Abstract
Seasonal dynamics of black truffle (Tuber melanosporum) extraradical mycelium as well as the associated mycorrhizal community have been evaluated in a 16-year-old plantation with productive and non-productive trees. Mycelium biomass was seasonally quantified by real-time PCR over two consecutive years and the correlation with environmental variables explored. Extraradical mycelium biomass varied seasonally and between the two consecutive years, being correlated with the precipitation that occurred 1 month before sampling. In addition, productive trees had more mycelium in the brûlé area than non-productive trees did. The ectomycorrhizal community composition inside the burnt areas was seasonally evaluated during a year. Ten mycorrhizal morphotypes were detected; T. melanosporum was the most abundant in productive and non-productive trees. Black truffle mycorrhizas were more abundant (mycorrhizal tips per unit of soil volume) in productive trees, and no seasonal variation was observed. The occurrence of black truffle mycorrhizas was significantly and positively correlated with the biomass of extraradical mycelium. The mycorrhizal community within the brûlé areas was significantly different between productive and non-productive trees, and no variation was detected between seasons. The assessment of the fungal vegetative structures in a mature plantation is of paramount importance to develop trufficulture methods based on the knowledge of the biological cycle of the fungus and its relationships with the associated ectomycorrhizal communities.
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References
Agerer R (2001) Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114. doi:10.1007/s005720100108
Agerer R (2008) Colour atlas of Ectomycorrhizae (1st–14th delivery). Einhorn-Verlag, Schwäbisch Gmünd
Águeda B, Agerer R, De Miguel AM, Parladé J (2010a) Quercirhiza quadratum: a revision of the characters and identity of the AD type ectomycorrhiza. In: 3o Congreso Internazionale di Spoleto sul tartufo: 303–307
Águeda B, Fernández-Toirán LM, De Miguel AM, Martínez-Peña F (2010b) Ectomycorrhizal status of a mature productive black truffle plantation. For Syst 19:89–97
Bencivenga M, Donnini D, Di Massimo G (1992) Analisi dellemicorrize in una tartufaia coltivata di Tuber melanosporum undici anni dopo l’impianto. Micol Veg Mediterr 7:159–171
Bonito G (2009) Fast DNA-based identification of the black truffle Tuber melanosporum with direct PCR and species-specific primers. FEMS Microbiol Lett 301:171–175. doi:10.1111/j.1574-6968.2009.01812.x
Bustin SA, Benes V, Garson JA, Hellemnas J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time experiments. Clin Chem 55:611–622
Cairney JWG (2012) Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol Biochem 47:198–208. doi:10.1016/j.soilbio.2011.12.029
Callot G (1999) La truffe, la terre, la vie. INRA ed, Versailles
Ceruti A, Fontana A, Nosenzo C (2003) Le specie europee del genere Tuber : una revisione storica. Museo Regionale di Scienze Naturali, Torino
Chevalier G (1994) Evolution des recherches sur les plants mycorhizes pour la truffe et perspectives de dévelopment. G Bot Ital 128:7–18
Chevalier G (2012) Europe, a continent with high potential for the cultivation of the burgundy truffle (Tuber aestivum/uncinatum). Acta Mycol 12:127–132
Chevalier G, Giraud M, Bardet M (1982) Interaction entre le mycorrhizes de Tuber melanosporum et celles d’autres champignons ectomycorrhiziennes en sols favorable à la truffe. Les mycorhizes biologie et utilisaition Le Colloques de l’INRA 13:313–321
Chevalier G, Sourzat P (2012) Soils and techniques for cultivating Tuber melanosporum and Tuber aestivum in Europe. In: Zambonelli A, Bonito G (eds) Edible ectomycorrhizal mushrooms, current knowledge and future prospects. Soil biology 34, Springer-Verlag, Berlin, pp 163–189
De la Varga H, Águeda B, Martínez-Peña F, Parladé J, Pera J (2012) Quantification of extraradical soil mycelium and ectomycorrhizas of Boletus edulis in a scots pine forest with variable sporocarp productivity. Mycorrhiza 22:59–68. doi:10.1007/s00572-011-0382-2
De la Varga H, Águeda B, Ágreda T, Martínez-Peña F, Parladé J, Pera J (2013) Seasonal dynamics of Boletus edulis and Lactarius deliciosus extraradical mycelium in pine forests of central Spain. Mycorrhiza 23:391–402. doi:10.1007/s00572-013-0481-3
De Miguel AM, Águeda B, Sáez R, Sánchez S, Parladé J (2016) Diversity of ectomycorrhizal Thelephoraceae in Tuber melanosporum-cultivated orchards of northern Spain. Mycorrhiza 26:227–236. doi:10.1007/s00572-015-0665-0
De Miguel AM, Águeda B, Sánchez S, Parladé J (2014) Ectomycorrhizal fungus diversity and community structure with natural and cultivated truffle hosts: applying lessons learned to future truffle culture. Mycorrhiza 24:S5–S18. doi:10.1007/s00572-013-0554-3
García-Montero LG, Manjón JL, Pascual C, García-Abril A (2007) Ecological patterns of Tuber melanosporum and different Quercus Mediterranean forests: quantitative production of truffles, burn sizes and soil studies. For Ecol Manag 242:288–296. doi:10.1016/j.foreco.2007.01.045
Giraud M (1979) Etude comparative des mycorrhizes d’arbes producteurs de truffes ou non en zone truffière. Graduation dissertation, Ecole Nationale Supérieure Agronomique 1 de Rennes, and Institut National de la recherche Agronomique, Clermont-Ferrand, France.
