Cantharellus (Cantharellales, Basidiomycota) Revisited in Europe Through a Multigene Phylogeny
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Fungal Diversity DOI 10.1007/s13225-016-0376-7 Cantharellus (Cantharellales, Basidiomycota) revisited in Europe through a multigene phylogeny 1,2 1 1 2 Ibai Olariaga • Gabriel Moreno • Jose Luis Manjo´n • Isabel Salcedo • 3 4 5 Vale´rie Hofstetter • Diego Rodrı´guez • Bart Buyck Received: 12 May 2016 / Accepted: 21 October 2016 Ó School of Science 2016 Abstract Resolving species delimitation issues of Euro- ecology. Eighteen type specimens from Europe are pean Cantharellus is crucial to correctly name chanterelles sequenced. Based on revised species concepts sixteen around the globe. Thirty names referring to Cantharellus s. novel taxonomic synonyms are here proposed for European str. have been described in Europe, some of which are used chanterelles: C. alborufescens (= C. henrici, C. ilicis, C. in other continents. Based on combined analyses of ITS2, lilacinopruinatus), C. amethysteus (= C. cibarius subsp. LSU, RPB2 and TEF-1, merely eight species are here squamulosus, C. cibarius var. umbrinus, C. rufipes), C. recognized in Europe applying the genealogical concor- cibarius (= C. cibarius var. atlanticus, C. parviluteus), C. dance phylogenetic species recognition criteria, one of ferruginascens (= C. cibarius var. flavipes), C. friesii (= C. which, C. roseofagetorum, is described as new. Morpho- ignescens), C. pallens (= C. cibarius var. albidus, C. logical characters used in species delimitation are mapped cibarius var. bicolor, C. subpruinosus), and C. romagne- and their variability evaluated. The colour of the hyme- sianus (= C. pseudominimus, C. lourizanianus, C. romag- nophore in young specimens is found to be a rather con- nesianus var. parvisporus). The type of Cantharellus, C. stant morphological character of taxonomic use. European cibarius, is epitypified. Descriptions, colour illustrations species of Cantharellus are morphologically distinguished and a key to all European species are provided. by unique combinations of characters, such as the presence of a pink pileal coating, pileus and hymenophore colour Keywords Cantharelloid clade Á Cantharellaceae Á when young, and in some cases, the mean spore length and Epitype Á Edible fungi Á Genealogical concordance Á Species delimitation & Ibai Olariaga [email protected] Bart Buyck Introduction [email protected] Chanterelles are popularly known and commercialized 1 Department of Life Sciences (Botany), University of Alcala´, fungi that belong to the genus Cantharellus Adans.: Fr. ´ 28805 Alcala de Henares, Madrid, Spain Cantharellus, as circumscribed by early authors (e.g. Fries 2 Department of Plant Biology and Ecology (Botany), 1821, 1874; Fuckel 1870; Que´let 1888), comprised an University of the Basque Country (UPV/EHU), Apdo 644, artificial assemblage of species with veined or folded 48080 Bilbao, Spain 3 hymenophore, but this initial broad concept was progres- Department of Plant Protection, Agroscope Changins- sively narrowed down (Buyck et al. 2014) to species in the Wadenswil Research Station, ACW, Rte de Duiller, 1260 Nyon, Switzerland Cantharelloid clade (Moncalvo et al. 2006), with Can- tharellus cibarius Fr.: Fr. selected as the type species by 4 Kherdzmari St. Microdistrict 11. Block 58, Flat 69, Temka, Tbilisi, Georgia Earle (1909). The controversial boundary between Can- tharellus and Craterellus Pers.: Fr. (Corner 1966; Petersen 5 De´partement Syste´matique et E´ volution, CP 39, ISYEB, UMR 7205 CNRS MNHN UPMC EPHE, Muse´um National 1971), both classified in Cantharellaceae, has been d’Histoire Naturelle, 12 Rue Buffon, 75005 Paris, France resolved with aid of molecular data (Dahlman et al. 2000; 123 Fungal Diversity Moncalvo et al. 2006). Compared to Craterellus, Can- taxa of Cantharellus were published without good colour tharellus is featured by having bicyclic carotenoids and, illustrations and this complicates name interpretations even with few exceptions, basidiomata with a solid stipe (Buyck upon examination of type material. Even when attempting et al. 2014). Hydnum L.: Fr. and Sistotrema confluens Pers.: identification of fresh material, species limits are often Fr. are sister to Cantharellaceae in available phylogenies unclear and knowledge of intraspecific morphological (Moncalvo et al. 2006). Nevertheless, rates of evolution of variability is poor. Some of the diagnostic characters used nuclear ribosomal RNA genes are higher in Cantharellus in species delimitation have been stated to vary during and Craterellus than in other members of the Cantharelloid basidioma development, such as the pileal coating, colour, clade and conflicts exist between single-gene genealogies the scaliness (Petersen 1979; Redhead et al. 1997; Buyck of ribosomal and protein-coding genes (Moncalvo et al. et al. 2015; Olariaga et al. 2015) or the staining upon 2006; Olariaga, unpublished data). Thus, more robust manipulation (Olariaga 2009), but molecular data have not protein-coding phylogenies are needed to propose a solid been used to assert these assumptions. Large intraspecific family delimitation in the core of the Cantharelloid clade. variation is probably due to the long-lived nature of Can- Little attention was drawn to taxonomy of European tharellus basidiomata (Largent and Sime 1995; Norvell species of Cantharellus until the dawn of the XXth century. 1995). Thus, several issues concerning species delimitation A number of new taxa was published scattered (e.g. Que´let and name interpretation remain unaddressed. 1883; Maire 1937; Pila´t 1959), mostly employing basid- In the last decade, molecular tools have increasingly ioma size and colour as diagnostic characters. The staining been used to support new species descriptions and existing of basidiomata upon manipulation (Gillet 1878; Malenc¸on species concepts. Several new Cantharellus species have and Bertault 1975) and ecological characters (Orton 1969) been described using ITS molecular data (Feibelman et al. have occasionally been taken into consideration as well, 1996; Dettman et al. 2003), but the use of the ITS, uni- but microscopic characters were never used as ultimate versal barcode of fungi (Schoch et al. 2012), is problem- diagnostic characters when describing new Cantharellus atic in Cantharellus. The ITS1 region is extremely long taxa in Europe. The first modern monographic treatment of (Feibelman et al. 1994), its amplification sometimes Cantharellus was published by Corner (1966) as part of his unsuccessful, and, due to its multicopy nature (Hillis and worldwide monograph of Cantharelloid fungi. This author Dixon 1991), a single basidioma can contain ITS1 copies provided interpretations for all available Cantharellus diverging in up to 3% between each other (Kumari et al. names, albeit without having examined type material in 2011). Moreover, ITS amplification with the general or most cases. Among more recent monographic treatments, fungal specific primers (ITS1 or ITS1F with ITS4) often the one by Romagnesi (1995) deserves attention, since he generates multiple bands due to the presence of endo- proposed the wall-thickness of the pileipellis hyphae as phytic fungi (Buyck et al. in prep.). Ribosomal nuclear novel taxonomic character. large subunit (nucLSU) has also been used to support In the context of a worldwide revision of Cantharellus descriptions of new species (Kumari et al. 2011; Shao species (Eyssartier 2001), Eyssartier and Buyck et al. 2014), but this region has frequently a too low res- (2000) published an exhaustive compilation of accepted olution to discriminate between closely related species in European taxa. These authors provided modern interpre- Cantharellus (Buyck et al. 2011), particularly in subgenus tations for all European taxa granting taxonomic impor- Cantharellus. As an alternative, the translation elongation tance to the staining of basidiomata upon manipulation, the factor 1-alpha (TEF-1) region has been shown to provide presence of pileal coating and the wall-thickness of surface phylogenetic signal to resolve species limits in Can- hyphae in the pileipellis. New combinations, typifications tharellus, and has been employed alone (Buyck and and a new species were also proposed. This study stimu- Hofstetter 2011; Buyck et al. 2011, 2015; Ariyawansa lated description of new taxa of Cantharellus in Europe et al. 2015; Liu et al. 2015; Shao et al. 2016)orin (Ferna´ndez-Sasia et al. 2003; Blanco-Dios 2004, 2011; combination with the ITS2 and nrLSU regions (Foltz et al. Hermitte et al. 2005; Olariaga and Salcedo 2008), but 2013) when describing new taxa. Also, Buyck et al. (2014) considerable confusion has remained on name interpreta- utilized the RNA polymerase II second largest subunit tions and species boundaries. On the one hand, the paucity (RPB2) and the rDNA mitochondrial small subunit of discriminant microscopic characters (Buyck et al. 2014), (mtSSU) regions to propose an updated infrageneric widely used in species delimitation in Agaricomycetes, classification of Cantharellus. hinders most Cantharellus species from being identified Olariaga et al. (2015) generated a few ITS-nucLSU microscopically. One the other hand, most diagnostic sequences to place albino and orange specimens of some characters (pileus and hymenophore colour, staining) are European Cantharellus but, while molecular data have lost after desiccation and this makes identification of dried become increasingly available for Cantharellus in other material practically impossible. Regrettably, many new continents, no study has ever evaluated species boundaries 123 Fungal Diversity of Cantharellus in Europe using