Symbiotic interactions between orchids and Tuber borchii
DOI:
https://doi.org/10.6092/issn.2531-7342/15348Keywords:
Bianchetto truffle, Anacamptis morio, Cephalanthera longifolia, Limodorum abortivum, Ophrys sphegodes, Orchis purpurea, mycorrhizaAbstract
Tuber borchii is a precious truffle, which forms ectomycorrhizal associations with several coniferous and broadleaf trees, arbutoid mycorrhizas with the strawberry tree and recently it was found also to form orchid mycorrhizas with Epipactis atrorubens. In this work, we investigated the formation of T. borchii mycorrhizas in other orchid species (Anacamptis morio, Cephalanthera longifolia, Limodorum abortivum, Ophrys sphegodes, Orchis purpurea). To this aim the orchids growing in three T. borchii production areas located in Emilia Romagna region (Italy) were collected and the presence of T. borchii mycorrhizas was investigated by morphological and molecular approaches. For T. borchii molecular identification, specific primers were used by a nested PCR approach. Tuber borchii was identified in 2 out of 6 samples of A. morio, 3 out of 4 samples of C. longifolia, and 2 out 6 samples of O. sphegodes. The ecological and biological roles of the orchid association in the truffle life cycle are discussed.
References
Amicucci A, Zambonelli A, Giomaro G, Potenza L, Stocchi V (1998) Identification of ectomycorrhizal fungi of the genus Tuber by species-specific ITS primers. Molecular Ecology 7:273–277.
Bajaj SR, Shamekh S (2021) Finnish wild truffles: A review. International Journal of Engineering and Applied Sciences (IJEAS) 8(10):2394–3661. https://dx.doi.org/10.31873/IJEAS.8.10.02
Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Letters in Applied Microbiology 39:425–430. https://doi.org/10.1111/j.1472-765X.2004.01606.x
Corticelli S, Garberi ML, Gavagni A, Guandalini B (2004) Carte della vegetazione e della naturalità dei Parchi Regionali e di altre zone. Coperture vettoriali 1:000–001.
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Molecular Ecology 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gardin L (2005) I tartufi minori in Toscana: gli ambienti di crescita dei tartufi marzuolo e scorzone. ARSIA, Tuscany, Italy.
Hall IR, Brown GT, Zambonelli A (2007) Taming the truffle. The history lore and science of the ultimate mushroom. Timber Press, Portland, OR, USA.
Illyés Z, Ouanphanivanh N, Rudnóy SZ, Orczán ÁK, Bratek Z (2010) The most recent results on orchid mycorrhizal fungi in Hungary. Biologia Futura 61(1):68–76. https://doi.org/10.1556/ABiol.61.2010.Suppl.8
Iotti M, Lancellotti E, Hall I, Zambonelli A (2010) The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiology Ecology 72:250–260. https://doi.org/10.1111/j.1574-6941.2010.00844.x
Iotti M, Zambonelli A (2006) A quick and precise technique for identifying ectomycorrhizas by PCR. Mycological Research 110(1):60–65. https://doi.org/10.1016/j.mycres.2005.09.010
Jacquemyn H, Waud M, Brys R, Lallemand F, Courty PE, Robionek A, Selosse MA (2017) Mycorrhizal associations and trophic modes in coexisting orchids: an ecological continuum between auto-and mixotrophy. Frontiers in Plant Science 8:1497. https://doi.org/10.3389/fpls.2017.01497
Johnson LJ, Gónzalez-Chávez M del CA, Carrillo-González R, Porras-Alfaro A, Mueller GM (2021) Vanilla aerial and terrestrial roots host rich communities of orchid mycorrhizal and ectomycorrhizal fungi. Plants, People, Planet 3(5):541–552. https://doi.org/10.1002/ppp3.10171
Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse MA (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and non photosynthetic individuals of Cephalanthera damasonium. New Phytologist 166(2):639–653. https://doi.org/10.1111/j.1469-8137.2005.01364.x
Lancellotti E, Iotti M, Zambonelli A, Franceschini (2014) Characterization of Tuber borchii and Arbutus unedo mycorrhizas. Mycorrhiza 24:481–486. https:/doi.org/10.1007/s00572-014-0564-9
Lancellotti E, Iotti M, Zambonelli A, Franceschini A (2016) The Puberulum group sensu lato (whitish truffles). In: True Truffle (Tuber Spp.) in the World (Zambonelli A, Iotti M, Murat C, eds), Soil Biology, vol 47. Springer International, Cham, Switzerland, pp. 105–124. https://doi.org/10.1007/978-3-319-31436-5_7
