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Lichenicolous Fungi from Florida Growing on Graphidales

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Lichenicolous Fungi from Florida Growing on Graphidales © 2019 W. Szafer Institute of Botany Polish Academy of Sciences Plant and Fungal Systematics 64(2): 249–282, 2019 ISSN 2544-7459 (print) DOI: 10.2478/pfs-2019-0021 ISSN 2657-5000 (online) Lichenicolous fungi from Florida growing on Graphidales Paul Diederich1*, Ralph S. Common2, Uwe Braun3, Bettina Heuchert 3, Ana Millanes4, Ave Suija5 & Damien Ertz 6,7 Abstract. The lichenicolous fungi growing on Graphidales hosts in Florida are revised, Article info mainly based on collections by the second author (R. C.). Twenty-one species are rec- Received: 29 Mar. 2019 ognized. The new genus and species Lawreya glyphidiphila is described for a common Revision received: 19 Aug. 2019 asexual fungus growing on Glyphis scyphulifera and more rarely Trypethelium eluteriae, Accepted: 20 Aug. 2019 characterized by black stromatic conidiomata in which subspherical conidiogenous loculi Published: 2 Dec. 2019 develop, producing aseptate, subglobose, brown conidia. Nine additional new species Associate Editor are described: Amerosporiopsis phaeographidis (on Phaeographis brasiliensis), Arthonia Adam Flakus acanthotheciicola (on Acanthothecis floridensis), A. subgraphidicola (on Graphis assimilis), Hemigrapha graphidicola (on G. assimilis), Skyttea graphidicola (on Graphis spp.), Strigula graphidicola (on G. assimilis), S. perparvula (on Graphidales), Talpapellis graphidis (on Graphis caesiella) and Tremella wedinii (on Glyphis scyphulifera). Phylogenetic place- ments of Lawreya glyphidiphila, Skyttea graphidicola and Tremella wedinii are presented. Identification keys are given for the species of Cornutispora and Talpapellis, and for the 66 species known to grow on Graphidales hosts worldwide. Key words: lichen parasites, lichens, phylogeny, taxonomy, Cornutispora, Lawreya, Talpapellis Introduction The Graphidales, for a long time placed in Ostropales orders: Lichenostigma chlaroterae (mainly on Lecanora but recently proposed as a separate order by Kraichak but also on Buellia, Fuscidea and Graphis) and Taenio­ et al. (2018), are known to harbour a large diversity of lella punctata (mainly on Graphis, rarely on Arthonia, lichenicolous fungi, with 66 known species (Diederich Fissurina, Pertusaria and Phaeographis). Polycoccum et al. 2018). Some of these are opportunists, growing on arnoldii has been reported from Diploschistes and Rhizo­ a wide variety of lichens belonging to different orders, carpon, while Sphinctrina leucopoda is known from Per­ such as Corynespora laevistipitata, Etayoa trypethelii, tusaria and Diploschistes; in both cases, further studies Lichenodiplis lecanorae, Marchandiomyces corallinus, may reveal that populations from different hosts repre- Ovicuculispora parmeliae or Taeniolella delicata. Two sent genetically distinct species. All other known species species appear to be specialized on a small number of have been reported from a single Graphidales host genus. hosts, including Graphidales but also species from other Amongst these, eight were known from Diploschistes, eight from Graphis, five fromPhaeographis and 12 from Thelotrema. Each of the genera Acanthothecis, Anomo­ 1 Musée national d’histoire naturelle, 25 rue Munster, L-2160 Luxem- morpha, Chapsa, Diorygma, Fissurina, Nitidochapsa, bourg, Luxembourg Pallidogramme, Reimnitzia and Sarcographa were known 2 534 Fenton St, Lansing, MI 48910, USA 3 Martin-Luther-Universität, Institut für Biologie, Bereich Geobotanik, to host one lichenicolous species. Herbarium, Neuwerk 21, 06099 Halle (Saale), Germany Over many years, the second author has collected 4 Departamento de Biología y Geología, Universidad Rey Juan Carlos, corticolous lichens in Florida and has carefully scrutinized E-28933 Móstoles, Spain the specimens for lichenicolous fungi. Several licheni- 5 Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai Street, 51005 Tartu, Estonia colous species have already been published in previous 6 Meise Botanic Garden, Department of Research, Nieuwelaan 38, papers: Etayoa trypethelii (Ertz et al. 2014), Taeniolella B-1860 Meise, Belgium delicata (Heuchert et al. 2018), T. hawksworthiana (Ertz 7 Fédération Wallonie-Bruxelles, Direction Générale de l’Enseignement et al. 2016), Tremella graphidis, T. phaeographinae and non obligatoire et de la Recherche scientifique, rue A. Lavallée 1, B-1080 Bruxelles, Belgium T. pyrenulae (Ariyawansa et al. 2015). The aim of this * Corresponding author e-mail: [email protected] paper is to publish all species of lichenicolous fungi This work is licensed under the Creative Commons BY-NC-ND 4.0 License 250 Plant and Fungal Systematics 64(2): 249–282, 2019 collected and identified on Graphidales hosts in Florida, were purified with Exosap