The Phylogeny of the Families Lecanoraceae and Bacidiaceae (Lichenized Ascomycota) Inferred from Nuclear SSU rDNA Sequences

S. Ekman; M. Wedin

doi:10.1055/s-2000-3703

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2000; 2(3): 350-360
DOI: 10.1055/s-2000-3703

Original Paper

Georg Thieme Verlag Stuttgart ·New York

The Phylogeny of the Families Lecanoraceae and Bacidiaceae (Lichenized Ascomycota) Inferred from Nuclear SSU rDNA Sequences

S. Ekman ¹ , M. Wedin ^{2, 3}

¹ Department of Botany, University of Bergen, Bergen, Norway
² Botany Department, The Natural History Museum, London SW7 5BD, United Kingdom
³ Present address: Department of Ecology and Environmental Science/BMG, Umeå University, Umeå, Sweden

Abstract

The phylogeny of the families Lecanoraceae and Bacidiaceae (Lecanorales, Ascomycota) was investigated using 29 nuclear small subunit ribosomal DNA sequences, 9 of which were newly determined. The data set contained 368 variable characters, 234 of which were parsimony-informative. Phylogenetic estimations were performed with maximum parsimony and maximum likelihood optimality criteria. In the most parsimonious and most likely reconstructions, the Bacidiaceae sensu Hafellner 1988 forms a monophyletic group and the Lecanoraceae sensu Hafellner a paraphyletic group. The genera Tephromela and Scoliciosporum appear to belong outside these families. However, the hypothesis that the Lecanoraceae sensu Hafellner is monophyletic cannot be rejected, as indicated by a Kishino-Hasegawa test. Three hypotheses were rejected by Kishino-Hasegawa tests, viz. (1) that the Lecanoraceae and Bacidiaceae together form a monophyletic group; (2) that both the Lecanoraceae (incl. Scoliciosporum) and Bacidiaceae (incl. Tephromela) are monophyletic; and (3) that the ascus apex anatomy reflects phylogeny. The suborder Lecanorineae is paraphyletic unless the Stereocaulaceae and Cladoniaceae are included. One or both of the Bacidia and Lecanora types of ascus have probably evolved at least twice.

Key words

Lichens - Lecanorales - Lecanoraceae - Bacidiaceae - ribosomal DNA - molecular phylogeny - ascus