Granetti B, Angelini P (1992) Competizione tra alcuni funghi ectomicorrizici e Tuber melanosporum in una tartufaia coltivata. Micol Veg Mediterr 7:173–188
Gryndler M, Beskid O, Hršelová H, Bukovská P, Hujslová M, Gryndlerová H, Konvalinková T, Schepf A, Sochorova L, Jansa J (2015) Mutabilis in mutabili: spatiotemporal dynamics of a truffle colony in soil. Soil Biol Biochem 90:62–70. doi:10.1016/j.soilbio.2015.07.025
Gryndler M, Hršelová H, Soukupová L, Streiblová E, Valda S, Borovička J, Gryndlerová H, Gažo J, Miko M (2011) Detection of summer truffle (Tuber aestivum Vittad.) in ectomycorrhizae and in soil using specific primers. FEMS Microbiol Lett 318:84–91. doi:10.1111/j.1574-6968.2011.02243.x
Gryndler M, Trilcová J, Hrselová H, Streiblová E, Gryndlerová H, Jansa J (2013) Tuber aestivum Vittad. Mycelium quantified: advantages and limitations of a qPCR approach. Mycorrhiza 23:341–348. doi:10.1007/s00572-012-0475-6
Hall IR, Brown GT, Zambonelli A (2007) Taming the truffle. The history, lore and science of the ultimate mushroom. Timber press, Portland, OR
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis
Hortal S, Pera J, Parladé J (2008) Tracking mycorrhizas and extraradical mycelium of the edible fungus Lactarius deliciosus under field competition with Rhizopogon spp. Mycorrhiza 18:69–77. doi:10.1007/s00572-007-0160-3
Iotti M, Leonardi M, Lancellotti E et al (2014) Spatio-temporal dynamic of Tuber magnatum mycelium in natural truffle grounds. PLoS One 9:1–18. doi:10.1371/journal.pone.0115921
Iotti M, Marchetti M, Bonuso E, Zambonelli A (2005) Morphological and molecular characterization of the mycorrhizas of Inocybe rufuloides and Inocybe splendens. Mycotaxon 94:75–84
Kjøller R (2006) Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia. FEMS Microbiol Ecol 58:214–224. doi:10.1111/j.1574-6941.2006.00166.x
Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. doi:10.1111/mec.12481
Landeweert R, Leeflang P, Kuyper TW, Hoffand E, Rosling A, Wenars K, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69:327–333. doi:10.1128/AEM.69.1
Lilleskov EA, Bruns TD (2003) Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies nutrient patches. New Phytol 159:141–151. doi:10.1046/j.0028-646x.2003.00794.x
Liu B, Fischer C, Bonet JA, Olivera A, Inchusta A, Colinas C (2014) Pattern of Tuber melanosporum extramatrical mycelium expansion over a 20-year chronosequence in Quercus ilex-truffle orchards. Mycorrhiza 24:47–54. doi:10.1007/s00572-014-0559-6
Martin F, Kohler A, Murat C et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038. doi:10.1038/nature08867
Mello A, Napoli C, Murat C, Morin E, Marceddu G, Bonfante P (2011) ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle-grounds. Mycologia 103:1184–1193. doi:10.3852/11- 027
Murat C (2015) Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25:77–81. doi:10.1007/s00572-014-0593-4
Murat C, Vizzini A, Bonfante P, Mello A (2005) Morphological and molecular typing of the below-ground fungal community in a natural Tuber magnatum truffle-ground. FEMS Microbiol Lett 245:307–313. doi:10.1016/j.femsle.2005.03.019
Napoli C, Mello A, Borra A, Vizzini A, Sourzat P, Bonfante P (2010) Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytol 185:237–247. doi:10.1111/j.1469- 8137.2009.03053.x
Nilsson LO, Wallander H (2003) Production of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilization. New Phytol 158:409–416. doi:10.1046/j.1469-8137.2003.00728.x
Olivier JM, Savignac JC, Sourzat P (2012) Truffe et trufficulture. Ed. Fanlac, Perigueux
Paolocci F, Rubini A, Granetti B, Arcioni S (1999) Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizae. FEMS Microbiol Ecol 28:23–30
Parladé J, De la Varga H, De Miguel AM, Sáez R, Pera J (2013) Quantification of extraradical mycelium of Tuber melanosporum in soils from truffle orchards in northern Spain. Mycorrhiza 23:99–106. doi:10.1007/s00572-012-0454-y
Parladé J, Hortal S, Pera J, Galipienso L (2007) Quantitative detection of Lactarius deliciosus extraradical soil mycelium by real-time PCR and its application in the study of fungal persistence and interspecific competition. J Biotechnol 128:14–23. doi:10.1016/j.jbiotec.2006.09.010
