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Ascomyceteorg 07-06 Ascomyceteorg Novel Tuber spp. (Tuberaceae, Pezizales) in the Puberulum Group from Mexico Gonzalo GUEVARA-GUERRERO Summary: Recent taxonomic and molecular studies on Tuber in North America have revealed several new Gregory BONITO species. Here we propose Tuber bonitoi, T. brunneum, T. pseudoseparans and T. tequilanum as new species. Efrén CÁZARES-GONZÁLEZ These species are described from Mexico and differ in a combination of morphologically features including Rosanne HEALY ascospore size, pellis cell size, peridium thickness and ascoma color. These new taxa have phylogenetic affi- nity to Tuber separans, described from the United States. Phylogenetic placement of these novel Tuber species Rytas VILGALYS in the /puberulum clade are presented. James TRAPPE Keywords: Ascomycota, systematics, taxonomy, white truffles, phylogeny, biodiversity. Résumen: Recientes estudios taxonómicos y moleculares en el género Tuber de Norteamérica han revelado Ascomycete.org, 7 (6) : 367-374. varias nuevas especies. Proponemos aquí Tuber bonitoi, T. brunneum, T. pseudoseparans y T. tequilanum como Novembre 2015 nuevas especies. Estas especies son descritas de México y difieren en una combinación de características Mise en ligne le 30/11/2015 morfológicas en el tamaño de la ascospora, tamaño de las células del epicutis, grosor del peridio y color de ascomas. Estos nuevos taxones tienen afinidad filogenética a T. separans descrita de Estados Unidos. La ubi- cación filogenética de estas especies nuevas de Tuber en el clado /puberulum es presentado. Palabras clave: Ascomycota, sistemática, taxonomía, trufas blancas, filogenia, diversidad. Introduction T. zhongdianense X. Y. He, Hai M. Li & Y. Wang, T. sinosphaerosporum L. Fan, J. Z. Cao & Yu Li, T. lijiangense L. Fan & J. Z. Cao, T. vesicoperi- dium L. Fan, T. microsphaerosporum L. Fan & Y. Li, T. alboumbilicum The genus Tuber P. Micheli ex F. H. Wigg. is one of the most impor- Y. Wang & Shu H. Li, T. pseudosphaerosporum L. Fan, T. panzhihua- tant truffle lineages given its ecological and economic value. Some nense X. J. Deng & Y. Wang, and T. microverrucosum L. Fan & C. L. Hou, species of Tuber (e.g. T. melanosporum Vittad., T. aestivum (Wulfen) but also several undescribed species with light color ascoma and Spreng, T. borchii Vittad.) are cultivated worldwide and contribute reticulate spores (BONITO et al., 2009, 2010; CHEN & LIU, 2007; FAN et al., to a multimillion dollar industry (HALL et al., 2007; MARTIN & BONITO, 2012; HALASZ et al., 2005; JEANDROZ et al., 2008; KINOSHITA et al., 2011; 2012; MELLO et al., 2006; PACIONI, 1999; PALENZONA et al., 1972; PAOLOCCI PAYEN et al., 2014; WANG et al., 2007). BONITO et al. (2009) further asses- et al., 2006; PAYEN et al., 2014). Tuber species are part of forest food sed diversity of these fungi through phylogenetic study on Tuber webs with links to vertebrate and invertebrate taxa, which play a from North America and showed that many species appear endemic role in truffle spore propagule dispersal ASER(M et al., 2008; MCGRAW to North America and include many taxa pending formal descrip- et al., 2002; TRAPPE et al., 2009). In addition, Tuber spp. form ectomy- tion. Tuber separans appeared as a complex of species distributed corrhizal associations with both conifers and woody flowering across the western United States, where it was described, into cen- plants and help their plant hosts acquire mineral nutrition and water tral and eastern Mexico (BONITO et al., 2009; CÁZARES et al., 1992; GUE- however this mutualist association is more complex than it seems VARA et al., 2013). The morphology of these southern collections only to be e.g. T. magnatum, and not much information on nutritional loosely fit the description T. separans. Closer morphological and mo- transfer exists (BIDARTONDO et al., 2004; KOVACS & JAKUCS, 2006; LALLI et lecular analysis has revealed cryptic diversity in the southern part al., 2015; TRAPPE et al., 2009; WALKER et al., 2005; WURZBURGER et al., of the T. separans lineage in Mexico. In this study we propose four 2001), related to this, T. aestivum could have detrimental effects on southern taxa as novel species for North America based on morpho- oaks and hazel seedlings (TORDA et al., 2014). Within the genus Tuber, logical and phylogenetic analyses: Tuber bonitoi, T. brunneum, the /puberulum clade is one of the most species diverse and geo- T. pseudoseparans and T. tequilanum. graphically widespread of the eleven recognized clades (BONITO et al., 2013; PAYEN et al., 2014). Truffles belonging to the /puberulum clade tend to be small to medium sized, white to brown in color with Material and Methods alveolate-reticulate spore ornamentation. Tuber borchii (aka ‘bian- chetto’) is one species in this clade that has economic importance Sample collection.