Shifts in soil fungal communities in Tuber melanosporum plantations over a 20-year transition from agriculture fields to oak woodlands
Abstract
Aim of study: To explore the diversity of soil fungi found in black truffle (Tuber melanosporum) plantations following the introduction of the mycorrhizal-colonized host tree, (Quercus ilex), through the development of the brûlé and production of mature sporocarps.
Area of study: This research was carried out province of Teruel, Aragon (central eastern Spain).
Material and Methods: Soil samples from 6 plantations were collected beneath Q. ilex trees inoculated with T. melanosporum, of 3, 5, 7, 10, 14 and 20 years after out planting in truffle plantations. Soil DNA was extracted, PCR-amplified and sequenced to compare soil fungi present at different ages.
Main results: As tree age increased, we observed an increased frequency of T. melanosporum (from 8% to 71% of sequenced colonies) and concomitant decrease in the combined frequency of Fusarium spp. and Phoma spp. (from 64% to 3%).
Research highlights: There are important shifts in species richness and in functional groups in the soil fungal communities in maturing black truffle-oak woodland plantations. The observed inverse relationship between the frequency of soil endophytic and/or pathogenic fungi and that of the mycorrhizal mutualist T. melanosporum provides support to continue a deeper analysis of shifts in fungal communities and functional groups where there is a transition from agriculture fields to woodlands.
Abbreviations used: Ectomycorrhiza (ECM) fungus; Vesicular arbuscular mycorrhiza (VAM); Operational taxonomic unit (OTU).
Downloads
References
References
Abarenkov K, Nilsson RH, Larsson K, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, et al., 2010. The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186: 281-285. http://dx.doi.org/10.1111/j.1469-8137.2009.03160.x
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389
Baciarelli-Falini L, Rubini A, Riccioni C, Paolocci F, 2006. Morphological and molecular analyses of ectomycorrhizal diversity in a man-made T. melanosporum plantation: Description of novel truffle-like morphotypes. Mycorrhiza 16: 475-484. http://dx.doi.org/10.1007/s00572-006-0066-5
Belfiori B, Riccioni C, Tempesta S, Pasqualetti M, Paolocci F, Rubini A, 2012. Comparison of ectomycorrhizal communities in natural and cultivated Tuber melanosporum truffle grounds. FEMS Microbiol Ecol 81: 547-561. http://dx.doi.org/10.1111/j.1574-6941.2012.01379.x
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, 2011. GenBank. Nucleic Acids Res 39: D32-D37. http://dx.doi.org/10.1093/nar/gkq1079
Chakravarty P, Hwang SF, 1991. Effect of an ectomycorrhizal fungus, Laccaria laccata, on Fusarium damping-off in Pinus banksiana seedlings. Eur J Plant Pathol 21: 97–106. http://dx.doi.org/10.1111/j.1439-0329.1991.tb00949.x
Chakravarty P, Unestam T, 1987. Differential influence of ectomycorrhizae on plant growth and disease resistance in Pinus sylvestris seedlings. J Phytopathol, 120: 104–120. http://dx.doi.org/10.1111/j.1439-0434.1987.tb04423.x
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 (Suppl 1): S5–S18. http://dx.doi.org/10.1007/s00572-013-0554-3
Donnini D, Bencivenga M, 1995. Micorrize inquinanti frequenti nelle piante tartufigene. Inquinanti in campo. Micol Ital 20: 185-207.
Gordon TR. Martyn RD, 1997. The evolutionary biology of Fusarium oxysporum. Annu Rev Phytopathol. 35:111-28. http://dx.doi.org/10.1146/annurev.phyto.35.1.111
Grayston SJ, Vaughan D, Jones D, 1996. Rhizosphere carbon flow in trees in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5, 29–56. http://dx.doi.org/10.1016/S0929-1393(96)00126-6
Huang X, Madan A, 1999. CAP3: A DNA sequence assembly program. Genome Res 9: 868-877. http://dx.doi.org/10.1101/gr.9.9.868
Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, … Lindahl BD, 2012. New primers to amplify the fungal ITS2 region--evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol, 82(3), 666–77. http://dx.doi.org/10.1111/j.1574-6941.2012.01437.x
Kim MS, Stewart JE, Dumroese RK, Klopfenstein NB, 2012. Occurrence of the root rot pathogen, Fusarium commune, in forest nurseries of the Midwestern and western United States. J Phytopathol 160: 112–114. http://dx.doi.org/10.1111/j.1439-0434.2011.01865.x
Kües U, Martin F, 2011. On the road to understanding truffles in the underground. Fungal Genet Biol 48: 555-560. http://dx.doi.org/10.1016/j.fgb.2011.02.002
Latiffah Z, Azaman RS, 2011 Fusarium species isolated from forest soil samples. Malays J Microbiol 7(3), 171–174.
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 Suppl 1, S47–54. http://dx.doi.org/10.1007/s00572-014-0559-6
Maremmani A, Bedini S, Mato I, Tomei PE, 2003. Type of mycorrhizal associations in two coastal nature reserves of the Mediterranean basin. Mycorrhiza 13: 33–40. http://dx.doi.org/10.1007/s00572-002-0194-5
Martín-Pinto P, Pajares J, Díez J, 2006. In vitro effects of four ectomycorrhizal fungi, Boletus edulis, Rhizopogon roseolus, Laccaria laccata and Lactarius deliciosus on Fusarium damping off in Pinus nigra seedlings. New For 32(3): 323–334. http://dx.doi.org/10.1007/s11056-006-9006-7
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. http://dx.doi.org/10.1111/j.1469-8137.2009.03053.x
Olivera A, Fischer CR, Bonet JA, Martínez de Aragón J, Oliach D, Colinas C, 2011. Weed management and irrigation are key treatments in emerging black truffle (Tuber melanosporum) cultivation. New For 42(2): 227–239. http://dx.doi.org/10.1007/s11056-011-9249-9
Park D, 1963. The presence of Fusarium oxysporum in soils. Trans Br Mycol Soc 46(3): 444–448. http://dx.doi.org/10.1016/S0007-1536(63)80038-8
Reyna S, Garcia-Barreda S, 2014. Black truffle cultivation: a global reality, Forest Syst 23(2): 317–328. http://dx.doi.org/10.5424/fs/2014232-04771
Rubini A, Belfiori B, Passeri V, Falini LB, Arcioni S, Riccioni C, Paolocci F, 2011. The AD-type ectomycorrhizas, one of the most common morphotypes present in truffle fields, result from fungi belonging to the Trichophaea woolhopeia species complex. Mycorrhiza 21: 17-25. http://dx.doi.org/10.1007/s00572-010-0308-4
Smith SE, Read DJ, 2008. Mycorrhizal Symbiosis, Third Edition. Academic Press. New York. pp. 602.
Splivallo R, Ottonello S, Mello A, Karlovsky P, 2011. Truffle volatiles: From chemical ecology to aroma biosynthesis. New Phytol 189: 688-699. http://dx.doi.org/10.1111/j.1469-8137.2010.03523.x
Streiblová E, Gryndlerová H, Gryndler M, 2012. Truffle brûlé: an efficient fungal life strategy. FEMS Microbiology Ecology 80(1): 1–8. http://dx.doi.org/10.1111/j.1574-6941.2011.01283.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 Ecol Letters 285(1): 72–8. http://dx.doi.org/10.1111/j.1574-6968.2008.01213.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. http://dx.doi.org/10.1016/j.apsoil.2012.02.013
Zengpu L, Junran J, Changwen W, 1994. Antagonism between Ectomycorrhizal fungi and plant pathogens. In: Mycorrhizas for Plantation Forestry in Asia; Brundett M, Dell B, Malajczuk N, and Mingqin G. (eds). pp 77-81. Proceedings of an international symposium and workshop, Kaiping, Guangdong Province, P.R. China 7-11 Nov 1994.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.
