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Entoloma Species of the Rhodopolioid Clade

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Entoloma Species of the Rhodopolioid Clade Entoloma species of the rhodopolioid clade (subgenus Entoloma; Tricholomatinae, Basidiomycota) in Norway Tor Erik Brandrud1, Egil Bendiksen1, John Bjarne Jordal2, Øyvind Weholt3, Siw Elin Eidissen3, Jostein Lorås3, Bálint Dima4,5, Machiel E. Noordeloos6 1Norwegian Institute for Nature Research, Gaustadalléen 21, NO-0349 Oslo, Norway 2Biolog J.B. Jordal, Auragata 3, NO-6600 Sunndalsøra, Norway 3Nord University, Nesna, NO-8700 Nesna, Norway 4Department of Plant Anatomy, Institute of Biology, Eötvös Loránd University, Pázmány Péter sétány 1/c, H-1117 Budapest, Hungary 5Department of Biosciences, Plant Biology, Viikki Plant Science Centre, University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland 6Naturalis Biodiversity Center, section Botany, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands Corresponding author: [email protected] arter innenfor Rhodopolia-gruppa er samlet og verifisert med DNA-sekvensering. Av Norsk tittel: Rødsporer i Rhodopolia-gruppa disse er 10 nye for Norge og inkluderer også (Entoloma underslekt Entoloma; Tricholoma- tre ubeskrevne arter. Fire forskjellige øko- tinae, Basidiomycota) i Norge geografiske elementer kan skilles ut: (i) det sørlige (boreonemorale) lind-eik-hassel- Brandrud TE, Bendiksen E, Jordal JB, Weholt elementet, (ii) det boreal-arktisk-alpine selje- Ø, Eidissen SE, Lorås J, Dima B, Noordeloos vier-or-bjørk-elementet, (iii) det arktisk- ME, 2018. Entoloma species of the rhodopo- alpine dvergvier(-reinrose)-elementet, og (iv) lioid clade (subgenus Entoloma; Tricholoma- det boreale bjørk(-gran)-elementet. Alle 24 tinae, Basidiomycota) in Norway. Agarica artene kommenteres i den taksonomiske delen, 2018, vol. 38: 21–46. ordnet etter de fem slektskapsgruppene (klader) som framkommer i den fylogenetiske analysen. KEY WORDS: DNA-sequencing, ecology, distribution, Salix-Alnus-Betula-associates, ABSTRACT Tilia-Quercus associates The rhodopolioid species of Entoloma (subgen. Entoloma) in Norway are presented. The NØKKELORD: DNA-sekvensering, økologi, rhodopolioid clade consists of tricholomatoid utbredelse, Salix-Alnus-Betula-arter, Tilia- or collybioid, rarely omphalinoid, ectomycor- Quercus-arter rhizal species. Altogether 24 species of the rhodopolioid clade were recorded and verified SAMMENDRAG by rDNA ITS sequence data, of which 10 are Gruppa omkring lutrødspore (Rhodopolia- here reported as new to Norway, including gruppa) i slekta rødspore (Entoloma) i Norge three apparently undescribed species. Four presenteres. Gruppa består av musserongaktige different eco-geographical elements can be og flathattaktige, sjelden traktsoppaktige, mykorrhiza(sopprot)-dannende arter. I alt 24 AGARICA vol. 38 21 Brandrud et al. distinguished from our material; (i) the south- supported clades, the rhodopolioid clade ern (boreonemoral) Tilia-Quercus-Coryluse- (including the type species of the genus E. lement, (ii) the boreal-arctic-alpine Salix- sinuatum) and the Nolanidea clade (incl. E. Alnus-Betula element, (iii) the arctic-alpine clypeatum and allies). The latter group has Salix(-Dryas) element, and (iv) the boreal apparently a special variant of mycorrhiza Betula(-Picea) element. All 24 species are including parasitism, and is associated with commented in the taxonomic part, arranged wooden plants rarely forming (ecto)mycorrhiza, according to the five well-supported clades such as Rosaceae members like Sorbus, from phylogenetic analyses. Prunus and Malus, as well as Ulmus (Koba- yashi and Hatano 2001). The present paper INTRODUCTION will, however, only focus on the rhodopol- Entoloma is one of the most species-rich ioid species. genera within Agaricales, well characterized The rhodopolioid species can be disting- by many-angled spores that leave a pinkish uished from the E. clypeatum group (Nolanidea brown spore print. Like Cortinarius, it is one clade) at the section level (sect. Entoloma) or of the few remaining “mammoth-genera” at the subgenus level (subgen. Entoloma = which (at least in Europe) is still kept as one subgen. Rhodopolia s. Kokkonen 2015). The single genus and not split into several smaller infrageneric taxonomy we do not consider genera, despite the large morphological, genetic further in this paper, and hence we preliminary and ecological variation across the numerous apply the terms rhodopolioid clade and rhodo- lineages (cfr. monographs of subgenera such polioid species for our study group (cfr. also as Morgado et al. 2013, Morozova et al. 2014, e.g. Sánchez-Garcia and Matheny 2016). and regional fungas such as Jeppesen et al. The rhodopolioid clade has been extensively 2012, Krieglsteiner and Gminder 2003, Ludwig treated by Noordeloos (1981, introducing sect. 2007). The reasons for this