Advertisement

Mycorrhiza

, Volume 26, Issue 2, pp 161–168 | Cite as

Mycorrhization between Cistus ladanifer L. and Boletus edulis Bull is enhanced by the mycorrhiza helper bacteria Pseudomonas fluorescens Migula

  • Olaya Mediavilla
  • Jaime Olaizola
  • Luis Santos-del-Blanco
  • Juan Andrés Oria-de-Rueda
  • Pablo Martín-PintoEmail author
Original Article

Abstract

Boletus edulis Bull. is one of the most economically and gastronomically valuable fungi worldwide. Sporocarp production normally occurs when symbiotically associated with a number of tree species in stands over 40 years old, but it has also been reported in 3-year-old Cistus ladanifer L. shrubs. Efforts toward the domestication of B. edulis have thus focused on successfully generating C. ladanifer seedlings associated with B. edulis under controlled conditions. Microorganisms have an important role mediating mycorrhizal symbiosis, such as some bacteria species which enhance mycorrhiza formation (mycorrhiza helper bacteria). Thus, in this study, we explored the effect that mycorrhiza helper bacteria have on the efficiency and intensity of the ectomycorrhizal symbiosis between C. ladanifer and B. edulis. The aim of this work was to optimize an in vitro protocol for the mycorrhizal synthesis of B. edulis with C. ladanifer by testing the effects of fungal culture time and coinoculation with the helper bacteria Pseudomonas fluorescens Migula. The results confirmed successful mycorrhizal synthesis between C. ladanifer and B. edulis. Coinoculation of B. edulis with P. fluorescens doubled within-plant mycorrhization levels although it did not result in an increased number of seedlings colonized with B. edulis mycorrhizae. B. edulis mycelium culture time also increased mycorrhization levels but not the presence of mycorrhizae. These findings bring us closer to controlled B. edulis sporocarp production in plantations.

Keywords

MHB Mycelium culture Mycorrhizal plants Sporocarps Ectomycorrhizal fungi cultivation 

Notes

Acknowledgments

This study was partially funded by the research project VA206U13 (Junta de Castilla y León). We would like to thank Dr. Valentin Pando (Department of Statistics, University of Valladolid) for the statistical support. We would also like to thank Alfonso Centeno (University of Valladolid), Fernando Fernández (Director of Ecology and Environmental Consultants Ireland Ltd.), and María Hernández Rodríguez (PhD Student, University of Valladolid) for helping to significantly improve the document.

