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Nrm.Diva-Portal.Org http://www.diva-portal.org This is the published version of a paper published in The Lichenologist. Citation for the original published paper (version of record): Otálora, M A., Wedin, M. (2013) Collema fasciculare belongs in Arctomiaceae. The Lichenologist, 45(3): 295-304 http://dx.doi.org/10.1017/S0024282912000849 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:nrm:diva-65 The Lichenologist 45(3): 295–304 (2013) 6 British Lichen Society, 2013 doi:10.1017/S0024282912000849 Collema fasciculare belongs in Arctomiaceae Mo´nica A. G. OTA´ LORA and Mats WEDIN Abstract: The phylogenetic placement of Collema fasciculare (L.) F. H. Wigg, the most deviating species within Collema (Collemataceae, Lecanoromycetidae), was studied using maximum likelihood and Bayesian analysis of three molecular loci (mitochondrial SSU rDNA, and the protein-coding, nuclear RPB1 and MCM7 genes). Collema fasciculare belongs to Arctomiaceae (Ostropomycetidae) forming a strongly supported monophyletic group with members of Arctomia. The spores, paraphyses, asci and hymenial reactions in Collema fasciculare are similar to other Arctomia, but the ascoma ontogeny is somewhat different. Also C. leptosporum Malme, another species in the Fasciculare group, shows similarities with Arctomia regarding spores and asci. Arctomia is morphologically hetero- geneous and the genus is in need of revision. Until then, the species of the Fasciculare group fit best in Arctomia s. lat. and the combinations Arctomia fascicularis (L.) Ota´lora & Wedin, Arctomia leptospora (Malme) Ota´lora & Wedin, Arctomia papuanarum (Degel.) Ota´lora & Wedin and Arctomia uviformis (Hue) Ota´lora & Wedin are proposed. Key words: Arctomia, ascoma ontogeny, Collemataceae, cyanolichens, lichens, taxonomy Accepted for publication 21 November 2012 Introduction distinct and distantly related lineages: Arcto- miaceae (Lumbsch et al. 2005; Wedin et al. During recent decades, tremendous progress 2005) and the Peltigerales (Wedin et al. has been made in understanding relation- 2005; Mia˛dlikowska et al. 2006) in the ships among Ascomycota by using DNA Lecanoromycetes, and Lichinales in the Li- sequence data (Lutzoni et al. 2004; Mia˛dli- chinomycetes (Reeb et al. 2004). kowska et al. 2006; Hibbett et al. 2007; Although the Peltigerales is by far the most Ekman et al. 2008). As a consequence, the species-rich cyanolichen group, it contains classification of Ascomycetes has undergone lineages that have not yet been well studied. substantial changes (Hibbett et al. 2007; One of these is the Collemataceae s. str., a Kirk et al. 2008; Lumbsch & Huhndorf group of distinctly gelatinous cyanolichens 2009). In addition, the constant increase in which comprises two large genera; Collema the number of taxa in phylogenetic studies F. H. Wigg. with c. 80 currently accepted has also revealed the phylogenetic placement species, and Leptogium (Ach.) Gray with of sterile or enigmatic taxa. In the lichen- c. 180 species (Kirk et al. 2008). The detailed forming Ascomycetes associating with cyano- phylogenetic relationships within the Colle- bacteria (cyanolichens), several recent major mataceae are still unclear, despite some re- taxonomic changes have been proposed cent studies (Ota´lora et al. 2008, 2010; (Lumbsch et al. 2005; Wedin et al. 2009; Wedin et al. 2009). Although these studies Ota´lora et al. 2010; Muggia et al. 2011; have confirmed that Collema and Leptogium Spribille & Muggia 2012). Molecular phy- are non-monophyletic, they have also shown logenies suggest that cyanolichens form three that the traditional family delimitation (Hens- sen 1965; Henssen & Jahns 1974; Henssen et al. 1981) did not reflect the phylogenetic re- M. A. G. Ota´lora and M. Wedin: Cryptogamic Botany, Swedish Museum of Natural History, P.O. Box 50007, lationships. Most genera previously classified SE-104 05 Stockholm, Sweden. in Collemataceae were shown to belong to Email: [email protected] 296 THE LICHENOLOGIST Vol. 45 Pannariaceae (Wedin et al. 2009; Ota´lora et the members of the Fasciculare-group and al. 2010), and currently only Collema and other Collema species have largely been rec- Leptogium constitute the Collemataceae. ognized and accepted by other lichenologists Another group of cyanolichens that was (Filson 1992; Jørgensen 2007), no molecular earlier considered to belong to Peltigerales studies have investigated the phylogenetic is Arctomiaceae. Arctomiaceae was originally position of any member of this group. proposed by Fries (1860), but never gained The aim of this study is to investigate the wide acceptance, and Arctomia Th. Fr. was phylogenetic placement of C. fasciculare. To included in Collemataceae by Zahlbruckner achieve