Full Text

References

01 Ekman, S.. (1996); The corticolous and lignicolous species of Bacidia and Bacidina in North America. Op. Bot.. 127 1-148
02 Ekman, S.. (1997); The genus Cliostomum revisited. Symb. Bot. Ups.. 32 (1) 17-28
03 Ekman, S.. (1999); PCR optimization and troubleshooting, with special reference to the amplification of ribosomal DNA in lichenized fungi. Lichenologist. 31 517-531
04 Elix, J. A., and Crook, C. E.. (1992); The joint occurrence of chloroxanthones in lichens, and further thirteen new lichen xanthones. Bryologist. 95 52-64
05 Eriksson, O. E., and Hawksworth, D. L.. (1987 a); Notes on ascomycete systematics - Nos 464 - 551. Syst. Ascomycetum. 6 237-258
06 Eriksson, O. E., and Hawksworth, D. L.. (1987 b); Outline of the ascomycetes - 1987. Syst. Ascomycetum. 6 259-337
07 Eriksson, O. E., and Hawksworth, D. L.. (1992); Notes on ascomycete systematics - Nos 1294 - 1417. Syst. Ascomycetum. 11 49-82
08 Eriksson, O. E., and Hawksworth, D. L.. (1993); Outline of the ascomycetes - 1993. Syst. Ascomycetum. 12 51-257
09 Eriksson, O. E., and Hawksworth, D. L.. (1998); Outline of the ascomycetes - 1998. Syst. Ascomycetum. 16 83-296
10 Farris, J. S.,, Albert, V. A.,, Källersjö, M.,, Lipscomb, D.,, and Kluge, A. G.. (1996); Parsimony jackknifing outperforms neighbour-joining. Cladistics. 12 99-124
11 Gargas, A., and DePriest, P. T.. (1996); A nomenclature for fungal PCR primers with examples from intron-containing SSU rDNA. Mycologia. 88 745-748
12 Gargas, A.,, DePriest, P. T.,, and Taylor, J. W.. (1995); Positions of multiple insertions in SSU rDNA of lichen-forming fungi. Mol. Biol. Evol.. 12 208-218
13 Grube, M.,, DePriest, P. T.,, Gargas, A.,, and Hafellner, J.. (1995); DNA isolation from lichen ascomata. Mycol. Res.. 99 1321-1324
14 Gu, X.,, Fu, Y.-X,, and Li, W.-H.. (1995); Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol. Biol. Evol.. 12 546-557
15 Hafellner, J.. (1984); Studien in Richtung einer natürlicheren Gliederung der Sammelfamilien Lecanoraceae und Lecideaceae. Beih. Nova Hedwigia. 79 241-371
16 Hafellner, J.. (1988) Principles of classification and main taxonomic groups. Handbook of Lichenology, Vol. 3. Galun, M., ed. Boca Raton; CRC Press pp. 41-52
17 Hawksworth, D. L., and Dalby, D. H.. (1992) Lecanora Ach. (1810). The Lichen Flora of Great Britain and Ireland. Purvis, O. W., Coppins, B. J., Hawksworth, D. L., James, P. W., and Moore, D. M., eds. London; Natural History Museum Publications pp. 292-318
18 Henssen, A.,, Keuck, G.,, Renner, B.,, and Vobis, G.. (1981) The lecanoralean centrum. Ascomycete Systematics, the Luttrellian Concept. Reynolds, D. R., ed. New York, Heidelberg, Berlin; Springer Verlag pp. 138-234
19 Hertel, H., and Rambold, G.. (1985); Lecidea sect. Armeniacae: lecideoide Arten der Flechtengattung Lecanora und Tephromela (Lecanorales). Bot. Jahrb.. 107 469-501
20 Hertel, H., and Rambold, G.. (1995); On the genus Adelolecia (lichenized Ascomycotina, Lecanorales). Bibl. Lichenol.. 57 211-230
21 Hillis, D. M.,, Mable, B. K.,, Larson, A.,, Davis, S. K.,, and Zimmer, E. A.. (1996) Nucleic acids IV: sequencing and cloning. Molecular Systematics, 2nd ed. Hillis, D. M., Moritz, C., and Mable, B. K., eds. Sunderland; Sinauer Associates pp. 321-381
22 Huelsenbeck, J. P., and Crandall, K. A.. (1997); Phylogeny estimation and hypothesis testing using maximum likelihood. Ann. Rev. Ecol. Syst.. 28 437-466
23 Huelsenbeck, J. P., and Rannala, B.. (1997); Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science. 276 227-232
24 Jahns, H. M.. (1970); Untersuchungen zur Entwicklungsgeschichte der Cladoniaceen unter besonderer Berücksichtigung des Podetien-Problems. Nova Hedwigia. 20 1-177
25 Kishino, H., and Hasegawa, M.. (1989); Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol.. 29 170-179
26 Knoph, J. G.. (1990); Untersuchungen an gesteinsbewohnenden xanthonhaltigen Slippen der Flechtengattung Lecidella (Lecanoraceae, Lecanorales) unter besonderer Berücksichtigung von aussereuropäischen Proben exklusive Amerika. Bibl. Lichenol.. 36 1-183
27 Knoph, J. G., and Leuckert, C.. (1994); Chemotaxonomic studies in the saxicolous species of the lichen genus Lecidella (Lecanorales, Lecanoraceae) in America. Nova Hedwigia. 59 455-508
28 Letrouit-Galinou, M. A.. (1966); Recherches sur l'ontogenie et l'anatomie comparées des apothécies de quelques discolichens. Rev. Bryol. Lichenol.. 34 413-588
29 Leuckert, C.,, Knoph, J. G.,, and Hertel, H.. (1992); Chemotaxonomic studies within the genus Lecidella (Lecanorales, Lecanoraceae): II. European species of the Lecidella asema group. Herzogia. 9 1-17
30 Leuckert, C.,, Knoph, J. G.,, Ziegler, H. G.,, and Hertel, H.. (1990); Chemotaxonomic studies in the genus Lecidella (Lecanorales, Lecanoraceae): I. Lecidella carpathica and Lecidella viridans: studies of central and southern European samples. Herzogia. 8 265-272
31 Lumbsch, H. T.. (1991); Die Fruchtkörperperontogenie bei Bacidia bagliettoana (Massal. und de Not.) Jatta mit Bemerkungen zur Gattung Bacidia de Not. Nova Hedwigia. 52 419-426
