Origin and Evolution of the Lichenized Ascomycete Order Lichinales: Monophyly and Systematic Relationships Inferred from Ascus, Fruiting Body and SSU rDNA Evolution

Abstract

The Lichinales are a group of lichenized ascomycetes that almost exclusively possess cyanobacteria as their primary photobiont and are hitherto separated from the Lecanorales, the major group of lichenized ascomycetes, by thallus structure, ascoma ontogeny, ascus structure and ascus function. The relationship of the two families Peltulaceae and Lichinaceae, both placed within the Lichinales, with the Heppiaceae, placed within the Lecanorales, was investigated, as well as a possible sister group relationship of the Lichinales to the Lecanorales. Phylogenetic analyses included non-molecular data as well as 18S rDNA sequence data. The monophyly of the Lichinales including the family Heppiaceae and a sister group relationship of Lichinales and Lecanorales, based on the shared presence of lecanoralean asci, are proposed in a morphological hypothesis. Parsimony and distance analyses of 18S rDNA sequence data strongly support the monophyly of the Lichinales, including all three families. Therefore, the presence of rostrate, lecanoralean asci in Peltula and part of the Lichinaceae suggests that this ascus type is an autapomorphy of the monophyletic Lichinales. Furthermore, the occurrence of prototunicate asci in the Heppiaceae and most of the Lichinaceae is autapomorphic and was gained independently by reduction of the rostrate ascus. The 18S rDNA analysis did not reject the non-molecular hypothesis of a sister group relationship of the Lichinales and the Lecanorales as based on ascus characters. The alternative placement of the Lichinales as the sister group of all inoperculate euascomycetes excluding the Sordariomycetes and most of the Leotiales in the gene tree received unsufficient bootstrap support and no support from any non-molecular data and consequently was rejected.

Key words

Lichenized ascomycetes - Lichinales - Lecanorales - phylogeny - ascus and ascoma evolution - SSU rDNA

