Register      Login
Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

The genus Karoowia (Parmeliaceae, Ascomycota) includes unrelated clades nested within Xanthoparmelia

Guillermo Amo de Paz A , H. Thorsten Lumbsch B , Paloma Cubas A , John A. Elix C and Ana Crespo A D
+ Author Affiliations
- Author Affiliations

A Universidad Complutense de Madrid, Departamento de Biología Vegetal II, Plaza de Ramón y Cajal s/n, 28040 Madrid, Spain.

B Department of Botany, The Field Museum, 1400 S. Lake Shore Drive Chicago, IL 60605, USA.

C Research School of Chemistry, Building 33, Australian National University, Canberra, ACT 0200, Australia.

D Corresponding author. Email: acrespo@farm.ucm.es

Australian Systematic Botany 23(3) 173-184 https://doi.org/10.1071/SB09055
Submitted: 15 December 2009  Accepted: 6 May 2010   Published: 14 July 2010

Abstract

Thallus morphology has traditionally played a major role in the classification of lichenised fungi. We have used a combined dataset of nuITS, nuLSU and mtSSU rDNA sequences to evaluate the phylogenetic relationships between the subcrustose genus Karoowia and the mostly foliose genus Xanthoparmelia. Our phylogenetic analyses using maximum parsimony, maximum likelihood and a Bayesian approach show that Karoowia species do not form a monophyletic group but cluster in different clades nested within Xanthoparmelia. The monophyly of Karoowia either as a separate clade from Xanthoparmelia, or nested within Xanthoparmelia is significantly rejected using alternative hypothesis testing. These results suggest that the usefulness of the phenotypic features used to define Karoowia has been overestimated because the subcrustose growth form has evolved independently in several clades within Xanthoparmelia. Other characters used to circumscribe Karoowia, such as the presence of cylindrical conidia, also occur in Xanthoparmelia, and the differences in rhizine morphology are minimal. Consequently, we propose to reduce Karoowia to synonymy with Xanthoparmelia. The enlarged genus is characterised by the presence of Xanthoparmelia-type lichenan in the hyphal cell walls and the presence of an arachiform vacuolar body in the ascospores. Fifteen new combinations in Xanthoparmelia and the new name Xanthoparmelia mucinae for Karoowia squamatica are made.


Acknowledgements

This study was financially supported by CGL2004–01848/BOS and CGL2007–64652/BOS projects from the Spanish Ministerio de Ciencia e Innovación. The new sequences were generated at Unidad de Genómica (Parque Científico de Madrid, UCM). The authors wish to thank to Christine Cargill (Canberra) for her helpful assistance and David Hawksworth (Madrid) for facilitating access to samples from the Natural History Museum, London.


References


Amo de Paz G, Lumbsch HT, Cubas P, Elix JA, Crespo A (2010) The morphologically deviating genera Omphalodiella and Placoparmelia belong to Xanthoparmelia (Parmeliaceae). The Bryologist In press. 113(2), open url image1

Armaleo D, Clerc P (1991) Lichen chimeras: DNA analysis suggests that one fungus forms two morphotypes. Experimental Mycology 15, 1–10.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Arup U, Grube M (1998) Molecular systematics of Lecanora subgenus Placodium. Lichenologist 30, 415–425.
Crossref | GoogleScholarGoogle Scholar | open url image1

Arup U, Grube M (2000) Is Rhizoplaca (Lecanorales, Lichenized Ascomycota) a monophyletic genus? Canadian Journal of Botany 78, 318–327.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blanco O, Crespo A, Divakar PK, Esslinger TL, Hawksworth DL, Lumbsch HT (2004a) Melanelixia and Melanohalea, two new genera segregated from Melanelia (Parmeliaceae) based on molecular and morphological data. Mycological Research 108, 873–884.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Blanco O, Crespo A, Elix JA, Hawksworth DL, Lumbsch HT (2004b) A molecular phylogeny and a new classification of Parmelioid lichens containing Xanthoparmelia-type lichenan (Ascomycota: Lecanorales). Taxon 53, 959–975.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blanco O, Crespo A, Divakar PK, Elix JA, Lumbsch HT (2005) Molecular phylogeny of Parmotremoid Lichens (Ascomycota, Parmeliaceae). Mycologia 97, 150–159.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Blanco O, Crespo A, Ree RH, Lumbsch HT (2006) Major clades of parmelioid lichens (Parmeliaceae, Ascomycota) and the evolution of their morphological and chemical diversity. Molecular Phylogenetics and Evolution 39, 52–69.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clauzade G , Roux C (1986, “1985”) ‘Likenoj de okcidenta Europo. Ilustrita determinlibro.’ (Bulletin de la Société Botanique du Centre-Ouest, Nouvelle Serie, Numero Special 7. Royan, France). 893 pp.