— In this study more than 100 fruiting bodies (LOTTI et al., 2010). Despite their ecological and economical impor- of Tuber (ascomata) were studied from northeastern México. Specific tance, studies on this clade of truffles have been limited due to the localities are listed in the “specimens examined” sections in the in- taxonomic difficulty to delimitate species based on morphology, dividual descriptions. Specimens were preserved following recom- the small sized ascomata (of most species in this group), and their mendations of CASTELLANO et al. (1989), and when possible duplicate generally low economic value (HALASZ et al., 2005; MELLO et al., 2000; splits have been deposited in the herbaria José Castillo Tovar (ITCV, BONITO et al., 2010). index herbariorum), Oregon State University (OSC), Duke University The taxonomy of Tuber puberulum Berk. & Broome and related (DUKE). Previously accessioned herbarium specimens of Tuber, in- species e.g. T. separans Gilkey has been controversial in the past (GIL- cluding type collections from OSC and ITCV, were also examined du- KEY, 1939, 1954; HARKNESS, 1899). Recent molecular phylogenetic stu- ring this study. dies from North America, Europe and Asia have shown that the Morphological observations.— Morphological data were ob- /puberulum clade is comprised of the species T. separans, T. borchii, tained by the methods of CASTELLANO et al. (1989), GILKEY (1939), and T. californicum Harkn., T. sphaerosporum Gilkey, T. puberulum, T. liui PEGLER et al. (1993). Examined characters included ascoma size, sur- A S. Xu, T. dryophilum Tul. & C. Tul., T. oligospermum Tul. & C. Tul., T. ra- face texture and color, peridial structure; spore length and width paeodorum Tul. & C. Tul., T. maculatum Vittad., T. foetidum Vittad., (excluding ornamentation), length/width ratio (Q), shape, wall thick- T. cruposum R. Hesse, T. whetstonense J.L. Frank, D. Southw. & Trappe, ness, number of reticular meshes along and across spore axes, T. latisporum Juan Chen & J. G. Liu, T. huizeanum L. Fan & C. L. Hou, height of the meshes, color and ascus size, shape, wall thickness, T. cistophilum P. Alvarado, G. Moreno, Manjón, Gelpi & J. Muñoz, and number of spores per ascus. Hand-cut sections were mounted 367 in 5% KOH and Melzer’s reagent for light microscopy. Spore measu- Peridium 200–550 μm thick; pellis a pseudoparenchyma 50– rements of Tuber spp. in KOH compared to those in water showed 300 μm thick, the cells 5–53 μm broad, isodiametric to slightly an- no KOH effect (J. Trappe, unpublished data). Microscopic structures gular, the widest surrounded by smaller cells resulting in a “rosette were measured and photographed under a light microscope and like” appearance (Fig. 2 C), pubescent in some areas or grouped to stereomicroscope. form warts, hyaline to yellowish orange in KOH, the walls 2 μm thick; DNA sequencing and phylogenetic analyses.— Molecular pro- dermatocystidia 35–88 × 5–6 μm, single, clustered or turf, tapered tocols follow those of GUEVARA et al. (2008). DNA was extracted from to the tip, some sinuate, fragile, thin and irregular-walled, septate; truffle fruiting bodies with the chloroform extraction technique subpellis 75–400 μm thick, hyaline interwoven hyphae, 5– 10 μm using CTAB 2X DNA extraction buffer. The ITS region was amplified broad at the septa, thin to thick (1–3 μm) walled. Gleba of hyaline, with the primer pair ITS1f-LR5 (GARDES & BRUNS, 1993; VILGALYS & HES- parallel to interwoven, thin-walled hyphae, 3.5–10 μm broad at the TER, 1990; WHITE et al., 1990). PCR products were cleaned of single septa, the cells commonly cylindrical to slightly inflated. stranded oligonucleotides enzymatically with antarctic phospha- Ascospores broadly ellipsoid, subglobose or sometimes globose; tase and endonuclease digestion (New England Biolabs). Sanger se- thick walled, excluding their alveolate-reticulate ornamentation, in quencing was performed by Big Dye chemistry v3.1 with the 1-spored asci 35–50 × 33–45 μm (Q=1.0–1.51), 2-spored 30 –48 × forward primer ITS5 (WHITE et al., 1990) and reverse primers LR5. DNA 25–38 μm (Q=1.06–1.35), 3-spored 23–43 × 20–33 μm (Q=1.0–1.43), sequences were determined on an ABI 3700 capillary sequencer. and 4-spored 22–35 × 20–33 μm (Q=1.0–1.4), the walls up to 2 μm DNA sequences were viewed and manually edited in Sequencher thick and yellowish in KOH; reticulum with (6–)7–9 meshes along 4.0. Sequences were queried against GenBank with the BLASTN al- the spore length and 6–7 across, the alveolar walls 5 μm tall. Asci gorithm to verify that sequences belonged to Tuber. Sequences 82–100 × 50–82 μm, globose, subglobose to broadly ellipsoid, ses- were aligned with MUSCLE (EDGAR, 2004). Alignments were manually sile to pedicellate and bifurcate in some, the walls up to 2 μm thick, checked and ambiguous regions were excluded in Mesquite 2.5 with 1, 2 or 3 layers, hyaline in KOH. (MADDISON & MADDISON, 2009). Phylogenetic analyses were conducted with maximum likelihood Distribution, habitat and season: Mexico, Veracruz, under Pinus (ML) in PAUP* (SWOFFORD, 2002). The best fit nucleotide substitution hartwegi, in a mountainous forest, with Abies religiosa. September. model was based on the Akaike information criterion and was im- Specimens examined: HOLOTYPE.
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