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Reconsideration of Protocrea (Hypocreales, Hypocreaceae)

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Reconsideration of Protocrea (Hypocreales, Hypocreaceae) Mycologia, 100(6), 2008, pp. 962–984. DOI: 10.3852/08-101 # 2008 by The Mycological Society of America, Lawrence, KS 66044-8897 Reconsideration of Protocrea (Hypocreales, Hypocreaceae) Walter M. Jaklitsch1 INTRODUCTION Faculty Centre for Systematic Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria Hypocrea typically consists of a teleomorph, the stroma of which is usually no more than a few Kadri Po˜ldmaa millimeters in diameter and includes primarily Natural History Museum, University of Tartu, pseudoparenchymatous tissue, bicellular ascospores Vanemuise 46, EE-51014, Tartu, Estonia that disarticulate at the septum and a Trichoderma Gary J. Samuels Pers. anamorph with green or, less frequently, United States Department of Agriculture, Agricultural colorless (white in mass) conidia. However several Research Service, Systematic Mycology and Microbiology described species vary from this stereotype in having Laboratory, Room 304, B-011A, BARC-W, Beltsville, effused stromata or a subiculum and/or having Maryland 20705 acremonium-, verticillium- or gliocladium-like ana- morphs. Segregate genera have been proposed for some of these species, including Protocrea and Abstract: The genus Protocrea is redefined, based on Arachnocrea Moravec, but in the absence of critical holotype and fresh specimens of its type species P. study, the paucity of specimens and the lack of farinosa, using morphology of teleomorph and cultures that elucidate anamorphs while providing anamorph and phylogenetic analyses of rpb2 sequenc- molecular phylogenetic information correct applica- es. Data based on currently available specimens tion of these generic names and assignment of species suggest the existence of three well defined and three has been haphazard. still unnamed species. Apart from the type, P. Petch (1937) erected the genus Protocrea including farinosa, none of the species originally included are Hypocrea farinosa Berk. & Broome, H. delicatula Tul. accepted in the genus. Species of Protocrea are and H. stipata (Lib.) Fuckel. He did not indicate a characterized by perithecia formed in or on a type species. Moravec (1956) lectotypified the genus subiculum, bicellular ascospores that disarticulate at with P. farinosa, while retaining P. delicatula and the septum while still in the ascus and by anamorphs removing P. stipata to his new genus Arachnocrea, the belonging to Gliocladium sensu stricto. For Hypocrea latter characterized by disarticulating biconical asco- farinosa sensu auct. the new species H. decipiens is spores. Po˜ldmaa (2000) provided molecular phyloge- introduced. Hypocrea pallida is recognized as a species netic evidence that the type species of Arachnocrea, A. of Protocrea. It is closely related to P. farinosa, stipata, having a verticillium-like anamorph (Po˜ldmaa morphologically, phylogenetically and by habit. Pro- 1999), is distinct from Hypocrea, including H. pallida. tocrea illinoe¨nsis is described here as the sister taxon Hypocrea delicatula in contrast belongs to Hypocrea, of P. farinosa found in the USA. All species are based on gene sequences and a verticillium-like polyporicolous, with the principal hosts Skeletocutis (Trichoderma sect. Hypocreanum) anamorph (W. nivea for P. farinosa and P. illinoe¨nsis, and species of Jaklitsch, unpubl) and will be treated elsewhere. Oligoporus/Tyromyces for P. pallida. In addition to Overton et al (2006b) epitypified Protocrea, but as hosts the main differences among these species are a we will demonstrate this epitypification was based on stronger (orange) pigmentation of perithecia and misidentified material and must be overturned. subiculum in P. pallida and a violaceous KOH Another common species similar to P. farinosa, reaction in P. pallida and P. illinoe¨nsis. P. farinosa is producing perithecia in a subiculum and a Gliocladi- known only from Europe with certainty and P. um anamorph, and occurring on polypores is illinoe¨nsis only from the USA, while P. pallida is Hypocrea pallida. Based on LSU ribosomal DNA probably cosmopolitan. Putative synonymy of some sequences, the species was found to fall outside similar species is discussed. Hypocrea in the Hypocreaceae, but no generic Key words: Ascomycetes, Gliocladium, Hypocrea, redisposition has been suggested for it (Rehner and Hypocreales, ITS, LSU, morphology, phylogeny, Samuels 1994, Po˜ldmaa et al 1999, Po˜ldmaa 2000). rpb2, sequence analysis, systematics, tef1 The main objectives of this study are (i) the correct interpretation, conceptual definition and description of the genus Protocrea and its type species P. farinosa, Accepted for publication 29 July 2008. (ii) to determine the phylogenetic position of 1 Corresponding author. E-mail: [email protected] Protocrea and ‘Hypocrea’ pallida and (iii) to describe 962 JAKLITSCH ET AL:RECONSIDERATION OF PROTOCREA 963 the fungus interpreted as Hypocrea farinosa by recent nuclear rDNA, containing the ITS1 and 2 regions, was authors as a new species of Hypocrea. amplified by PCR with the primer combinations SR6R and LR1 (White et al 1990) or with ITS4 (White et al 1990) and ITS1F (Gardes and Bruns 1993). LSU rDNA was amplified MATERIALS AND METHODS with the latter primer in combination with LR5 (http:// www.biology.duke.edu/fungi/mycolab/primers.htm). A Isolates and specimens.