Common RS (1991) The distribution and taxonomic significance of lichenan and isolichenan in the Parmeliaceae (Lichenized Ascomycotina), as determined by iodine reactions. 1. Introduction and Methods, 2. The Genus Alectoria and associated taxa. Mycotaxon 41, 67–112. open url image1

Common R, Brodo IM (1995) Bryoria sect. subdivergentes recognized as the new genus Nodobryoria (Lichenized Ascomycotina). The Bryologist 98, 189–206.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crespo A, Cubero OF (1998) A molecular approach to the circumscription and evaluation of some genera segregated from Parmelia s. lat. Lichenologist 30, 369–380. open url image1

Crespo A, Blanco O, Hawksworth DL (2001) The potential of mitochondrial DNA for establishing phylogeny and stabilising generic concepts in the parmelioid lichens. Taxon 50, 807–819.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crespo A, Lumbsch HT, Mattsson JE, Blanco O, Divakar PK, Articus K, Wiklund E, Bawingan PA, Wedin M (2007) Testing morphology-based hypotheses of phylogenetic relationships in Parmeliaceae (Ascomycota) using three ribosomal markers and the nuclear rpb1 gene. Molecular Phylogenetics and Evolution 44, 812–824.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Crespo A, Ferencova Z, Pérez-Ortega S, Argüello A, Elix JA, Divakar PK (2010) Austroparmelina, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota): a multigene and morphological approach. Systematics and Biodiversity 8, 209–221. open url image1

Culberson CF (1972) Improved conditions and new data for the identification of lichen products by a standardized thin-layer chromatographic method. Journal of Chromatography. A 72, 113–125.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Culberson CF, Johnson A (1982) Substitution of methyl tert.-butyl ether for diethyl ether in standardized thin-layer chromatographic method for lichen products. Journal of Chromatography. A 238, 483–487.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Culberson CF, Culberson WL, Johnson A (1981) A standardized TLC analysis of β-orcinol depsidones. The Bryologist 84, 16–29.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Del Prado R, Ferencova Z, Armas-Crespo V, Amo de Paz G, Cubas P, Crespo A (2007) The arachiform vacuolar body: an overlooked shared character in the ascospores of a large monophyletic group within Parmeliaceae (Xanthoparmelia Clade, Lecanorales). Mycological Research 111, 685–692.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Divakar PK, Crespo A, Blanco O, Lumbsch HT (2006) Phylogenetic significance of morphological characters in the tropical Hypotrachyna clade of parmelioid lichens (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution 40, 448–458.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Divakar PK, Lumbsch HT, Ferencova Z, Del Prado R, Crespo A (2010) Remototrachyna, a newly recognized tropical lineage of lichens in the hypotrachynoid clade (Parmeliaceae, Ascomycota), originated in the Indian subcontinent. American Journal of Botany 97, 579–590.
Crossref | GoogleScholarGoogle Scholar | open url image1

Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Elix JA (1993) Progress in the generic delimitation of Parmelia sensu lato lichens (Ascomycotina: Parmeliaceae) and a synoptic key to the Parmeliaceae. The Bryologist 96, 359–383.
Crossref | GoogleScholarGoogle Scholar | open url image1

Elix JA (1994) Xanthoparmelia. In ‘Flora of Australia. Volume 55 Lichens-Lecanorales 2, Parmeliaceae’ (Ed. C Grgurinovic) pp. 201–308. (Australian Biological Resouces Study: Canberra)

Elix JA (1997) New species and new combinations in the lichen family Parmeliaceae (Ascomycotina) from South Africa. Mycotaxon 63, 335–343. open url image1

Elix JA (1999) Further new species and new reports in the lichen family Parmeliaceae (Ascomycotina) from South Africa. Mycotaxon 70, 103–110. open url image1

Elix JA (2000) A new species of Karoowia from Australia. Australasian Lichenology 46, 18–20. open url image1

Elix JA (2001) A Revision of the lichen genus Paraparmelia Elix & J. Johnst. Bibliotheca Lichenologica 80, 1–224. open url image1

Elix JA (2003) The lichen genus Paraparmelia, a synonym of Xanthoparmelia (Ascomycota, Parmeliaceae). Mycotaxon 87, 395–403. open url image1

Eriksson O, Hawksworth DL (1986) Notes on Ascomycete systematics. nos. 1–224. Systema Ascomycetum 5, 113–174. open url image1

Esslinger TL (1977) A chemosystematic revision of the brown Parmeliae. The Journal of the Hattori Botanical Laboratory 42, 1–211.
CAS |
open url image1

Feige GB, Lumbsch HT, Huneck S, Elix JA (1993) Identification of lichen substances by a standardized high-performance liquid-chromatographic method. