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Phylogenetic Classification of Peltigeralean Fungi (Peltigerales,Ascomycota) Based on Ribosomal Rna Small and Large Subunits1

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Phylogenetic Classification of Peltigeralean Fungi (Peltigerales,Ascomycota) Based on Ribosomal Rna Small and Large Subunits1 American Journal of Botany 91(3): 449±464. 2004. PHYLOGENETIC CLASSIFICATION OF PELTIGERALEAN FUNGI (PELTIGERALES,ASCOMYCOTA) BASED ON RIBOSOMAL RNA SMALL AND LARGE SUBUNITS1 JOLANTA MIADLIKOWSKA2,3,4 AND FRANCËOIS LUTZONI2 2Department of Biology, Duke University, Durham, North Carolina 27708-0338 USA; and 3Plant Taxonomy and Nature Conservation, Gdansk University, Al. Legionow 9, 80-441 Gdansk, Poland To provide a comprehensive molecular phylogeny for peltigeralean fungi and to establish a classi®cation based on monophyly, phylogenetic analyses were carried out on sequences from the nuclear ribosomal large (LSU) and small (SSU) subunits obtained from 113 individuals that represent virtually all main lineages of ascomycetes. Analyses were also conducted on a subset of 77 individuals in which the ingroup consisted of 59 individuals representing six families, 12 genera, and 54 species potentially part of the Peltigerineae/ Peltigerales. Our study revealed that all six families together formed a strongly supported monophyletic group within the Lecanoro- mycetidae. We propose here a new classi®cation for these lichens consisting of the order Peltigerales and two subordersÐCollematineae subordo nov. (Collemataceae, Placynthiaceae, and Pannariaceae) and Peltigerineae (Lobariaceae, Nephromataceae, and Peltigeraceae). To accommodate these new monophyletic groups, we rede®ned the Lecanorineae, Pertusariales, and Lecanorales sensu Eriksson et al. (Outline of AscomycotaÐ2003, Myconet 9: 1±103, 2003). Our study con®rms the monophyly of the Collemataceae, Lobariaceae, Nephromataceae, and Peltigeraceae, and the genera Nephroma, Sticta, and Peltigera. However, Leptogium, Lobaria, Pseudocyphellaria, and Solorina were found to be nonmonophyletic genera. Reconstruction of ancestral symbiotic states within the Peltigerales, using maximum likelihood (ML) and a Bayesian approach to account for phylogenetic uncertainty, revealed an evolutionary scenario in which bimembered associations with cyanobacteria were ancestral, followed by multiple independent acquisitions of green algae to form tripartite symbioses and rare subsequent losses of the cyanobiont to form bimembered symbioses with green algae. Key words: ancestral state reconstruction; Collematineae; Lecanoromycetidae; lichen symbiosis; molecular phylogenetic classi- ®cation of ascomycetes; nuclear ribosomal large (LSU nrDNA) and small (SSU nrDNA) subunits; Peltigerales; Peltigerineae. Peltigeralean lichen-forming fungi (Peltigerineae/Peltigera- (Schreber) Ach., Lobaria (Schreber) Hoffm., Psoroma Mi- les W. Watson, Ascomycota) are generally characterized by chaux, and Peltigera Willd.] can also form a cyanomorph thal- foliose, subfruticose, or granular-squamulose thalli; the pres- lus, in which the same fungus is associated with only the cy- ence of rhizines or tomentum on the lower side of the thalli; anobacterial partner, forming a bipartite thallus that is attached predominantly multiseptate, colorless or brown ascospores or growing separately from the mother tripartite thallus formed in asci with some lecanoralean features, i.e., reactive (Tùnsberg and Holtan-Hartwig, 1983; White and James, 1988; a-layer and thick c-layer; and mostly unbranched and free pa- Armaleo and Clerc, 1991; Gof®net and Bayer, 1997; Paulsrud raphyses. This group contains both bipartite (one mycobiont et al., 1998, 2000; Holien and Jùrgensen, 2000). Peltigeralean and one photobiont) and tripartite lichens (one mycobiont and lichens are worldwide in distribution; however, the Lobari- two photobionts). Cyanobacteria (Nostoc Vauch., Scytonema aceae Chevall. are most abundant and diverse in the Southern Agardh, or less commonly, Dichotrix Zanardini) are the pho- Hemisphere, whereas other families (e.g., Peltigeraceae Du- tobionts most frequently found in thalli of bipartite peltigera- mort.) are more common and diverse in the Northern Hemi- lean species or are restricted to internal or external cephalodia sphere. These lichens grow on various substrates: mosses, in tripartite species in which a green alga is the main photo- rocks, soil, or bark, and mostly in moist to humid wooded biont (e.g., Tschermak-Woess, 1988; Rai, 1990; Schenk, habitats. 