References

  1. Agerer R (1991) Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Techniques for the study of mycorrhiza, Methods in. Academic Press, London, pp 25–73CrossRefGoogle Scholar
  2. Águeda B, Parladé J, Fernández-Toirán LM et al (2008) Mycorrhizal synthesis between Boletus edulis species complex and rockroses (Cistus sp.). Mycorrhiza 18:443–449CrossRefPubMedGoogle Scholar
  3. Aspray TJ, Frey-Klett P, Jones JE, Whipps JM, Garbaye J, Bending JD (2006) Mycorrhization helper bacteria: a case of specificity for altering ectomycorrhiza architecture but not ectomycorrhiza formation. Mycorrhiza 16:533–541CrossRefPubMedGoogle Scholar
  4. Boa E (2004) Wild edible fungi: A global overview of their use and importance to people. Non-wood Forest Products No17. FAO, Rome, pp 1–147Google Scholar
  5. Bonet JA, Oliach D, Fischer CR, Olivera A, Martinez de Aragón J, Colinas C (2009) Cultivation methods of the black truffle, the most profitable mediterranean non-wood forest product; a state of the art review. In: Palahí M, Birot Y, Bravo F, Gorriz E (eds) Modeling, valuing and managing Mediterraneam forests ecosystems for non-timber goods and services. EFI Procedings, pp 57–71Google Scholar
  6. Brulé C, Frey-Klett P, Pierrat JC et al (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and the effects of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33:1683–1694CrossRefGoogle Scholar
  7. Cannon PF, Kirk PM (2007) Fungal families of the world. CAB International, Wallingford, Oxfordshire, UKGoogle Scholar
  8. Catcheside PS, Catcheside DEA (2012) Boletus edulis (Boletaceae), a new record for Australia. J Adelaide Bot Gard 25:5–10Google Scholar
  9. De Oliveira VL, Garbaye J (1989) Les microorganisms auxiliaires de l’établissement des symbioses ectomycorrhiziennes. Eur J For Pathol 19:54–64CrossRefGoogle Scholar
  10. Dentinger BTM, Ammirati JF, Both EE et al (2010) Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). Mol Phylogenet Evol 57:1276–1292CrossRefPubMedGoogle Scholar
  11. Díaz-Balteiro L, Álvarez-Nieto A, Oria-de-Rueda JA (2003) Integración de la producción fúngica en la gestión forestal. Aplicación al monte «Urcido» (Zamora). Investig Agrar Sist Recur For 12:5–19Google Scholar
  12. Diez J, Manjón JL, Kovács GM, Celestino C, Toribio M (2000) Mycorrhization of vitroplants raised from somatic embryos of cork oak (Quercus suber L.). Appl Soil Ecol 15:119–123CrossRefGoogle Scholar
  13. Dominguez JA, Martin A, Anriquez A, Albanesi A (2012) The combined effects of Pseudomonas fluorescens and Tuber melanosporum on the quality of Pinus halepensis seedlings. Mycorrhiza 22:429–436CrossRefPubMedGoogle Scholar
  14. Duponnois R (2006) Bacteria helping mycorrhiza development. In: Mukerji KG, Manoharachary J (eds) Soil Biology. Springer- Verlag, Berlin, GermanyGoogle Scholar
  15. Duponnois R (1992) Les bactéries auxiliaires de la mycorhization du Douglas (Pseudotsuga menziesii (Mirb.) Franco) par Laccaria laccata souche S238. PhD thesis, Université de Nancy I, FranceGoogle Scholar
  16. Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with the Douglas fir-Laccaria laccata symbiosis : effects in aseptic and in glasshouse conditions. Ann Sci 48:239–251CrossRefGoogle Scholar
  17. Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13:85–91CrossRefPubMedGoogle Scholar
  18. Fischer C, Colinas C (1997) Propuesta de metodología para la certificación de planta de Quercus ilex inoculada con Tuber melanosporum para la aplicación comercial. Departamento de Investigación Forestal de Valonsadero, Soria, SpainGoogle Scholar
  19. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36CrossRefPubMedGoogle Scholar
  20. Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  21. Garbaye J, Bowen GD (1989) Stimulation of ectomycorrhizal infection of Pinus radiata by some microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388CrossRefGoogle Scholar
  22. Garbaye J, Bowen GD (1987) Effect of different microflora on the success of mycorrhizal inoculation of Pinus radiata. Can J For Res 17:941–943CrossRefGoogle Scholar
  23. Garbaye J, Duponnois R, Wahl JL (1990) The bacteria associated with Laccaria laccata ectomycorrhizas or sporocarps: effect of symbiosis establishment on Douglas fir. Symbiosis 9:267–273Google Scholar
  24. 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 soilless conditions. Can J Microbiol 46:790–799CrossRefPubMedGoogle Scholar
  25. Hall IR, Lyon JE, Sinclair L (1998) Ectomycorrhizal fungi with edible fruiring bodies. Boletusedulis. Econ Bot 52:44–56CrossRefGoogle Scholar
  26. Honrubia M, Díaz G, Gutiérrez A (1997) Micorrización controlada de Pinus halepensis en vivero en función del tipo de inóculo y técnicas de cultivo. I Congreso Forestal Hispano Luso, Pamplona, pp 301–306Google Scholar
  27. Honrubia M, Torres P, Diaz G, Morte A (1994) Biotecnología forestal: Técnicas de micorrización y micropropagación de plantasGoogle Scholar
  28. Iriondo JM, Moreno C, Pérez C (1995) Micropropagation of six rockrose (Cistus) species. Hortic Sci 30:1080–1081Google Scholar
  29. 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 25:1815–1819CrossRefGoogle Scholar