Leonardi P, Baroni R, Puliga F, Iotti M, Salerni E, Perini C, Zambonelli A (2021) Co-occurrence of true truffle mycelia in Tuber magnatum fruiting sites. Mycorrhiza 31:389–394. https://doi.org/10.1007/s00572-021-01030-9
McKendrick SL, Leake JR, Read DJ (2000) Symbiotic germination and development of myco-heterotrophic plants in nature: transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytologist 145(3):539–548. https://doi.org/10.1046/j.1469-8137.2000.00592.x
Ogura-Tsujita Y, Yukawa T (2008) Epipactis helleborine shows strong mycorrhizal preference towards ectomycorrhizal fungi with contrasting geographic distributions in Japan. Mycorrhiza 18:331–338. https://doi.org/10.1007/s00572-008-0187-0
Ouanphanivanh N (2008) Could orchids indicate truffle habitats?: mycorrhizal association between orchids and truffles. Acta Biologica Szegediensis 52(1):229–232. https://abs.bibl.u-szeged.hu/index.php/abs/article/view/2630
Puliga F, Illice M, Iotti M, Leonardi P, Baghdadi A, Mozafari AA, Zambonelli A (2021) True truffle diversity in Iran. Italian Journal of Mycology 50:52–62. https://doi.org/10.6092/issn.2531-7342/12822
Qin J, Feng B (2022) Life cycle and phylogeography of true truffles. Genes 13(1):145. https://doi.org/10.3390/genes13010145
Rosa-Gruszecka A, Hilszczańska D, Pacioni G (2021) Virtual truffle hunting—A new method of Burgundy truffle (Tuber aestivum Vittad.) site typing. Forests 12(9):1239. https://doi.org/10.3390/f12091239
Schiebold JMI, Bidartondo MI, Karasch P, Gravendeel B, Gebauer G (2017) You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species. Annals of Botany 119(7):1085–1095. https://doi.org/10.1093/aob/mcw265
Schneider-Maunoury L, Deveau A, Moreno M, Todesco F, Belmondo S, Murat C, Courty PE, Jąkalski M, Selosse MA (2020) Two ectomycorrhizal truffles, Tuber melanosporum and Tuber aestivum, endophytically colonize roots of non-ectomycorrhizal plants in natural environments. New Phytologist 225(6): 2542–2556. https://doi.org/10.1111/nph.16321
Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47:416–426. https://doi.org/10.1007/s00248-003-2034-3
Shefferson RP, Kull T, Tali K (2005) Adult whole‐plant dormancy induced by stress in long‐lived orchids. Ecology 86(11):3099–3104. https://doi.org/10.1890/05-0586
Shefferson RP, Warren RJ, Pulliam HR (2014) Life‐history costs make perfect sprouting maladaptive in two herbaceous perennials. Journal of Ecology 102(5):1318–1328. https://doi.org/10.1111/1365-2745.12281
Těšitelová T, Těšitel J, Jersáková J, Říhová G, Selosse MA (2012) Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology. American Journal of Botany 99(6):1020–1032. https://doi.org/10.3732/ajb.1100503
Vohník M (2020) Ericoid mycorrhizal symbiosis: theoretical background and methods for its comprehensive investigation. Mycorrhiza 30:671–695. https://doi.org/10.1007/s00572-020-00989-1
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky J, White TJ, eds). Academic Press, San Diego, CA, pp. 315–322.
Zambonelli A, Rivetti C, Percudani R, Ottonello S (2000) TuberKey: a delta-based tool for the description and interactive identification of truffles. Mycotaxon 74(1):57–76.
Zambonelli A, Iotti M, Giomaro G, Hall I, Stocchi V (2002) T. borchii cultivation: an interesting perspective. In: Edible Mycorrhizal Mushrooms and Their Cultivation. Proceedings of the Second International Conference on Edible Mycorrhizal Mushrooms, 3-6 July 2001. Christchurch, New Zealand, pp. 0–7.
Zambonelli A, Iotti M, Boutahir S, Lancellotti E, Perini C, Pacioni G (2012) Ectomycorrhizal fungal communities of edible ectomycorrhizal mushrooms. In: Edible Ectomycorrhizal Mushrooms: Current Knowledge and Future Prospects (Zambonelli A., Bonito GM, eds), Soil Biology, vol 34. Springer-Verlag, Berlin, pp. 105–124. https://doi.org/10.1007/978-3-642-33823-6_7
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Simone Graziosi, Pamela Leonardi, Alessandra Zambonelli
This work is licensed under a Creative Commons Attribution 4.0 International License.
