Abstract
The highly prized black truffle is a fungus mostly harvested in orchards planted with mycorrhizal seedlings. It is an obligatory outcrossing fungus with a single MAT locus containing two alternative mating-type idiomorphs. In the orchards, at the mycorrhizal level, these mating types are frequently spatially segregated. Some studies found that this segregation was pronounced from the nursery stage, whereas others did not find such a marked segregation. Besides, information on the host tree species and nursery conditions used in Spain, one of the main truffle-producing countries, are very scarce. In this study, we investigated the temporal dynamics of mating types in nursery seedlings of Quercus ilex and Quercus faginea, as well as the influence of cultural conditions in the nursery. Our results indicated that at the plant level, there was a trend for one of the mating types to dominate over the other from the first to the second year in the nursery, in both host species and both nursery conditions tested. However, this segregation process was not so sharp as previously reported. Our results support the hypothesis that intraspecific competition results in reduced evenness of mating-type abundance from the nursery stage, although almost all seedlings maintained both mating types and, at the seedling batch scale, the occurrence of both mating types was roughly balanced.
Similar content being viewed by others
Data Availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Olivier JM, Savignac JC, Sourzat P 2002 Truffe et trufficulture, 2nd ed. Fanlac, Périgueux, France
Reyna S, Garcia-Barreda S (2014) Black truffle cultivation: a global reality. For Syst 23:317–328. https://doi.org/10.5424/fs/2014232-04771
Bencivenga M 2001 La tartuficoltura in Italia: problematiche e prospettive. In: Fédération Française des Trufficulteurs (ed) Actes du Ve Congrès International Science et culture de la truffe. Aix-en-Provence, France, pp 27–29
Sourzat P 2008 Principe de précaution en trufficulture. Station d’Expérimentation sur la Truffe, Le Montat, France
Selosse MA, Taschen E, Giraud T (2013) Do black truffles avoid sexual harassment by linking mating type and vegetative incompatibility? New Phytol 199:10–13. https://doi.org/10.1111/NPH.12329
Le Tacon F, Rubini A, Murat C et al (2016) Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.). Ann For Sci 73:105–117. https://doi.org/10.1007/s13595-015-0461-1
Martin F, Kohler A, Murat C et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038. https://doi.org/10.1038/nature08867
Taschen E, Rousset F, Sauve M et al (2016) How the truffle got its mate: insights from genetic structure in spontaneous and planted Mediterranean populations of Tuber melanosporum. Mol Ecol 25:5611–5627. https://doi.org/10.1111/mec.13864
Chen J, De la Varga H, Todesco F et al (2021) Frequency of the two mating types in the soil under productive and non-productive trees in five French orchards of the Périgord black truffle (Tuber melanosporum Vittad.). Mycorrhiza 31:361–369. https://doi.org/10.1007/S00572-020-01011-4
Riccioni C, Belfiori B, Rubini A et al (2008) Tuber melanosporum outcrosses: analysis of the genetic diversity within and among its natural populations under this new scenario. New Phytol 180:466–478. https://doi.org/10.1111/J.1469-8137.2008.02560.X
Rubini A, Belfiori B, Riccioni C et al (2011) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189:710–722. https://doi.org/10.1111/J.1469-8137.2010.03492.X
Rubini A, Belfiori B, Riccioni C et al (2011) Tuber melanosporum: mating type distribution in a natural plantation and dynamics of strains of different mating types on the roots of nursery-inoculated host plants. New Phytol 189:723–735. https://doi.org/10.1111/j.1469-8137.2010.03493.x
De la Varga H, Le Tacon F, Lagoguet M et al (2017) Five years investigation of female and male genotypes in Périgord black truffle (Tuber melanosporum Vittad.) revealed contrasted reproduction strategies. Environ Microbiol 19:2604–2615. https://doi.org/10.1111/1462-2920.13735
Murat C (2015) Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25:77–81. https://doi.org/10.1007/s00572-014-0593-4
Murat C, De la Varga H, Akroume E et al (2013) Fine-scale spatial genetic structure of the black truffle (Tuber melanosporum) investigated with neutral microsatellites and functional mating type genes. New Phytol 199:176–187. https://doi.org/10.1111/nph.12264
Linde CC, Selmes H (2012) Genetic diversity and mating type distribution of Tuber melanosporum and their significance to truffle cultivation in artificially planted Truffiéres in Australia. Appl Environ Microbiol 78:6534–6539. https://doi.org/10.1128/AEM.01558-12
