Edible ectomycorrhizal fungi and Cistaceae. A study on compatibility and fungal ecological strategies

Autoři: Rui Albuquerque-Martins aff001;  Pedro Carvalho aff001;  Daniel Miranda aff001;  Maria Teresa Gonçalves aff001;  António Portugal aff001
Působiště autorů: Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226849


Wild edible mycorrhizal mushrooms are among the most appreciated and prized mushrooms in the world. Despite the cultivation of ectomycorrhizal (ECM) mushrooms has been a growing subject of study worldwide, it has been hampered by the mutualistic lifestyle of the fungi. Although not being obligate symbionts, most of the species of ECM mushrooms only produce fruit bodies in association with trees or shrubs. In the present study, we aimed at understanding certain aspects of the ecology of four different edible ECM fungi: Lactarius deliciosus, Tricholoma equestre, T. portentosum and Boletus fragrans. Despite having a broad distribution worldwide, these fungi inhabit also Mediterranean habitats with understories typically dominated by rockroses (Cistaceae). Studying the ecology of these mutualistic fungi as well as the interaction with these species of shrubs is not only scientifically relevant but also pivotal for the discovery of profitable cultivation protocols. We evaluated the compatibility of these ECM species with five species within Cistaceae family - Cistus ladanifer, C. psilosepalus, C. salviifolius, Halimium halimifolium and Tuberaria lignosa. Each species of fungi proved to be able to establish mycorrhizas with at least 2 different plants species but varied in their host range of the tested Cistaceae. The dissimilarity in terms of host specificity between some fungal species seemed to be connected with the phylogenetic distances of the fungi. A correlation between the colonization percentage of the root systems and the mycelial growth rates in pure culture was found. The connection of these traits might be an important key to understanding the ecological competitor-colonizer tradeoffs of these ECM fungal species. Altogether, our study reports unknown plant-fungi combinations with economical relevance and also adds new insights about the ecology of these species of ECM fungi.

Klíčová slova:

Fungi – Mycelium – Phylogenetic analysis – Phylogenetics – Pure culture – Species colonization – Mycorrhiza – Plant phylogenetics


1. Boa E. Local Communities and Edible Ectomycorrhizal Mushrooms. In: Zambonelli A, Bonito GM, editors. Edible Ectomycorrhizal Mushrooms: Current Knowledge and Future Prospects. Berlin, Heidelberg: Springer Berlin Heidelberg; 2012. pp. 307–315. doi: 10.1007/978-3-642-33823-6_17

2. Smith SE, Read D. Mycorrhizal Symbiosis [Internet]. Third Edit. Smith SE, Read D, editors. London: Academic Press; 2008. doi: 10.1016/B978-012370526-6.50019–2

3. Marx DH, Cordell CE. Specific ectomycorrhizae improve reforestation and reclamation in the eastern United States. Proceedings of the Canadian workshop on mycorrhizae in forestry. 1988.

4. Duddridge JA. The development and ultrastructure of ectomycorrhizas. IV. Compatible and incompatible interactions between Suillus grevillei (Klotzcsh) Sing. and a number of ectomycorrhizal hosts in vitro in the presence of exogenous carbohydrate. New Phytol. 1986;103: 465–471. doi: 10.1111/j.1469-8137.1986.tb02883.x

5. Duddridge JA. The development and ultrastructure of ectomycorrhizas. III. Compatible and incompatible interactions between Suillus grevillei (Klotzcsh) Sing. and a number of ectomycorrhizal hosts in vitro in the presence of exogenous carbohydrate. New Phytol. 1986;103: 465–471. doi: 10.1111/j.1469-8137.1986.tb02883.x

6. Mason PA, Last FT, Pelham J, Ingleby K. Ecology of some fungi associated with an ageing stand of birches (Betula pendula and B. pubescens). For Ecol Manage. 1982;4: 19–39. doi: 10.1016/0378-1127(82)90026-3

7. Mason PA, Wilson J, Last FT, Walker C. The concept of succession in relation to the spread of sheathing mycorrhizal fungi on inoculated tree seedlings growing in unsterile soils. Plant Soil. 1983;71: 247–256. doi: 10.1007/BF02182659

8. Newton A. Towards a functional classification of ectomycorrhizal fungi. Mycorrhiza. 1992; 75–79. Available: http://eprints.bournemouth.ac.uk/12276/1/licence.txt

9. Taylor DL, Bruns T. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the …. Mol Ecol. 1999; 1837–1850. Available: http://www.blackwell-synergy.com/doi/abs/10.1046/j.1365-294x.1999.00773.x%5Cnpapers2://publication/uuid/F7611421-85E2-46DD-9770-B5C603239AFB doi: 10.1046/j.1365-294x.1999.00773.x 10620228

10. Townsend CR, Begon M, Harper JL. Essentials of Ecology, 3rd. Massachusetts MA. 2008;

11. Kennedy PG, Higgins LM, Rogers RH, Weber MG. Colonization-competition tradeoffs as a mechanism driving successional dynamics in ectomycorrhizal fungal communities. PLoS One. 2011;6. doi: 10.1371/journal.pone.0025126 21949867

12. Barros L, Grangeia C, Martins A, Ferreira ICFR. Nutritional and nutraceutical potential of saprotrophic and mycorrhizal wild edible mushrooms from Northeast Portugal. International PSE Symposium on “Phytochemicals in Nutrition and Health.” Phytochemical Society of Europe; 2011.

