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New Insights Into Classification and Evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from Phylogenetic Analyses Of

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New Insights Into Classification and Evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from Phylogenetic Analyses Of Mycologia, 98(6), 2006, pp. 1088–1103. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes Jolanta Miadlikowska1 Soili Stenroos Frank Kauff Botanical Museum, Finnish Museum of Natural Vale´rie Hofstetter History, University of Helsinki, P.O. Box 7, FI-00014 Emily Fraker Finland Department of Biology, Duke University, Durham, Irwin Brodo North Carolina 27708-0338 Canadian Museum of Nature, P.O. Box 3443, Station Martin Grube D, Ottawa, Ontario, K1P 6P4 Canada Josef Hafellner Gary B. Perlmutter Institut fu¨ r Botanik, Karl-Franzens-Universita¨t, North Carolina Botanical Garden, University of North Holteigasse 6, A-8010, Graz, Austria Carolina at Chapel Hill, CB 3375, Totten Center, Chapel Hill, North Carolina 27599-3375 Vale´rie Reeb Brendan P. Hodkinson Damien Ertz Department of Biology, Duke University, Durham, National Botanic Garden of Belgium, Department of North Carolina 27708-0338 Bryophytes-Thallophytes, Domaine de Bouchout, B-1860 Meise, Belgium Martin Kukwa Department of Plant Taxonomy and Nature Paul Diederich Conservation, Gdansk University, A. Legionow 9, Muse´e national d’histoire naturelle, 25 rue Munster, 80-441 Gdansk, Poland L-2160 Luxembourg, Luxembourg Robert Lu¨cking James C. Lendemer Field Museum of Natural History, 1400 South Lake Department of Botany, Academy of Natural Sciences of Shore Drive, Chicago, Illinois 60605-2496 Philadelphia, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103 Geir Hestmark Department of Biology, University of Oslo, P.O. Box Philip May 1066 Blindern, NO-0316 Oslo, Norway Farlow Herbarium, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts 02138 Monica Garcia Otalora A´ rea de Biodiversidad y Conservacio´n, ESCET, Conrad L. Schoch Universidad Rey Juan Carlos, c/ Tulipa´n s/n, Department of Botany and Plant Pathology, Oregon 28933-Mo´stoles, Madrid, Spain State University, Corvallis, Oregon Alexandra Rauhut A. Elizabeth Arnold Burkhard Bu¨del Department of Plant Sciences, University of Arizona, Fachbereich Biologie, Abt. Pflanzeno¨kologie und 1140 E. South Campus Drive, Forbes 204, Tucson, Systematik, University of Kaiserslautern, Postfach Arizona 85721 3049, 67653 Kaiserslautern, Germany Ce´cile Gueidan Christoph Scheidegger Erin Tripp Swiss Federal Institute for Forest, Snow and Landscape Rebecca Yahr Research (WSL/FNP), Zu¨ rcherstrasse 111, 8903 Connie Robertson Birmensdorf, Switzerland Franc¸ois Lutzoni Einar Timdal Department of Biology, Duke University, Durham, North Carolina 27708-0338 Botanical Museum, University of Oslo, Sars’ gate 1, N-1162 Oslo, Norway Abstract: The Lecanoromycetes includes most of the lichen-forming fungal species (.13 500) and is therefore one of the most diverse class of all Fungi Accepted for publication 15 October 2006. in terms of phenotypic complexity. We report phylo- 1 Corresponding author. E-mail: [email protected] genetic relationships within the Lecanoromycetes 1088 MIADLIKOWSKA ET AL:SYSTEMATICS OF THE LECANOROMYCETES 1089 resulting from Bayesian and maximum likelihood ascal wall of which two layers are thick enough to be analyses with complementary posterior probabilities visible with light microscopy and display different types and bootstrap support values based on three com- of dehiscence (predominantly rostrate but also semi- bined multilocus datasets using a supermatrix ap- fissitunicate or bilabiate), however some members proach. Nine of 10 orders and 43 of 64 families (calicioid lichen-forming fungi, such as Calicium and currently recognized in Eriksson’s classification of the Sphaerophorus) produce asci with a single evanescent Lecanoromycetes (Outline of Ascomycota—2006 My- layer (Luttrell 1955; Eriksson 1981; Reynolds 1981, conet 12:1–82) were represented in this sampling. Our 1989; Tibell 1984; Hafellner 1988). analyses strongly support the Acarosporomycetidae Members of the Lecanoromycetes form bipartite and Ostropomycetidae as monophyletic, whereas the symbiotic associations with a broad range of photo- delimitation of the largest subclass, the Lecanoromy- bionts, representing chlorococcalean algae (Astero- cetidae, remains uncertain. Independent of future chloris, Coccomyxa s.l., Dictyochloropsis s.l. and Tre- delimitation of the Lecanoromycetidae, the Rhizocar- bouxia, are the most frequent genera), filamentous paceae and Umbilicariaceae should be elevated to the algae (Trentepohlia, Phycopeltis) and cyanobacteria ordinal level. This study shows that recent classifica- (Calothrix, Nostoc, Scytonema and Stigonema) (e.g. tions include several