Marozzi G, Sánchez S, Benucci GMN et al (2016) Mycorrhization of pecan (Carya illinoinensis) with black truffles: Tuber melanosporum and Tuber brumale. Mycorrhiza 27:303–309. https://doi.org/10.1007/S00572-016-0743-Y
Donnini D, Benucci GMN, Bencivenga M, Baciarelli-Falini L (2014) Quality assessment of truffle-inoculated seedlings in Italy: proposing revised parameters for certification. For Syst 23:385–393. https://doi.org/10.5424/fs/2014232-05029
Garcia-Barreda S, Sánchez S, Marco P, Serrano-Notivoli R (2019) Agro-climatic zoning of Spanish forests naturally producing black truffle. Agric For Meteorol 269–270:231–238. https://doi.org/10.1016/j.agrformet.2019.02.020
Garcia-Barreda S, Molina-Grau S, Reyna S (2017) Fertilisation of Quercus seedlings inoculated with Tuber melanosporum: effects on growth and mycorrhization of two host species and two inoculation methods. IForest 10:267–272. https://doi.org/10.3832/ifor2096-009
Le Tacon F, Zeller B, Plain C et al (2013) Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique. PLoS ONE 8:e64626. https://doi.org/10.1371/journal.pone.0064626
Uscola M, Salifu KF, Oliet JA, Jacobs DF (2015) An exponential fertilization dose–response model to promote restoration of the Mediterranean oak Quercus ilex. New For 46:795–812. https://doi.org/10.1007/s11056-015-9493-5
Rubini A, Riccioni C, Belfiori B, Paolocci F (2014) Impact of the competition between mating types on the cultivation of Tuber melanosporum: Romeo and Juliet and the matter of space and time. Mycorrhiza 24:19–27. https://doi.org/10.1007/S00572-013-0551-6
Leonardi P, Murat-Furminieux C, Puliga F et al (2019) Ascoma genotyping and mating type analyses of mycorrhizas and soil mycelia of Tuber borchii in a truffle orchard established by mycelial inoculated plants. Environ Microbiol 22:964–975. https://doi.org/10.1111/1462-2920.14777ï
Deacon J, Fleming L (1992) Interactions of ectomycorrhizal fungi. In: Allen MF (ed) Mycorrhizal Functioning: an Integrative Plant-Fungal Process. Chapman and Hall, New York, pp 249–300
Agerer R (2002) Colour atlas of Ectomycorrhizae 1st-12th del. Eihorn-Verlag, Berlin
Iotti M, Zambonelli A (2006) A quick and precise technique for identifying ectomycorrhizas by PCR. Mycol Res 110:60–65. https://doi.org/10.1016/j.mycres.2005.09.010
Paolocci F, Rubini A, Riccioni C, Arcioni S (2006) Reevaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72:2390–2393. https://doi.org/10.1128/AEM.72.4.2390-2393.2006/ASSET/492A113C-9699-4B8A-B5BF-BF0DE23605CA/ASSETS/GRAPHIC/ZAM0040666230001.JPEG
Gómez-Molina E, Sánchez S, Parladé J et al (2020) Glyphosate treatments for weed control affect early stages of root colonization by Tuber melanosporum but not secondary colonization. Mycorrhiza 30:725–733. https://doi.org/10.1007/S00572-020-00990-8
Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. https://doi.org/10.1111/mec.12481
R Core Team 2020 R: a language and environment for statistical computing
Makowski D, Ben-Shachar MS, Patil I, Lüdecke D 2020 Methods and algorithms for correlation analysis in R. J Open Source Softw 5:2306. https://doi.org/10.21105/JOSS.02306
Lenth R V 2021 emmeans: estimated marginal means, aka Least-Squares Means
Fridley JD, Grime JP (2010) Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity. Ecology 91:2272–2283. https://doi.org/10.1890/09-1240.1
Iotti M, Rubini A, Tisserant E et al (2012) Self/nonself recognition in Tuber melanosporum is not mediated by a heterokaryon incompatibility system. Fungal Biol 116:261–275. https://doi.org/10.1016/J.FUNBIO.2011.11.009
Oliach D, Castaño C, Fischer CR et al (2022) Soil fungal community and mating type development of Tuber melanosporum in a 20-year chronosequence of black truffle plantations. Soil Biol Biochem 165:108510. https://doi.org/10.1016/J.SOILBIO.2021.108510
Funding
This work was funded by the collaboration agreement for the operation of CIET (funded by Diputación Provincial de Huesca, with the participation of CITA, Comarca de la Ribagorza and Ayuntamiento de Graus).
Author information
Authors and Affiliations
Contributions
E.G.-M., S.S., and S.G.-B. conceived and designed the study. Funding was secured by E.G.-M., and S.S. Laboratory protocols were conducted by E.G.-M., M.P.-P., and S.S. The data were analyzed by S.G.-B. The manuscript was initially written by E.G.-M., along with significant contributions from S.S. and S.G.-B.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gómez-Molina, E., Sánchez, S., Puig-Pey, M. et al. Intraspecific Competition Results in Reduced Evenness of Tuber melanosporum Mating-Type Abundance from the Nursery Stage. Microb Ecol 86, 253–260 (2023). https://doi.org/10.1007/s00248-022-02087-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-022-02087-5