13. Ferreira ICFR, Vaz J a, Vasconcelos MH, Martins A. Compounds from wild mushrooms with antitumor potential. Anticancer Agents Med Chem. 2010;10: 424–436. doi: 10.2174/1871520611009050424 20545620

14. Kalač P. Chemical composition and nutritional value of European species of wild growing mushrooms: A review. Food Chem. 2009;113: 9–16. doi: 10.1016/j.foodchem.2008.07.077

15. Rzymski P, Klimaszyk P. Is the Yellow Knight Mushroom Edible or Not? A Systematic Review and Critical Viewpoints on the Toxicity of Tricholoma equestre. Compr Rev Food Sci Food Saf. 2018;17: 1309–1324. doi: 10.1111/1541-4337.12374

16. Ortega-Martínez P, Águeda B, Fernández-Toirán LM, Martínez-Peña F. Tree age influences on the development of edible ectomycorrhizal fungi sporocarps in Pinus sylvestris stands. Mycorrhiza. 2011;21: 65–70. doi: 10.1007/s00572-010-0320-8 20524015

17. Kennedy P. Ectomycorrhizal fungi and interspecific competition: Species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol. 2010;187: 895–910. doi: 10.1111/j.1469-8137.2010.03399.x 20673286

18. Molina R, Massicotte H, Trappe JM. Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. Mycorrhizal Funct an Integr plant-fungal Process. 1992;357: e423.

19. Águeda B, Parladé J, de Miguel AM, Martínez-Peña F. Characterization and identification of field ectomycorrhizae of Boletus edulis and Cistus ladanifer. Mycologia. 2006;98: 23–30. doi: 10.1080/15572536.2006.11832709 16800301

20. Muñoz-Garmendía F, Navarro C. Cistaceae. Flora Iber. 1993;3: 318–436.

21. Comandini O, Contu M, Rinaldi AC. An overview of Cistus ectomycorrhizal fungi. Mycorrhiza. 2006;16: 381–395. doi: 10.1007/s00572-006-0047-8 16896800

22. Carvalho P, Martins R, Portugal A, Gonçalves MT. Do mycorrhizal fungi create below-ground links between native plants and Acacia longifolia? A case study in a coastal maritime pine forest in Portugal. 2018; 105–114.

23. Zaretsky M, Kagan-Zur V, Mills D, Roth-Bejerano N. Analysis of mycorrhizal associations formed by Cistus incanus transformed root clones with Terfezia boudieri isolates. Plant Cell Rep. 2006;25: 62–70. doi: 10.1007/s00299-005-0035-z 16322996

24. Oria De Rueda JA, Martín-Pinto P, Olaizola J. Bolete productivity of Cistaeous scrublands in Northwestern Spain. Econ Bot. 2008;62: 323–330.

25. Zitouni-Haouar FEH, Fortas Z, Chevalier G. Morphological characterization of mycorrhizae formed between three Terfezia species (desert truffles) and several Cistaceae and Aleppo pine. Mycorrhiza. 2014;24: 397–403. doi: 10.1007/s00572-013-0550-7 24384787

26. Taudiere A, Munoz F, Lesne A, Monnet A-C, Bellanger J-M, Selosse M-A, et al. Beyond ectomycorrhizal bipartite networks: projected networks demonstrate contrasted patterns between early- and late-successional plants in Corsica. Front Plant Sci. 2015;6: 1–14. doi: 10.3389/fpls.2015.00001

27. Wenkart S, Roth-Bejerano N, Mills D, Kagan-Zur V. Mycorrhizal associations between Tuber melanosporum mycelia and transformed roots of Cistus incanus. Plant Cell Rep. 2001;20: 369–373. doi: 10.1007/s002990100325

28. Giovannetti G, Fontana A. Mycorrhizal Synthesis Between cistaceae and tuberaceae. New Phytol. 1982;92: 533–537.

29. Bustan A, Ventura Y, Kagan-Zur V, Roth-Bejerano N. Optimized conditions for mycorrhiza formation between the pink rockrose (Cistus incanus) and the black Perigord truffle (Tuber melanosporum). Isr J Plant Sci. 2006;54: 87–96. doi: 10.1560/IJPS_54_2_87

30. Águeda B, Parladé J, Fernández-Toirán LM, Cisneros Ó, De Miguel AM, Modrego MP, et al. Mycorrhizal synthesis between Boletus edulis species complex and rockroses (Cistus sp.). Mycorrhiza. 2008;18: 443–449. doi: 10.1007/s00572-008-0192-3 18695982

31. Bordallo J-J, Rodríguez A, Muñoz-Mohedano JM, Suz LM, Honrubia M, Morte A. Five new Terfezia species from the Iberian Peninsula. Mycotaxon. 2013;124: 189–208.