—Isolates and GenBank accession 1.3 kb fragment of the tef1 gene encoding translation numbers for ITS, LSU, rpb2 and tef1 sequences in this study elongation factor 1 alpha was amplified with the primer pair are listed (TABLE I). Isolates given as C.P.K. (Kubicek) are those maintained in the collection of the Institute of EF1728F and TEF1LLErev (Jaklitsch et al 2005, 2006). This Chemical Engineering, Vienna University of Technology, fragment includes the fourth and the fifth introns and a those listed as G.J.S. are those maintained at the USDA-ARS, part of the last large exon. A 0.9 kb fragment of RNA Systematic Mycology and Microbiology Laboratory, Belts- polymerase II subunit B (rpb2) was amplified with the ville, Maryland, and those given as TFC are maintained at primer pair fRPB2-5f and fRPB2-7cr (Liu et al 1999). PCR the University of Life Sciences, Tartu, Estonia. Representa- products either were purified with the QIAquick Kit tive isolates have been deposited at the Centraalbureau voor (QIAGEN) according to the manufacturer’s instructions Schimmelcultures, Utrecht, The Netherlands (CBS). Spec- or with an enzymatic PCR cleanup (Werle et al 1994). For imens were deposited in the Herbarium of the Institute of the latter 20 mL PCR reactions were digested with 10 u Botany, University of Vienna, Austria (WU), in the U.S. exonuclease I (Fermentas, St Leon-Rot, BRD) and 2 u calf National Fungus Collections, Beltsville, Maryland (BPI), or intestine alkaline phosphatase (Fermentas) for 45 min at the Estonian University of Life Sciences, Tartu, Estonia 37 C, followed by an enzyme deactivation step at 85 C for (TAA). 15 min. DNA was cycle-sequenced with the ABI PRISM Big Single-ascospore isolates (C.P.K., CBS strains) were Dye Terminator Cycle Sequencing Ready Reaction Kit v. 3.1 prepared from fresh specimens of Hypocrea stromata as (Applied Biosystems, Warrington) with the same primers as described by Jaklitsch et al (2006), or a mass of ascospores in PCR, or with ITS4 and ITS5 (White et al 1990) for ITS, or was isolated onto 2% MEA (TFC strains). Cultures with the internal primers 59-CCGTGA(T/C)TT CATCAA- designated G.J.S. were isolated with the use of a microma- GAACATG-3 and 59-TTGGCAGTGTCCATCTT GTTG-39 for nipulator on cornmeal agar (Difco) supplemented with 2% tef1, and an automated DNA sequencer (ABI Genetic dextrose (CMD). Analyzers, Applied Biosystems). Growth characterization.—Strains were cultivated on CMD Molecular phylogenetic analyses.—Sequence fragments were (cornmeal agar, Sigma, St Louis, Missouri) supplemented analyzed and assembled with SeqMan Pro (Lasergene, with 2% (w/v) dextrose), PDA (potato-dextrose agar, DNASTAR, Madison, Wisconsin) or Sequencher 4.7 (Gene Merck, Darmstadt, Germany) and 2% MEA (malt extract Codes, Ann Arbor, Michigan). DNA sequences were agar, Merck), all in distilled water. Growth took place at submitted to GenBank. Alignments were performed with 25 C (alternating 12 h cool white fluorescent light and 12 h MAFFT v 6.240 (Katoh et al 2005), followed by manual darkness). adjustments with Genedoc 2.6 (Nicholas et al 1997). Maximum parsimony (MP) analyses were conducted in Morphological observations.—Structures of the anamorph PAUP* 4.0b10 (Swofford 2002) with 10000 heuristic were examined, measured and photographed on a com- searches with random taxon addition sequences and TBR pound microscope from cultures grown on CMD or PDA at branch swapping. The confidence of branching was assessed 25 C on the plates under low magnification and after with bootstrap resampling (bs): 1000 replicates, each with mounting in 3% KOH. Dry stromata were rehydrated 100 random taxon addition sequences. Gaps were treated as overnight by water vapor in a TLC chamber at room missing data. temperature, imbedded in Tissue-Tek O.C.T. Compound Bayesian inference of phylogeny was performed with LSU 4583 (Sakura Finetek Europe B.V., Zoeterwoude, The rDNA and rpb2 sequences of 25 members of the Hypocrea- Netherlands) and sectioned 12 mm thick with a freezing ceae and with the combined dataset of 19 Protocrea microtome. Sections were measured and photographed in sequences using MrBayes 3.1.2 (Huelsenbeck and Ronquist lactic acid, asci and ascospores in 3% KOH. Measurements 2001,
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