comprehensive Rhodopolia, 1992, 2004) and by Kokkonen approach are manyfold, but are mainly based (2015 as subgen. Rhodopolia). The former on the fact that variability in Entoloma is studies were based on morphological taxonomy, complex and still not fully understood, and whereas the latter also included DNA sequence more specifically, many clades in phylogenetic data, focusing on boreal(-alpine) species analyses show low support with the genetic from Finland. The rhodopolioid species are markers applied so far (see e.g. Morgado et distinguished from many other Entoloma al. 2013). This fragile phylogenetic structure, taxa by their (i) often large and robust basid- combined with the manifest lack of data from iomata (although also small, tiny representatives Entoloma species from many parts of the occur), (ii) rather uniform predominantly world, makes it too preliminary to subdivide brown, yellow-brown or grey-brown colours this mammoth into smaller genera. due to simultaneously encrusted-intracellular- Subgenus Entoloma is nevertheless one of plasmatic pigments (contrasting the often the genetically, ecologically and morphologi- vivid colours seen in other groups), and (iii) cally better defined entities within the genus, often pronounced farinaceous or nitrous smells especially since it apparently consists of (Noordeloos 1981, 1992, 2004, Kokkonen (ecto)mycorrhizal species (Kobayashi and 2015). The pileipellis structures are fairly Hatano 2001, Sánchez-Garcia and Matheny simple, mainly a cutis or ixocutis of narrow, 2016, Tedersoo et al. 2010). According to cylindrical hyphae, with or without a disting- phylogeny, the mycorrhizal species in uishable subpellis layer of inflated, short Entoloma can be subdivided into two well- elements. A number of species (e.g. E. serpens, 22 AGARICA vol. 38 Brandrud et al. E. sericatum) have fine hairs, particularly at Ratnasingham and Hebert (2007, 2013). the margin of young and fresh specimens, The present study focus on the ecology and visible as pileocystidia, but these structures distribution of the taxa recorded, based on are ephemeral and disappear with age. Caulo- ITS-sequence- and morphology data, with an cystidia frequently occur at the apex of the emphasis on new species to Norway. At stipe, variable in shape. Cheilocystidia are present, we have not sufficient sequence- and rarely differentiated, but seem to be charac- morphology data to present a detailed taxo- teristic and constant for some species. The nomy of the group. In particular, more studies spores show apparently little, taxonomic rele- are needed on the morphological variation of vant variation, size variation mainly expres- our phylogenetic taxa, and to what degree they sing size difference of two-spored versus are possible to distinguish morphologically. four-spored basidia (Noordeloos 1981, 1992, 2004, Kokkonen 2015). Many species occur MATERIAL AND METHODS in moist forest-woodland-shrubland habitats, Approximately 250 samples of rhodopolioid and a remarkable high percentage of the species have been collected during the Nor- species seems to be associated mainly with wegian 2015–2017 Entoloma study, and 176 Salix, Populus, Betula and Alnus hosts, samples were verified by ITS sequencing. including arctic-alpine habitats (Noordeloos The latter number includes some herbarium 2004, Kokkonen 2015). Conifers such as collections. In addition sequences of six type Picea abies seem hardly to be involved in the specimens and some important reference mycorrhizae of the rhodopolioid species, material, not collected by us, were studied in although many boreal species occur in Picea- connection with the present project. Sampling dominated forests (with presence of single focused on boreonemoral and southern/middle trees of Salix, Betula and other frondose boreal regions of SE Norway, where also trees) (Kokkonen 2015, and this paper). other mycological field projects were carried The present paper is part of the Norwegian out during the period. Further, many samples Entoloma study 2015–2017, as part of The were obtained from North Trøndelag, C Norwegian Taxonomy Initiative and funded Norway, during a project foray in 2016, and by The Norwegian Biodiversity Information many from the study of Holmvassdalen nature Centre. It also includes data from a study on reserve, Nordland, including some alpine the Entoloma fungi of the Holmvassdalen sites. All sequenced material from Norway is nature reserve, Nordland (see e.g. Weholt et listed under material examined. Collections al. 2014, Noordeloos et al. in prep). The labelled NOBAS or CAFUN were sequenced Norwegian Entoloma project has focused on through NorBOL, those labelled ALV were Entoloma hotspot-habitats, such as calcareous sequenced by Pablo Alvarado (ALVALAB, (semi-)natural grasslands and calcareous Spain), and those with no sequence label are
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