Buswell JA (eds) Proceedings of the 6th International Conference on Mushroom Biology and Mushroom Products, Höntges Quickdruck, Krefeld, pp 1–7
Vidović SS, Mujić IO, Zeković ZP, Lepojević ŽD, Tumbas VT, Mujić AI (2010) Antioxidant properties of selected Boletus mushrooms. Food Biophys 5:49–58
Wang Y, Hall IR (2004) Edible ectomycorrhizal mushrooms: challenges and achievements. Can J Bot 82:1063–1073
Yamada A, Ogura T, Ohmasa M (2001) Cultivation of mushrooms of edible ectomycorrhizal fungi associated with Pinus densiflora by in vitro mycorrhizal synthesis. Mycorrhiza 11:59–66
Yamada A, Maeda K, Kobayashi H, Murata H (2006) Ectomycorrhizal symbiosis in vitro between Tricholoma matsutake and Pinus densiflora seedlings that resembles naturally occurring ‘shiro’. Mycorrhiza 16:111–116
Acknowledgments
We thank our colleague J. Guinberteau for providing information on Boletus edulis production and his unpublished data.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Savoie, JM., Largeteau, M.L. Production of edible mushrooms in forests: trends in development of a mycosilviculture. Appl Microbiol Biotechnol 89, 971–979 (2011). https://doi.org/10.1007/s00253-010-3022-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-010-3022-4