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Coryneliaceae, Ascomycota): Caliciopsis Valentina Sp

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Coryneliaceae, Ascomycota): Caliciopsis Valentina Sp Mycol Progress (2015) 14: 10 DOI 10.1007/s11557-015-1034-2 ORIGINAL ARTICLE Unravelling the diversity of European Caliciopsis (Coryneliaceae, Ascomycota): Caliciopsis valentina sp. nov. and C. beckhausii comb. nov., with a worldwide key to Caliciopsis Isaac Garrido-Benavent & Sergio Pérez-Ortega Received: 23 October 2014 /Revised: 23 February 2015 /Accepted: 25 February 2015 /Published online: 11 March 2015 # German Mycological Society and Springer-Verlag Berlin Heidelberg 2015 Abstract The new species Caliciopsis valentina from the Members of Caliciopsis are characterized by the presence eastern Iberian Peninsula is characterized morphologically, of stalked, black perithecia, absence of paraphyses, evanes- anatomically, and molecularly. The occurrence of cent and long pedicellate asci with brown, one-celled asco- C. subcorticalis (Cooke & Ellis) Fitzp. in Europe is discussed. spores. Most species seem to be bound to a specific host plant, Based on the revision of fresh and herbarium specimens we either as saprotrophs or antagonistic biotrophs. Some of them propose the new combination Caliciopsis beckhausii with a grow on cankered tissues, or even on cynipid galls as neotype selected for this taxon. New molecular data (ITS and C. quercina Marm (Marmolejo 1999). The impact of parasitic nuLSU) are used in combination with available sequences to species on the fitness of their hosts has been long overlooked, build a preliminary phylogenetic hypothesis for this genus. but Ramsfield et al. (2009) recently assessed the effect of We point out some previously overlooked colour-reaction C. arceuthobii (Peck) M.E. Barr as a biological control agent tests as relevant for the systematics of the group. Finally, an for Arceuthobium americanum,thelodgepolepinedwarf updated key for all known Caliciopsis species is provided. mistletoe. The genus is known from temperate regions (North and South America, and Eurasia) and the tropics (Fitzpatrick Keywords Coryneliales . Eurotiomycetes . 1920, 1942; Benny et al. 1985;Rikkinen2000; Pratibha Iberian Peninsula . Mazaedium et al. 2010). So far, 28 species are known worldwide, but information regarding their distribution ranges is scarce for most of them. On the other hand, a phylogenetic hypothesis Introduction of the evolutionary relationships within the genus is still miss- ing due to the lack of recently collected specimens (Pratibha Recent research on the evolution of the mazaedium, a type of et al. 2010). passive spore-dispersion structure, confirmed that the genus So far, only four species have currently been reported for Caliciopsis Peck (Coryneliales, Ascomycota) belongs to the Europe: C. tiliae Arnaud, C. nigra (Schrad.) Fitzp., Eurotiomycetes (Prieto et al. 2013). This assignment was pre- C. subcorticalis (Cooke & Ellis) Fitzp., and C. ventricosa viously suggested in several comprehensive phylogenetic (Ach.) Tibell (= C. pinea Peck, see Tibell 1987). The latter studies (Geiser et al. 2006; Spatafora et al. 2006). The sole three grow on different species of the same host plant genus at family included in Coryneliales,theCoryneliaceae (Lumbsch each side of the Atlantic Ocean (Fitzpatrick 1920, 1942). and Huhndorf 2010), comprises seven additional genera, No revision of European species is currently available. The showing all but Coryneliopsis bitunicate asci (Johnston and few accessible occurrences (Germany, France, Finland, Spain, Minter 1989; Geiser et al. 2006). Switzerland, Italy, Yugoslavia) mostly date from the last centu- : ry (Fitzpatrick 1920, 1942; Benny et al. 1985). From the I. Garrido-Benavent (*) S. Pérez-Ortega Iberian Peninsula, only C. nigra has been hitherto reported, Departamento de Biogeoquímica y Ecología Microbiana, growing on Juniperus galls (Vila et al. 2004). However, during Museo Nacional de Ciencias Naturales, CSIC, C/ Serrano 115-bis, E-28006 Madrid, Spain a recent work focused on epiphytic lichens growing on bark of e-mail: [email protected] holm oak in eastern Spain (Garrido-Benavent et al. 2013), two 10 Page 2 of 11 Mycol Progress (2015) 14: 10 enigmatic Caliciopsis species were found growing on this amplification, using primers ITS1F (Gardes and Bruns 1993), broad-leaved tree. One of them apparently represents a new ITS1LM (Myllys et al. 1999), and ITS4 (White et al. 1990)for species and the other is morphologically similar to ITS, and LR0R (Rehner and Samuels 1994)andLR5 C. subcorticalis. (Vilgalys and Hester 1990) for nuLSU. PCR reactions were Thus, the present study has the following aims: 1) to char- performed in a total volume of 25 μl, containing 2.5 μlof acterize and to describe a new species of Caliciopsis,2)to reaction buffer (Biotools®), 5 μl of dNTPs (1 