1992). Bipartite fungal symbioses with green algae (usually All lecanoralean taxa having cyanobacteria as their main Coccomyxa LeÂger & Hesse, Dictyochloropsis Geitler, or Myr- photobiont are part of the suborder Peltigerineae (recognized mecia Printz) are relatively rare in these lichens (e.g., Tscher- also at the ordinal level Peltigerales; Kirk et al., 2001) when mak-Woess, 1988; Ahmadjian, 1993). The mycobiont of sev- broadly delimited. This broad circumscription of the Peltig- eral tripartite peltigeralean lichens [Nephroma Ach., Sticta erineae/Peltigerales includes 7±8 families (Rambold and Trie- bel, 1992; Tehler, 1996; J. Hafellner, H. Hertel, G. Rambold, 1 Manuscript received 1 July 2003; revision accepted 24 October 2003. and E. Timdal, unpublished manuscript), whereas the narrow The authors thank Bruce McCune, Trevor Goward, Orvo Vitikainen, Pak delimitation of this taxonomic group (Table 1) includes only Yau Wong, ValeÂrie Reeb, Walter Obermayer, Urszula Bielczyk, Pawel Czar- 3±5 families (Henssen and Jahns, 1973; Poelt, 1974; Hafellner, nota, Stanislaw Cieslinski, Wieslaw Faltynowicz, Martin Kukwa, Claude Roy, Richard Helliwell, and Mikhail Zhurbenko, who generously provided material 1988; Kirk et al., 2001; Eriksson et al., 2003). Differences in for this study. We are grateful to Martin Grube and Josef Hafellner for valu- family numbers within the two major types of delimitations able comments, as well as Molly McMullen and A. Elizabeth Arnold for are due in part to the recognition of separate families for So- proofreading the manuscript. We are indebted to Josef Hafellner for providing lorina Ach. and Nephroma (Solorinaceae Bayrh. and Nephro- the Latin translation. This research was ®nancially supported by NSF grants mataceae Wetm. ex J. C. David & D. Hawksw., respectively) (DEB-9615542 and DEB-0133891) to F. L. and the Kosciuszko Foundation instead of being classi®ed within the Peltigeraceae sensu lato Scholarship (1999/2000) to J. M. Sequences were generated in the Pritzker Laboratory for Molecular Systematics and Evolution at the Field Museum, (Table 1). No matter how the Peltigeraceae and Lobariaceae Chicago. (5 Stictaceae sensu Henssen and Jahns, 1973) have been de- 4 E-mail: [email protected]. limited, they have been always included within the Peltigeri- 449 450 AMERICAN JOURNAL OF BOTANY [Vol. 91 TABLE 1. Families included in the Peltigerineae/Peltigerales according to selected classi®cations/molecular phylogenetic studies compared to the classi®cation proposed here. Eriksson Henssen and Poelt, Hafellner, Rambold and Hafellner Tehler, Kirk et al., et al., Wiklund and This Taxon Jahns, 1973 1974 1988 Triebel, 1992 et al.a 1996 2001 2003 Wedin, 2003 study Peltigerales 2 2 1 2 2 2 1 2 2 1 Peltigerineae 1 1 2 1 1 1 2 1 1 1 Collematineae 2 2 2 2 2 2 2 2 2 1 Peltigeraceae 1b,c,d 1b 1 1b 1 1b,d 1b 1b 1b 1b Solorinaceae 2 2 1 2 1 2 2 2 2 2 Lobariaceae 1 1 1 1 1 1 1 1 1 1 Nephromataceae 2 1 1 1 1 1 1 1 1 1 Placynthiaceae 1 1e 1 1 1 1 1 1 1 1 Pannariaceae 2 2 2 1f 1f 1 2 2 1 1 Coccocarpiaceae 2 2 2 1 1 1 2 2 1 (1)g Collemataceae 2 2 2 1 1 1 2 2 1 1 Massalongia 22 ??1222 1 1 a J. Hafellner, H. Hertel, G. Rambold, and E. Timdal, unpublished manuscript. b Solorinaceae included. c Nephromataceae excluded. d Massalongia included. e Massalongia and Psoroma included. f Psoroma excluded. g Based on Wiklund and Wedin (2003). neae/Peltigerales. All authors listed in Table 1 also consider amyloid (I1) caplike structure. The Nephromataceae, with its the family Placynthiaceae AÊ . E. Dahl as part of the Peltigeri- nassasceous ascus, is the only family lacking an amyloid apical neae/Peltigerales; however, Hafellner (1988; 5 Lecotheciaceae structure within the Peltigerineae/Peltigerales (Poelt, 1974; KoÈrber) suggested that this taxon may not belong in this BellemeÁre and Letrouit-Galinou, 1981; Rambold and Triebel, group. Three additional families, Coccocarpiaceae (Mont. ex 1992). The ®ssitunicate type of dehiscence detected in Peltig- MuÈll. Stuttg.) Henssen, Collemataceae Zenker, and Pannari- era using transmission electron microscopy (Honegger, 1978) aceae Tuck., are sometimes considered as members of the Pel- is believed to occur also in the Nephromataceae (Nephroma), tigerineae/Peltigerales (Rambold and Triebel, 1992; Tehler, Solorina saccata (L.) Ach., and Lobariaceae (Lobaria and 1996; J. Hafellner, H. Hertel, G. Rambold, and E. Timdal, Sticta) based on evidence obtained with light microscopy unpublished manuscript). Otherwise, these three families have (Richardson, 1970; Eriksson, 1981). been placed within the heterogenous Lecanorales Nannf. The distribution of secondary compounds across families (Poelt, 1974; Hafellner, 1988; Kirk et al., 2001), or more spe- within the broad selection of peltigeralean lichens sensu lato ci®cally in the suborder Lecanorineae (Eriksson et al., 2003). (s.l.) is heterogeneous. A great diversity of secondary com- Circumscriptions of families within the Peltigerineae/Peltig- pounds is found within the Peltigeraceae, Nephromataceae, erales differ considerably among recent classi®cations. Only and Lobariaceae (e.g., Culberson, 1969, 1970; Yoshimura, the family Lobariaceae, with Lobaria, Pseudocyphellaria Vai- 1971; James and White, 1987; Galloway, 1988, 1991; White nio, and Sticta, was consistently de®ned as such in all systems. and James,
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