nonmonophyletic taxa at differ- Tschermak-Woess 1988; Rikkinen 1995; Beck et al ent ranks that need to be recircumscribed. Our 1998, 2002; Rambold et al 1998; Persˇoh et al 2004; phylogenies confirm that ascus morphology cannot Cordeiro et al 2005). Tripartite symbioses with be applied consistently to shape the classification of cyanobacteria as the secondary photobiont (in terms lichen-forming fungi. The increasing amount of of relative abundance in mature thalli) occur in missing data associated with the progressive addition several unrelated genera within the Lecanoromycetes, of taxa resulted in some cases in the expected loss of however they are particularly common in peltiger- support, but we also observed an improvement in alean lichens (Peltigerales). Rambold et al (1998) statistical support for many internodes. We conclude suggested that photobionts associated with lichen- that a phylogenetic synthesis for a chosen taxonomic forming fungi could be used in lichen systematics. group should include a comprehensive assessment of These authors detected a strong selectivity of myco- phylogenetic confidence based on multiple estimates bionts with respect to their photobionts at the rank of using different methods and on a progressive taxon families and genera in the order Lecanorales. sampling with an increasing number of taxa, even if it Most members of the Lecanoromycetes are known involves an increasing amount of missing data. to produce a wide variety of unique secondary Key words: Bayesian inference, Lecanoromy- compounds, especially polyketide derivatives (such cetes, lichen-forming ascomycetes, maximum likeli- as depsides and depsidones, anthraquinones and hood, missing data, mitochondrial ribosomal small xanthones) terpenes and pulvinic acid derivatives subunit (mitSSU), molecular phylogenetic classifica- (e.g. Elix 1996). These chemical compounds are of tion, nuclear ribosomal large subunit (nucLSU), biological and ecological importance (especially if nuclear ribosomal small subunit (nucSSU), phenoty- present in the upper cortex of lichen thalli; e.g. pic characters, photobionts, phylogenetic confiden- Rundel 1978, Lawrey 1986, Solhaug and Gauslaa ce, phylogeny, RNA polymerase II largest subunit 1996, Po¨ykko¨ et al 2005) and of systematic (e.g. Elix (RPB1), RNA polymerase II second largest subunit 1993, Culberson and Culberson 1994, Schmitt and (RPB2) Lumbsch 2004) and evolutionary significance (e.g. Culberson 1986). Circumscription and ranking of subgroups within INTRODUCTION the Lecanoromycetes varied in previous classifications, The Lecanoromycetes, as recognized in Eriksson’s and the last major improvement before molecular (2006) classification, is the largest class of Fungi. It phylogenetic studies was derived from the study of includes the majority (about 90%) of all described reproductive structures, in particular the apical struc- lichen-forming Ascomycota (estimated to be . 13 500 tures of asci. These characters were used to delineate species, Kirk et al 2001). A common character uniting groups of lichen-forming fungi and resulted in a high members of this class is their ascohymenial ascomatal number of families in the Lecanorales (Hafellner ontogeny, with a predominance of apothecial fruiting 1984). Because of controversy associated with the bodies, although of diverse construction and shape. uniform implementation of these characters to cir- Perithecioid ascomata are known in only four of 64 cumscribe families across the Lecanorales (e.g. Timdal families (Grube et al 2004, Schmitt et al 2005) of 1991) many families were redefined (e.g. Rambold and Eriksson’s (2006) classification and in a few unclassi- Triebel 1992, Hafellner 1993). fied genera. In most lineages asci have a multilayered Molecular studies have substantially challenged 1090 MYCOLOGIA phenotypically based groupings applied to previous small subunit [mitSSU]) (e.g. Lumbsch et al 2001, classifications, as well as resolved placement of many 2004a; Lutzoni et al 2001; Ekman and Tønsberg 2002; sterile taxa, and taxa with uncertain taxonomic Kauff and Lutzoni 2002; Lumbsch 2002; Lu¨cking et al affiliation. The Lecanoromycetes include a minimum 2004; Wedin et al 2005) with only four phylogenetic of three subclasses, the Acarosporomycetidae, Ostro- studies using at least one protein coding gene (RPB2: pomycetidae and Lecanoromycetidae, according to Liu and Hall 2004, Lutzoni et al 2004 and Reeb et al Reeb et al (2004) and Lutzoni et al (2004). The 2004; RPB1andRPB2: Hofstetter et al 2007). Acarosporomycetidae encompasses a single family, Hofstetter et al (2007) evaluated the phylogenetic the Acarosporaceae, defined in most cases by the contribution (resolving power and statistical confi- presence of a crustose or squamulose thallus, a chlor- dence) provided by protein-coding (RPB1
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