  30. Kurth F, Zeitler K, Feldhahn L, Neu TR, Weber T, Krištůfek V, Wubet T, Herrmann S, Buscot F, Tarkka M (2013) Detection and quantification of a mycorrhization helper bacterium and a mycorrhizal fungus in plant-soil microcosms at different levels of complexity. BMC Microbiol 13:205PubMedCentralCrossRefPubMedGoogle Scholar
  31. M’Kada J, Dorion N, Bigot C (1991) In vitro propagation of Cistus × purpureus Lam. Sci Hortic (Amsterdam) 46:155–160CrossRefGoogle Scholar
  32. Madesis P, Konstantinidou E, Tsaftaris A, Nianiou-Obeidat I (2011) Micropropagation and shoot regeneration of Cistus creticus ssp. Creticus. J Appl Pharm Sci 1:54–58Google Scholar
  33. Martín-Pinto P, Vaquerizo H, Peñalver F, Olaizola J, Oria-de-Rueda JA (2006) Early effects of a wildfire on the diversity and production of fungal communities in Mediterranean vegetation types dominated by Cistus ladanifer and Pinus pinaster in Spain. For Ecol Manag 225:296–305CrossRefGoogle Scholar
  34. Marx D (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163Google Scholar
  35. Mello A, Ghignone S, Vizzini A, Sechi C, Ruiu P, Bonfante P (2006) ITS primers for the identification of marketable boletes. J Biotechnol 121:318–329CrossRefPubMedGoogle Scholar
  36. Morte A, Honrubia M (1992) In vitro propagation of Helianhthemum almeriense Pau (Cistaceae). Agronomie 12:807–809CrossRefGoogle Scholar
  37. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479CrossRefGoogle Scholar
  38. Olaizola J (2007) Selección de hongos ectomicorrícicos comestibles para su utilización en el control biológico del damping-off causado por Fusarium oxysporum Schlecht y Fusarium verticillioides (Sacc.) Nirenberg. PhD thesis. Universidad de Valladolid, SpainGoogle Scholar
  39. Olivier JM, Guinberteau J, Rondet J, Mamoun M (1997) Vers l’inoculation contrôlée des cèpes et bolets comestibles? Rev Fr 49:222–234CrossRefGoogle Scholar
  40. Oria-de-Rueda JA, Martin-Pinto P, Olaizola J (2005) Boletus edulis production in xerophilic and pirophitic shrubs of Cistus ladanifer and Halimiumlasianthum in western Spain. IV International Workshop on Edible Mycorrhizal MushroomsGoogle Scholar
  41. Oria-de-Rueda JA, Martín-Pinto P, Olaizola J (2008) Bolete productivity of cistaceous scrublands in Northwestern Spain. Econ Bot 62:323–330CrossRefGoogle Scholar
  42. 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 171–176Google Scholar
  43. Pela Z, Pencheva M, Gerasopoulos D, Maloupa E (2000) In vitro induction of adventitious roots and proliferation of Cistus creticous creticous plants. Acta Hortic 541:518–524Google Scholar
  44. Pera J, Parladé J (2005) Inoculación controlada con hongos ectomicorrícicos en la producción de planta destinada a repoblaciones forestales : estado actual en España. Investig Agrar Sist Recur For 14:419–433CrossRefGoogle Scholar
  45. Requena N, Jeffries P, Barea JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62:842–847PubMedCentralPubMedGoogle Scholar
  46. Salerni E, Perini C (2004) Experimental study for increasing productivity of Boletus edulis s.l. in Italy. For Ecol Manag 201:161–170CrossRefGoogle Scholar
  47. Savoie JM, Largeteau ML (2011) Production of edible mushrooms in forests: Trends in development of a mycosilviculture. Appl Microbiol Biotechnol 89:971–979CrossRefPubMedGoogle Scholar
  48. Sitta N, Floriani M (2008) Nationalization and globalization trends in the wild mushroom commerce of Italy with emphasis on Porcini (Boletus edulis and allied species). Econ Bot 62:307–322CrossRefGoogle Scholar
  49. Sweet HC, Bolton WE (1979) The surface decontamination of seeds to produce axenic seedlings. Am J Bot 66:692–698CrossRefGoogle Scholar
  50. Tagu D, Faivre-Rampant P, Lapeyrie F, Frey-Klett P, Vion P, Villar M (2001) Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar (Populus spp.) cross. Mycorrhiza 10:237–240CrossRefGoogle Scholar
  51. Talei D, Saad MS, Yusop MK, Kadir MA, Valdiani A (2011) Effect of different surface sterilizers on seed germination and contamination of king of bitters (Andrographis paniculata Nees.). Am J Agric Environ Sci 10:639–643Google Scholar
  52. Walder F, Niemann H, Natarajan M, Lehmann MF, Bollet T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797PubMedCentralCrossRefPubMedGoogle Scholar
  53. Wu XQ, Hou LL, Sheng JM, Ren JH, Zheng L, Chen D, Ye JR (2012) Effects of ectomycorrhizal fungus Boletus edulis and mycorrhiza helper Bacillus cereus on the growth and nutrient uptake by Pinus thunbergii. Biol Fertil Soils 48:385–391CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Olaya Mediavilla
    • 1
    • 2
  • Jaime Olaizola
    • 2
  • Luis Santos-del-Blanco
    • 1
    • 3
  • Juan Andrés Oria-de-Rueda
    • 1
  • Pablo Martín-Pinto
    • 1
    Email author
  1. 1.Sustainable Forest Management Research Institute, Fire and Applied Mycology Laboratory, Departments of Agroforestry Sciences and Vegetal Production and Natural ResourcesUniversity of Valladolid (Palencia)PalenciaSpain
  2. 2.IDForest-Biotecnología Forestal AplicadaVenta de BañosSpain
  3. 3.Department of Ecology and EvolutionUniveristy of LausanneLausanneSwitzerland

Personalised recommendations