32. Kovacs GM, Balazs TK, Calonge FD, Martin MP. The diversity of Terfezia desert truffles: new species and a highly variable species complex with intrasporocarpic nrDNA ITS heterogeneity. Mycologia. 2011;103: 841–853. doi: 10.3852/10-312 21289106

33. Moreno G, Manjón JL. Guía de hongos de la Península Ibérica. Ediciones Omega. 2010;

34. Roger P. Mushrooms and other fungi of Great Britain and Europe. Pan Books, London; 1981.

35. Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes, application to the identification of mycorrihiza and rusts. Mol Ecol. 1993;2: 113–118. doi: 10.1111/j.1365-294x.1993.tb00005.x 8180733

36. White TJ, Bruns T, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc a Guid to methods Appl. 1990;18: 315–322.

37. Guindon S, Gascuel O. A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Syst Biol. 2003;52: 696–704. doi: 10.1080/10635150390235520 14530136

38. Posada D. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 2008;25: 1253–1256. doi: 10.1093/molbev/msn083 18397919

39. Sánchez R, Serra F, Tárraga J, Medina I, Carbonell J, Pulido L, et al. Phylemon 2.0: A suite of web-tools for molecular evolution, phylogenetics, phylogenomics and hypotheses testing. Nucleic Acids Res. 2011;39: 470–474. doi: 10.1093/nar/gkr408 21646336

40. Rambaut A. FigTree v1. 4. 2012.

41. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 1962;15: 473–497.

42. Agerer R, Rambold G. (2004–2008) [first posted on 2004-06-01; most recent update: 2007-05-02]. DEEMY—An information system for characterization and determination of Ectomycorrhizae. www.deemy.de—München, Germany [Internet].

43. Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc. 1970;55: 158–IN18.

44. Team RDC. R Development Core Team R. R: A Language and Environment for Statistical Computing. 2005; 1 (2.11. 1): 409. doi: 10.1007

45. Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14: 927–930.

46. Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, et al. Package ‘car.’ Vienna R Found Stat Comput. 2012;

47. Wickham H. ggplot2: elegant graphics for data analysis. Springer; 2016.

48. Moser M. Die Gattung Phlegmacium. Die Pilze Mitteleuropas. 1960;4: 134–135.

49. Lavorato C. Chiave analitica e note bibliografiche della micoflora del cisto. Assoc Micol Ecol Rom. 1991;24: 16–45.

50. Zervakis G, Dimou D, Balis C. A check-list of the Greek macrofungi including hosts and biogeographic distribution: 1. Basidiomycotina. Mycotaxon. 2010; 273–336.

51. Vila J, Llimona X. Noves Dades Sobre El Component Fúngic De Catalunya. Rev Catalana Micol. 2002;24: 75–121.

52. Guerin-Laguette a, Plassard C, Mousain D. Effects of experimental conditions on mycorrhizal relationships between Pinus sylvestris and Lactarius deliciosus and unprecedented fruit-body formation of the Saffron milk cap under controlled soilless conditions. Can J Microbiol. 2000;46: 790–799. doi: 10.1139/w00-059 11006839

53. Díaz G, Carrillo C, Honrubia M. Production of Pinus halepensis seedlings inoculated with the edible fungus Lactarius deliciosus under nursery conditions. New For. 2009;38: 215–227. doi: 10.1007/s11056-009-9142-y

54. Yamada A, Ogura T, Ohmasa M. Cultivation of mushrooms of edible ectomycorrhizal fungi associated with Pinus densiflora by in vitro mycorrhizal synthesis 1. Primordium and basidiocarp formation in open-pot culture. Mycorrhiza. 2001;11: 59–66. doi: 10.1007/s005720000093

55. Yamada A, Kobayashi H, Ogura T, Fukada M. Sustainable fruit-body formation of edible mycorrhizal Tricholoma species for 3 years in open pot culture with pine seedling hosts. Mycoscience. 2007;48: 104–108. doi: 10.1007/s10267-006-0338-0

56. Rodríguez A, de Ana Magán FJF. Evolución de una colonia de un hongo ectomicorrícico, Boletus fragans, bajo castaños híbridos. Congresos Forestal Español. 1993.

57. Guzmán B, Lledó MD, Vargas P. Adaptive radiation in Mediterranean Cistus (Cistaceae). PLoS One. 2009;4. doi: 10.1371/journal.pone.0006362 19668338

58. Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M. A strong species-area relationship for eukaryotic soil microbes: Island size matters for ectomycorrhizal fungi. Ecol Lett. 2007;10: 470–480. doi: 10.1111/j.1461-0248.2007.01035.x 17498146

59. Hilszczańska D, Sierota Z. Persistence of ectomycorrhizas by Thelephora terrestris on outplanted Scots pine seedlings. Acta Mycol. 2013;41: 313–318. doi: 10.5586/am.2006.032

60. Selosse MA, Jacquot D, Bouchard D, Martin F, Le Tacon F. Temporal persistence and spatial distribution of an American inoculant strain of the ectomycorrhizal basidiomycete Laccaria bicolor in a French forest plantation. Mol Ecol. 1998;7: 561–573. doi: 10.1046/j.1365-294x.1998.00353.x

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