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FUNGAL ECOLOGY 4 (2orr) 83-93 available at www.sciencedirecLcom ..,-dR# % ..;", ScienceDirect journal homepag,e: www.elsevier.com/locate/funeco The Asian black truffle Tuber indicum can form ectomycorrhizas with North American host plants and complete its life cycle in non-native soils Gregory BONITOa,., James M. TRAPPEb, Sylvia DONOVAW, Rytas VILGALYSa aDepartment afBiology, Duke University, Durham, NC 27708 0338, USA bDepartment of Forest Ecosystems and Society, Oregon State University, Corvallis, OR 97331 5752, USA CNorth American Trufflitlg Society, PO Box 296, Cart/allis, OR 97339, USA ARTICLE INFO ABSTR ACT Article history: The Asian black truffleT uber indicwll ismorphologically and phylogenetically similar to the Received 17 March 2010 European black truffle Tuber melunosporum. T. indicum is considered a threat to T. melullo­ Revision received 10 August 2010 sponun trufficulture due to its presumed competitiveness and broad host compatibility. Accepted 15 August 2010 Recently, in independent events, T. indicum was found fruiting in a forest in Oregon, USA, Available online 5 November 2010 and was detected as ectomycorrhizas within a t11lffle orchard established with trees Corresponding editor: believed to have been inoculated with T. melanosporum. We used haplotype networking to John W.G. Caimey assess intraspecific ITS rONA diversity among Asian and North AmericanT. indicum group B isolates.To further assess the potentialof T. indiclml to spread onto native host plants it Keywords: was inoculated onto seedlings of loblolly pine (Pinus taeda) and pecan (Carya iIIitloinensis, Black truffles Juglandaceae). species endemic to North America. T. indicum formed ectomycorrhizas on Ectomycorrhizal synthesis both host species examined. This supports previous studies from Europe and Asia that Exotic species indicate T. jndicum has a broad host spectrum, an ecological trait that may be important to Juglandaceae its invasion ecology. This is the firstreport ofT. indicum introductions in North America and Pinaceae of this species fruiting outside of its native range. To help prevent further unintended Species introductions t11lffle introductions we recommend that fruitbodies used by the truffle industry for Tuber inoculating seedlings first be identified with DNA methods. © 2010 Elsevier Ltd and The British Mycological Society. All rights reserved. Introduction Whereas invasions of fungal pathogens such as chestnut blight (Cryphonectria parasitical and Dutch elm disease Species of truffles in the genus Tuber are eagerly sought due to (Ophiastoma novo-ulmQ resulting in devastating effects are well their culinary qualities and highly valued fruit bodies (Mello documented (Desprez·Loustau et al. 2007; Loo 2009). invasions et aI. 2006). Among them is Tuber meianosporllnJ, one of the by mutualistic fungi are less understood and more easily few ectomycorrhizal fungal species successfully cultivatedby overlooked (Vellinga et al. 2009). Because so little is known humans. This has led to the establishment of truffieres (truffle about the geographic ranges fungi inhabit, a major aim of orchards) on several continents (Wang & Hall 2004; current taxonomic research is to use molecular phylogenetic Dominguez et aI. 2006). Unwanted exotic or competitor approaches to better assess species distributions and their species introduced during the establishment phase of a truf­ changes associated with human activity (Pringle et al. 2009; fiere could have economic and ecological consequences. Bonito et al. 2010j Wolfe et al. 2010) . • Corresponding <Hlthor. E-mail address: [email protected] (G. Bonito). 1754-5048/$ - see front matter © 2010 Elsevier Ltd andThe British Mycological Society. All rights reserved. doi: 10.1 016/j. f uneco. 20 10.08.003 84 G, Bonito et al. The European black truffle T. melanosporum is endemic to European tree hosts including Quercus spp. and Pinus pinea Mediterranean regions of southernEurope including Spain and indicating the potential of this species to invade European France (Ha,l et al. 2007; Agueda et al. 2010). It grows in calcar­ ecosystems (Zambonelli et al. 1998; Garcia-Montero et al. eous soils forming symbiotic ectomycorrhizal association 2008). particularly with deciduous trees (e.g. Quercus spp. and Corylus Here we document the occurrence ofT. indicum B from two avelfana) (M urat et 01. 2004; Hall et a1. 