mM), 1.25 μl discuss the presence of C. subcorticalis sensu Fitzpatrick in of each primer (10 μM), 1 μlofMgCl2 (50 mM), and 0.5 U of Europe, 3) to reevaluate the diagnostic usefulness of several DNA polymerase (Biotools®); final volume was reached by traits for this genus, and 4) to present an updated key to all adding distilled water. The following reaction conditions were known species worldwide. used for both DNA regions: initial denaturation for 5 min at 95 °C, followed by 35 cycles of 30 s at 95 °C, 1 min at 52 °C (ITS1F-ITS4, LR0R-LR5) or 56 °C (ITS1LM-ITS4), and Materials and methods 1 min and 30 s at 72 °C; the protocol concluded with a final extension step of 10 min at 72 °C. Morphological studies PCR products were purified and cleaned using the UltraClean® PCR Clean-Up Kit (MOBIO Laboratories, Inc.). All sampled specimens were examined using a Leica Both complementary DNA strands were sequenced at S8APO dissecting microscope fitted with a Leica EC3 MACROGEN EUROPE (The Netherlands). Accession num- image capture system. Slide preparations were observed bers corresponding to sequences generated in this study are in in a Zeiss Axioplan 2 microscope fitted with Table 1. "Nomarski" differential interference contrast, and photo- graphs were taken with a Zeiss AxioCam digital cam- Sequence alignment and phylogenetic analysis era. Microscopic observations and measurements were made using material mounted in H2O by means of the Electropherograms were checked, trimmed, and assem- Zeiss Axiovision 4.8 image analyser system. Ten per- bled using SeqmanII v.5.07© (Dnastar Inc.). Alignments cent KOH was used both for tissue dissociation and were carried out using Muscle v3.6 (Edgar 2004)and examination, and for testing possible colour reactions were manually examined in Bioedit v.7.0.9 (Hall 1999). of cellular elements, which were also tested by using Gblocks 0.91b (Castresana 2000)wasusedtoremove NO3H, commercial bleach (NaOCl) and Lugol’ssolu- ambiguously aligned regions, using the least restrictive tion. At least 20 spores per individual were measured options for removing gaps and allowing for positions with for each sampling locality. The average is followed by a gap in less than 50 % of the sequences. jModelTest its standard deviation, and the maximum and minimum v.2.1.4 (Darriba et al. 2012) was used to select the best values are given in parentheses. The length/width ratio nucleotide substitution model for subsequent analyses (Q) gives minimum and maximum values, average, and using the Akaike Information Criterion (AIC, Akaike its standard deviation. 1974). The GTR+G model was selected for both regions. The types of the novel taxa are deposited in MA (isotypes Bayesian analyses were those implemented in MrBayes in M, H). Herbarium acronyms follow Thiers (2014). v3.2 (Ronquist et al. 2012). Partitions were used for the Citations of taxon name authors follow Brummitt & Powell combined ITS + nuLSU analysis. Settings included two "Authors of Plant Names" (http://www.kew.org/data/authors. parallel runs with eight-chain runs over 10 M generations. html), and of exsiccate follow Triebel and Scholz (2001– Sampling was performed after every 200th step; the first 2014) (http://indexs.botanischestaatssammlung.de/). 10 % of saved data was discarded as "burn in". Convergence of chains and ESS values were checked in DNA extraction, PCR amplification, and DNA sequencing Tracer v.1.6 (available at http://tree.bio.ed.ac.uk/software/ tracer/). Phylogenetic trees were visualized in FigTree v. Because of the tiny size of the fruiting bodies, about 10–15 1.3.1 and Adobe Illustrator CS2® was used for fresh ascomata were sampled from the same bark fragment. artwork (Fig. 1). Maximum likelihood analyses were Their bases were removed with the help of a sterilized razor performed using PHYML v.3.0 (Guindon et al. 2010) blade and a needle. The remnants were subsequently through the web platform ATGC (http://atgc.lirmm.fr/ inspected under a dissecting and a light microscope in order phyml/); a non-parametric bootstrap analysis (1,000 repli- to avoid contamination by other fungi. Genomic DNA isola- cates) was carried out in order to assess branch support tion was performed by means of a modified version of the (Felsenstein 1985). Hamigera avellanea (Thom & CTAB method (Cubero et al. 1999). Internal transcribed spac- Turesson) Stolk & Samson and Spiromastix tentaculata er (ITS) and partial nuLSU rDNA regions were selected for Guarro, Gené & De Vroey were used as outgroups. Mycol Progress (2015) 14: 10 Page 3 of 11 10 Table 1 List of taxa used in this study, with collection numbers and GenBank accession numbers; newly produced sequences are in bold Taxa Locality and collector ITS LSU Caliciopsis beckhausii I162 San Juan del Monte, Burgos, SPAIN, S. Pérez-Ortega KP144005 (neotype) KP144010 (neotype) & M. A. Pérez Muriel
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