in Macrogene Inc. (Amster- to describe one new genus and 10 new species, and to dam, the Netherlands). Genomic DNA from Skyttea spec- present an identification key to all lichenicolous fungi imens was extracted from ascomata of dried herbarium known to inhabit Graphidales hosts. specimens, 3–4 ascomata per reaction, using a High Pure General information on the lichen flora from Flor- PCR Template Preparation Kit (Roche Applied Science, ida can be found in many papers, such as DeBolt et al. Penzberg, Germany) and following the protocol provided (2007), Harris (1990, 1995) or Seavey and Seavey (2019). by the manufacturer. The internal transcribed spacer (ITS) More specific information on the lichens of Fakahatchee was amplified using primers ITS0F (Tedersoo et al. 2008) Strand Preserve State Park, one of the richest localities or ITS1F (Gardes & Bruns 1993) and ITS4 (White et al. in Florida for ‘graphidicolous’ fungi, can be found in 1990). The PCR reaction mix (25 μL) consisted of 5 μL Lücking et al. (2011). 5× HOT FIREPol Blend Master Mix (Solis BioDyne, Tartu, Estonia), 0.5 μL of both primers (both at a con- Material and methods centration of 20 μM), 3 μL of target DNA, and distilled water up to the total volume. The PCR cycle consisted Morphological examination of 36 cycles and annealing temperature was set at 57°C. Almost all specimens studied in this paper were collected For purification of PCR products, 1 μL of FastAP and 0.5 by the second author (R. C.); these are kept in BR, MSC μL of exonuclease I (Thermo Scientific, Waltham, MA, and/or in the private herbarium of P. Diederich (Luxem- USA) were added per 20 μL of the product, and the tubes bourg), with some duplicates in HAL and S. Additional were incubated at 37°C for 45 min; the enzymes were specimens have been obtained on loan from NY and deactivated by heating at 85°C for 15 min. SBBG. Specimens collected by R. Common are abbre- DNA sequencing of both complementary strands was viated C, followed by the collection number. For all other performed in Macrogen Inc. (Amsterdam, the Nether- specimens the collector is indicated. lands) with the same primer set as for amplifications to Macroscopic photographs were obtained using a Canon generate Tremella sequences; primers LIC15R (Miad- 40D camera (Tokyo, Japan) with Nikon BD Plan 10 or likowska et al. 2002), LR3 and LR6 (Vilgalys & Hester Nikon M Plan 40 ELWD microscope objectives (Tokyo, 1990) for Lawreya sequences; and primers ITS4 and ITS5 Japan), StackShot (Cognisys, MI, USA) and Helicon Focus (White et al. 1990) for Skyttea sequences. (HeliconSoft, Kharkiv, Ukraine) for increasing the depth of field (P. Diederich); or a Keyence VHX-5000 digital Sequence alignment and phylogenetic analyses microscope and a VH-Z20R/W/T lens (Osaka, Japan) Twelve new Tremella sequences (6 ITS and 6 nLSU (D. Ertz); or a Wild Heerbrugg M400 Photomakroskop rDNA) were edited and assembled using Geneious ver. (Heerbrugg, Switzerland) fitted with an Apozoom objec- 6.1.2 (Biomatters Ltd., Auckland, NZ). Assembly of the tive and a Nikon D700 digital camera (Tokyo, Japan), nuclear rDNA included the whole ITS and a continued using Zerene Stacker (Zerene Systems, WA, USA) for fragment of ~1000 bp in the nLSU region. Sequencher increasing the depth of field (R. Common). Hand-made ver. 4.10.1 (GeneCodes Corp.®, Ann Arbor, MI, USA) was sections of ascomata and thallus were studied in tap water, used to check, assemble and manually adjust the resulting 5% KOH (K), Lugol’s reagent (1% I2) without (I) or with sequence fragments of four new Skyttea sequences, and KOH pre-treatment (K/I), lactophenol-cotton blue (LCB), Sequencher ver. 5.3 of three new Lawreya sequences. The Congo Red or phloxine B. Measurements based on statisti- consensus sequences generated for this study are deposited cal data are indicated as (minimum–) X-sd – X+sd (–max- in GenBank (https://www.ncbi.nlm.nih.gov/genbank/). imum), where X represents the arithmetic mean and sd the The new Tremella sequences were aligned together corresponding standard deviation, followed by the number with sequences already available in GenBank (Table 1). of measurements (n); the length/breadth ratio is indicated After a preliminary alignment including all regions, as L/B and given in the same way. Microscopic photo- the ITS1, 5.8S, ITS2 and nLSU regions were identified graphs were prepared using a Leica DMLB microscope and aligned separately using the Q-INS-I (for ITS1 and (Wetzlar, Germany) with interference contrast, fitted with ITS2), and the G-INS-i (for 5.8S and nLSU) algorithms a Leica EC3 camera (P. Diederich); or an Olympus BX51 in MAFFT ver. 7 multiple sequence alignment software microscope (Tokyo, Japan) with interference contrast, (Katoh & Toh 2008). The 5.8S region was considered connected to an Olympus Color View I digital camera unambiguously
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