32 Lumbsch, H. T.. (1997); Systematic studies in the suborder Agyriineae (Lecanorales). J. Hattori Bot. Lab.. 83 1-73
33 Lumbsch, H. T.,, Feige, G. B.,, and Elix, J. A.. (1994 a); Chemical variation in two species of the Lecanora subfusca group (Lecanoraceae, lichenized Ascomycotina). Pl. Syst. Evol.. 191 227-236
34 Lumbsch, H. T.,, Feige, G. B.,, and Elix, J. A.. (1994 b); The joint occurrence of chloroxanthones in southern hemisphere Lecanora species (Ascomycotina; Lecanoraceae). Bot. Acta. 107 30-35
35 Lutzoni, F. M.. (1997); Phylogeny of lichen- and non-lichen-forming omphalinoid mushrooms and the utility of testing combinability among multiple data sets. Syst. Biol.. 46 373-406
36 Maddison, W. P., and Maddison, D. R.. (1992) MacClade: Analysis of phylogeny and character evolution, Version 3. Sunderland; Sinauer Associates
37 Maidak, B. L.,, Cole, J. R.,, Parker, C. T.,, Garrity, G. M.,, Larsen, N.,, Li, B.,, Lilburn, T. G.,, McCaughey, M. J.,, Olsen, G. J.,, Overbeek, R.,, Pramanik, S.,, Schmidt, T. M.,, Tiedje, J. M.,, and Woese, C. R.. (1999); A new version of the RDP (Ribosomal Database Project). Nucleic Acids Res.. 27 171-173
38 Myllys, L.,, Källersjö, M.,, and Tehler, A.. (1999); Variable sizes of introns in the SSU rDNA in three species of Roccella (Arthoniales, Euascomycetes). Curr. Genetics. 36 79-85
39 Newton, C. R., and Graham, A.. (1997) PCR, 2nd ed. Oxford; BIOS Scientific Publishers
40 Poelt, J., and Grube, M.. (1993); Beiträge zur Kenntnis der Flechtenflora des Himalaya VI - die Gattung Tephromela (mit Bemerkungen zum Genus Heppsora). Nova Hedwigia. 57 1-17
41 Posada, D., and Crandall, K. A.. (1998); MODELTEST: testing the model of DNA substitution. Bioinformatics. 9 817-818
42 Printzen, C.. (1995); Die Flechtengattung Biatora in Europa. Bibl. Lichenol.. 60 1-275
43 Rambold, G.. (1989); A monograph of the saxicolous lecideoid lichens of Australia (excl. Tasmania). Bibl. Lichenol.. 34 1-345
44 Rambold, G.. (1993); Further species of the genus Tephromela (Lecanorales). Sendtnera. 1 281-288
45 Rambold, G., and Hagedorn, G.. (1998); The distribution of selected diagnostic characters in the Lecanorales. Lichenologist. 30 473-487
46 Rambold, G.,, Mayrhofer, H., and Matzer, M.. (1994); Correlations of ascus and spore characters in the Physciaceae (Lecanorales). Pl. Syst. Evol.. 192 31-40
47 Rambold, G., and Triebel, D.. (1992); The inter-lecanoralean associations. Bibl. Lichenol.. 48 1-201
48 Rodríguez, F.,, Oliver, J. F.,, Marin, A.,, and Medina, J. R.. (1990); The general stochastic model of nucleotide substitution. J. Theor. Biol.. 142 485-501
49 Sokal, R. R., and Rohlf, F. J.. (1995) Biometry. The principles and practice of statistics in biological research, 3rd ed. New York; W. H. Freeman & Co.
50 Stenroos, S. K., and DePriest, P. T.. (1998); SSU rDNA phylogeny of cladoniiform lichens. Am. J. Bot.. 85 1548-1559
51 Stoye, J.. (1998); Multiple sequence alignment with the divide-and-conquer method. Gene. 211 45-56
52 Swofford, D. L.. (1999) PAUP*, Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sunderland; Sinauer Associates
53 Swofford, D. L.,, Olsen, G. J.,, Waddell, P. J.,, and Hillis, D. M.. (1996) Phylogenetic inference. Molecular Systematics, 2nd ed. Hillis, D. M., Moritz, C., and Mable, B. K., eds. Sunderland; Sinauer Associates pp. 407-514
54 Tamura, K., and Nei, M.. (1993); Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol.. 10 512-526
55 Tibell, L.. (1998); Practice and prejudice in lichen classification. Lichenologist. 30 439-453
56 Timdal, E.. (1991); A monograph of the genus Toninia (Lecideaceae, Ascomycetes). Op. Bot.. 110 1-137
57 Vezda, A.. (1978); Neue oder wenig bekannte Flechten in der Tschechoslowakei. II. Folia Geobot. Phytotax. Praha. 13 397-420
58 Vobis, G.. (1980); Bau und Entwicklung der Flechten-Pycnidien und ihrer Conidien. Bibl. Lichenol.. 14 1-141
59 Wedin, M.,, Tehler, A.,, and Gargas, A.. (1998); Phylogenetic relationships of Sphaerophoraceae (Ascomycetes) inferred from SSU rDNA sequences. Pl. Syst. Evol.. 209 75-83
60 Wedin, M., and Tibell, L.. (1997); Phylogeny and evolution of Caliciaceae, Mycocaliciaceae, and Sphinctrinaceae (Ascomycota), with notes on the evolution of the prototunicate ascus. Can. J. Bot.. 75 1236-1242
61 Wheeler, W. C., and Gladstein, D. S.. (1994); MALIGN: a multiple sequence alignment program. J. Heredity. 85 417-418
62 Yang, Z.. (1994); Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol.. 39 306-314
63 Zahlbruckner, A.. (1905) Ascolichenes. Lieferung 3. Die natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen, 1 (1*). Engler, A. and Prantl, K., eds. Leipzig; Engelmann pp. 97-144
64 Zahlbruckner, A.. (1921 - 1940) Catalogous lichenum universalis. Band I - X. Leipzig, Berlin; Gebrüder Borntraeger
65 Zharkikh, A.. (1994); Estimation of evolutionary distances between nucleotide sequences. J. Mol. Evol.. 39 315-329

S. Ekman

Department of Botany University of Bergen

Allégaten 41 5007 Bergen Norway

Email: stefan.ekman@bot.uib.no

Section Editor: H. M. Jahns