this we performed phylogenetic (1925). Henssen (1969), however, resurrected analyses, including representatives from the Arctomiaceae, based on differences in the two lineages of Lecanoromycetes where ascoma development between Arctomia and cyanolichens are classified (Peltigerales and Collemataceae. Molecular sequence data con- Arctomiaceae), based on sequences of the firmed that Arctomiaceae is distantly related mitochondrial SSU rDNA and the protein to Collemataceae and suggested that it belongs coding genes RPB1 (RNA polymerase II to Ostropomycetidae (Lumbsch et al. 2005; subunit 1) and MCM7. In order to identify Wedin et al. 2005). morphological characters that explain the When studying the phylogenetic relation- phylogenetic placement of C. fasciculare,we ships within Collemataceae s. str., we soon also studied the ascus structure and the found that the most deviating species re- ascoma ontogeny. In addition, we studied garding spore and apothecial characteristics material of one other species of the Fascicu- within Collema [C. fasciculare (L.) F. H. lare group, C. leptosporum, and of Arctomia s. Wigg.] not only grouped outside Collemata- str., for comparison. ceae, but also outside the Peltigerales. Prelimi- nary BLAST searches suggested similari- ties to Arctomiaceae. Collema fasciculare is a Materials and Methods widely distributed, epiphytic species, form- Specimens and markers ing rounded cushions usually up to c.2cm diam. (rarely up to 7 cm) with a crustose to We used the mtSSU rDNA, RPB1 and MCM7 loci from a total of 35 species of Lecanoromycetes. Collema subfoliose, indistinctly lobed thallus, which fasciculare was represented by four specimens originating becomes swollen and gelatinous when wet. from different parts of the world (New Zealand, Spain Similar to Collema, it associates with Nostoc, and Sweden). The other species of the Fasciculare- has a homoiomerous thallus organization group were not represented in the sampling due to the without a true cortex, lecanorine apothecia lack of recent material. Only the sequences of C. fascicu- lare were generated for this study, the rest were obtained with a persistent thalline exciple, and lacks from GenBank (Table 1). A total of 39 mtSSU rDNA, secondary metabolites. However, it differs 37 RPB1 and 23 MCM7 sequences were included in from other Collema species in some distinct this study. ascomatal traits. The paraphyses and asco- Additional material examined. Arctomia delicatula Th. spores of C. fasciculare are comparatively Fr.—Sweden: Torne Lappmark: Karesuando par., more flexuous and thinner than in other Pa¨ltsan (Bealccan). alt. 1110 m, 2011, M. Westberg Collema species (Degelius 1954, 1974), and P108 (S). the proper exciple is poorly developed or Collema leptosporum Malme.—Brazil: Mato Grosso: Corumba´, in silva clararegionis calcariae, 14 viii 1894, sometimes absent. Based on these differ- Malme [Malme Lich. austr. amer. Exs. No 70] (S). ences, Degelius proposed the informal sub- generic Fasciculare group in which he in- cluded the widely distributed species C. DNA sequencing fasciculare (Degelius 1954) and the three Total genomic DNA was extracted using DNeasy rare or poorly collected tropical species C. (Qiagen) according to the manufacturer’s instructions. The mtSSU rDNA was amplified using the primers uviforme Hue, C. papuanorum Degel., and mtSSU1 and mtSSU3R (Zoller et al. 1999); the protein C. leptosporum Malme (Degelius 1974). Al- coding gene RPB1 using primers RPB1-Af (Stiller & though the morphological differences between Hall 1997) and RPB1-6R1asc (Hofstetter et al. 2007); 2013 Collema fasciculare in Arctomiaceae—Ota´lora & Wedin 297 Table 1. List of taxa included in this study and GenBank accession numbers. New sequences are indicated in bold GenBank accession number Species mtSSU RPB1 MCM7 Arctomia borbonica 1 JX030032 JX030034 – A. borbonica 2 JX030033 JX030035 – A. delicatula AY853307 DQ870929 GQ272388 A. interfixa DQ007348 – – A. teretiuscula DQ007349 DQ870930 GQ272389 Aspicilia caesiocinerea DQ780271 DQ870931 GQ272390 A. cinerea DQ780272 DQ870932 GQ272391 Coccotrema cucurbitula AF329161 DQ870939 GU980990 C. pocillarium AF329166 DQ870940 GU980992 Collema fasciculare 1 Spain, Arago´n & Marti. 3417 (MA) KC118988 KC118991 KC118995 C. fasciculare 2 Sweden, Karstro¨m 562 (UPS) KC118987 KC118993 KC118997 C. fasciculare 3 Spain, Arago´n 1041/95 (MA) KC118989 KC118992 KC118996 C. fasciculare 4 New Zealand, Wedin 8753 (S) KC118990 KC118994 KC118998 C. furfuraceum EU982567 GQ259048 JX992982 C. nigrescens EU982563 GQ259049 JX992989 Diploschistes scruposus AY584692 DQ870943 JX000163 Graphis scripta AY853322 DQ870947 JX000164 Gregorella humida AY853329 DQ870946 – Lecanora paramerae
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