2007). Since the 1970's locations in North America based on ITS rONA sequence data T. melanosporum has been cultivated in Europe by planting generated from fruit bodies and ectomycorrhizas. We verify seedlings produced with ectomycorrhizas of T. melanosponml that six different IT S haplotypes of T. indicum B have been into prepared fields (Grente et al. 1972; Boutekrabt et al. 1990). introduced to North America and demonstrate that T. indicum Evidence of black truffles fruiting in North America was B fonns ectomycorrhizas on North American angiosperm and absent prior to the 1980's when the cultivation of T. melano­ gymnosperm hosts. sporwn in California was firstreported (Rigdon 1994). However, a native black truffle species, Tuber regimontanum, recently Methods was described from an undisturbed montane oak forest near Monterrey, Mexico, providing the first evidence of the T. mel­ Truffle collections anosporum lineage in North America (Guevara et a1. 2008). T. regimontanum is phylogenetically distinct and basal to its Members of the North American Truffling Society (NATS) closest known relatives, T. melcmosporum and Tuber indicum, have been collecting truffles in Oregon since its founding in and is distinguished morphologically by having larger spores 1978. The basic technique to search for truffles involves the ornamented with spines connected by low reticulations. use of a multi- tined garden cultivator or hand rake for The Asian black truffle T. indicum was originally described removing leaf litter and scratching into the mineral as deep as from the Himalayas (Cooke & Massee 1892) and is harvested 15 cm. Forests composed of appropriate ectomycorrhizal commercially in the Yunnan and Sichuan provinces of China hosts and animal diggings are targeted. Because of the diffi­ (Zhang et al. 2005; Wang et a1. 2006; Wang & Liu 2009). culty in identifying truffle species such as Tuber based on However, recent molecular analysis indicates thatT. indicum is morphology alone, molecular methods are often needed to composed of at least two phylogenetic species, referred to as identify taxa and to place them in the fungal phylogeny T. indicum A & T. indicum B; their taxonomy is still in flux (Bonito et al. 2009). (Hu 1992; Zhang et a1. 2005; Wang et al. 2006; Huang et al. 2009; Bonito et al. 2010; Garcia-Montero et al. 2010). Analysis of87 T. Sampling orchard ectomycorrhizas indicwn IT S rONA sequences accessioned in Genbank showed >7.0% interspecific sequence divergence betweenT. indicwn A To determine whether T. melanosporum persisted as ectomy­ and B and <2.5% intraspecific variation within each clade corrhizas on roots of trees inoculated withT, melanosponml, root (Bonito et al. 2010). However, there are no apparent morpho­ samples were taken from seven private truffle orchards during logical characters that distinguish these two phylogenetic the summers of 2006-2008.Permissions were granted with the species from each other and both show high morphological request of anonymity. Orchards were located in NorthCarolina, intraspecific variation, broad geographic .distribution, and Tennessee and California, USA, and had been established both species fruit across a wide variety of soil types in asso­ between 4 and 15 yr prior to sampling with trees purchased ciation with host species in the Betulaceae (Corylus spp., AltIUS from companies specializing in the production ofT. melanospo· spp.), Fagaceae (Quercus spp., Castanea spp., Castanopsis spp., rum infected seedlings. Inoculation methods are often regarded Lithocarpus spp.) and Pinaceae (Pinus spp., Keteleeria spp.) as proprietary or trade secrets. In one case, however, trees had (Wang et al. 2006; Garcia-Montero et al. 2008; Geng et ai, 2009; been inoculated by the orchard owner using a sluny of spores, Wang & Liu 2009; Garcia-Montero et 01. 2010). similar to the method described below. At least ten trees were Organoleptic (culinary) properties of T. indicum are similar, sampled from each orchard by harvesting one to three 30 cm if more subtle than that of T. melanosporum. Levels of natural sections of fine roots from each tree. In the orchard where T. T. indicwn production are relatively high (>300 tons from indiculll was detected a second broader sampling of 150 trees Yunnan Province, China, in 2006) and T. indicum is sold at was conducted to assess the prevalence ofT. indicum within the a significantly lower price than is T. melanosporwn (Wang et a1. orchard. Collected roots were soaked in tap water for 1 hr to 2006; Murat et al. 2008). Since the late 1990's T. indicum has loosen soil debris, rinsed on a 1 mm sieve and examined under been exported from China to Europe, North America and a stereoscope. First, ectomycorrhizas were screened morpho­ Australia (Garcia-Montero et a1. 2010). It can be challenging to logically and sorted as Tuber and non-Tltber. The identity of distinguish T. indiwm from T. melanosporum because their Tuber morphotypes and a subset of non-Tuber morphotypes morphology is similar (Fig 1). Concerns ofT. indicum being sold were determined through specific-primer PCR assays and DNA as T. melmlOsporwn and unintentionally used as seedling sequence
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