Peter M, Ayer F, Egli S, Honegger R (2001) Above- and below-ground community structure of ectomycorrhizal fungi in three Norway spruce (Picea abies) stands in Switzerland. Can J Bot 79:1134–1151. doi:10.1139/b01-092
Raidl S, Bonfigli R, Agerer R (2005) Calibration of quantitative real-time Taqman PCR by correlation with hyphal biomass and its copies in mycelia of Piloderma croceum. Plant Biol 7:713–717. doi:10.1055/s-2005-873003
Reyna S (2012) Truficultura. Fundamentos y técnicas. Ed. Mundi-Prensa, Madrid
Rineau F, Maurice JP, Nys C, Voiry H, Garbaye J (2010) Forest liming durably impact the communities of ectomycorrhizas and fungal epigeous fruiting body. Ann For Sci 66:110–121. doi:10.1051/forest/2009089
Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci F (2011) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189:710–722. doi:10.1111/j.1469-8137.2010.03492.x
Sáez García-Falces R, De Miguel Velasco AM (2008) La trufa: guía de truficultura. ITGA ed, Villava, Spain
Sánchez S, Ágreda T, Águeda B, Martín M, De Miguel AM, Barriuso J (2014) Persistence and detection of black truffle ectomycorrhizas in plantations: comparison between two field detection methods. Mycorrhiza 24:S39–S46. doi:10.1007/s00572-014-0560-0
Sánchez S, De Miguel AM, Sáez R, Martín-Santafé M, Águeda B, Barriuso J, García-Barreda S, Salvador-Alcalde D, Reyna S (2016) La trufa de verano en la península ibérica: estado actual y potencial de cultivo. ITEA 112:20–33. doi:10.12706/itea.2016.007
Sims SE, Hendricks JJ, Mitchell RJ, Mitchell RJ, Kuehn KA, Pecot SD (2007) Nitrogen decreases and precipitation increases ectomycorrhizal extramatrical mycelia production in a longleaf pine forest. Mycorrhiza 17:299–309. doi:10.1007/s00572-007-0105-x
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, third edn. Academic Press, London
Splivallo R, Ottonello S, Mello A, Karlovsky P (2011) Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189:688–699. doi:10.1111/j.1469-8137.2010.03523.x
Suz LM, Martín MP, Colinas C (2006) Detection of Tuber melanosporum DNA in soil. FEMS Microbiol Lett 254:251–257. doi:10.1111/j.1574-6968.2005.00029.x
Suz LM, Martín MP, Oliach D, Fischer CR, Colinas C (2008) Mycelial abundance and other factors related to truffle productivity in Tuber melanosporum-Quercus ilex orchards. FEMS Microbiol Lett 285:72–78. doi:10.1111/j.1574-6968.2008.01213.x
Taschen E, Sauve M, Taudiere A, Parladé 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
Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Kõljalg U (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490. doi:10.1111/j.1469-8137.2008.02561.x
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
Wallander H, Ekblad A, Bergh J (2011) Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests. For Ecol Manag 262:999–1007. doi:10.1016/j.foreco.2011.05.035
White TJ, Bruns S, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc, San Diego, pp 315–322
Yun W, Hall IR (2004) Edible ectomycorrhizal mushrooms: challenges and achievements. Can J Bot 82:1063–1073
Zampieri E, Murat C, Cagnasso M, Bonfante P, Mello A (2010) Soil analysis reveals the presence of an extended mycelial network in a Tuber magnatum truffle-ground. FEMS Microbiol Ecol 71:43–49. doi:10.1111/j.1574-6941.2009.00783.x
Zampieri E, Rizzello R, Bonfante P, Mello A (2012) The detection of mating type genes of Tuber melanosporum in productive and non productive soils. Appl Soil Ecol 57:9–15. doi:10.1016/j.apsoil.2012.02.013
Acknowledgements
The authors would like to thank the owner of the truffle plantation and his valuable collaboration in the field work. This study was supported by the Spanish Ministry of Economy and Competitively (MINECO) through the projects AGL 2012-40035-C03 and AGL2015-66001-C3. We are also grateful to the Genomics Core Group at CIMA, University of Navarra, for their support in molecular sequencing and interpretation. This work is part of the doctorate of Mikel Queralt, financed by a grant Asociación de Amigos de la Universidad de Navarra.
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QUERALT, M., PARLADÉ, J., PERA, J. et al. Seasonal dynamics of extraradical mycelium and mycorrhizas in a black truffle (Tuber melanosporum) plantation. Mycorrhiza 27, 565–576 (2017). https://doi.org/10.1007/s00572-017-0780-1
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DOI: https://doi.org/10.1007/s00572-017-0780-1