References

• 01 Berbee,  M. L.. (1996);  Loculoascomycete origin and evolution of filamentous ascomycete morphology based on 18S rDNA gene sequence data.  Mol. Biol. Evol.. 13 462-470
• 02 Berbee,  M. L., and Taylor,  J. W.. (1992);  Two ascomycete classes based on fruiting-body characters and ribosomal DNA sequence.  Mol. Biol. Evol.. 9 278-284
• 03 Eriksson,  O. E. (ed.). (2000) Outline of ascomycota - 2000. www.umu.se/myconet/Myconet.html
• 04 Eriksson,  O. E., and Hawksworth,  D. L.. (1998);  Outline of the ascomycetes - 1998.  Syst. Ascomycet.. 16 83-296
• 05 Farris,  J. S.. (1995) Parsimony Jackknifer. Version 4.22. Stockholm; Molekylärsystematiska laboratoriet, Naturhistoriska riksmuseet
• 06 Gargas,  A., and Taylor,  J. W.. (1995);  Phylogeny of Discomycetes and early radiations of the apothecial Ascomycotina inferred from SSU rDNA sequence data.  Experimental Mycology. 19 7-15
• 07 Hamby,  R. K.,, Sims,  L. E.,, Issel,  L. E.,, and Zimmer,  E. A.. (1988);  Direct RNA sequencing: optimization of extraction and sequencing techniques for work with higher plants.  Pl. Mol. Biol. Rep.. 6 179-197
• 08 Henssen,  A.. (1980 [1979]);  Problematik der Gattungsbegrenzung bei den Lichinaceen.  Ber. Deutsch. Ges. Bot.. 92 483-506
• 09 Henssen,  A.. (1994);  Contribution to the morphology and species delimitation in Heppia sensu stricto (lichenized Ascomycotina).  Acta Bot. Fennica. 150 57-73
• 10 Henssen,  A.. (1995);  The new lichen family Gloeoheppiaceae and its genera Gloeoheppia, Pseudopeltula and Gudelia (Lichinales).  Lichenologist. 27 261-290
• 11 Henssen,  A., and Büdel,  B.. (1986) No. 115. Lichinales Henssen and Büdel ordo nov. P. 138. Notes on ascomycete systematics, nos. 1 - 224. Eriksson, O. E. and Hawksworth, D. L., eds. Syst. Ascomycet 5 pp. 113-184
• 12 Henssen,  A.,, Büdel,  B.,, and Titze,  A.. (1987);  Euopsis and Harpidium, genera of the Lichinaceae (Lichenes) with rostrate asci.  Botanica Acta. 100 49-55
• 13 Gunderson,  J. H.,, Elwood,  H.,, Ingold,  A.,, Kindle,  K.,, and Sogin,  M. L.. (1987);  Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes.  Proc. Natl. Acad. Sci. USA. 84 5823-5827
• 14 Landvik,  S.. (1996);  Neolecta, a fruit-body-producing genus of the basal ascomycetes, as shown by SSU and LSU rDNA sequences.  Mycol. Res.. 100 199-202
• 15 Landvik,  S.,, Eriksson,  O. E.,, Gargas,  A.,, and Gustafsson,  P.. (1993);  Relationships of the genus Neolecta (Neolectales ordo nov., Ascomycotina) inferred from 18S rDNA sequences.  Syst. Ascomycet.. 11 107-118
• 16 Landvik,  S.,, Shailer,  N. F. J.,, and Eriksson,  O. E.. (1996);  SSU rDNA sequence support for a close relationship between the Elaphomycetales and the Eurotiales and Onygenales.  Mycoscience. 37 237-241
• 17 Liu,  Y. J.,, Whelen,  S.,, and Hall,  B. D.. (1999);  Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit.  Mol. Biol. Evol.. 16 1799-1808
• 18 Olson,  G. J.. (1990) Sequence Editor and Analysis Program. 
• 19 Rambold,  G., and Hagedorn,  G.. (1998);  The distribution of selected diagnostic characters in the Lecanorales.  Lichenologist. 30 473-487
• 20 Spatafora,  J. W., and Blackwell,  M.. (1993);  Molecular systematics of unitunicate perithecial ascomycetes: the Clavicipitales-Hycocreales connection.  Mycologia. 85 912-922
• 21 Swofford,  D. L.. (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b4a test version. Sunderland, Massachusetts; Sinauer
• 22 Taylor,  T. N.,, Hass,  H.,, and Kerp,  H.. (1999);  The oldest fossile ascomycetes.  Nature. 399 648
• 23 Tehler,  A.. (1995);  Morphological data, molecular data, and total evidence in phylogenetic analysis.  Can. J. Bot.. 73 (Suppl. 1) S 667-S 676
• 24 Tehler,  A.. (1996) Systematics, phylogeny and classification. Lichen biology. Nash III, T. H., ed. Cambridge, New York, Melbourne; Cambridge University Press pp. 217-239
• 25 Tehler,  A.,, Farris,  J. S.,, Lipscomb,  D. L.,, and Källersjö,  M.. (2000);  Phylogenetic analyses of the fungi based on large rDNA data sets.  Mycologia. 92 459-474
• 26 Tibell,  L., and Wedin,  M.. (2000);  Mycocaliciales, a new order for nonlichenized calicioid fungi.  Mycologia. 92 577-581
• 27 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
• 28 Winka,  K.. (2000) Phylogenetic relationships within the Ascomycota based on 18S rDNA sequences. Umeå; Doctoral Dissertation pp. 25
• 29 Winka,  K.,, Ahlberg,  C.,, and Eriksson,  O. E.. (1998);  Are there lichenized Ostropales?.  Lichenologist. 30 455-462
• 30 Winka,  K.,, Eriksson,  E. O.,, and Bång,  A.. (1998);  Molecular evidence for recognizing the Chaetothyriales.  Mycologia. 90 822-830

Section Editor: M. Jahns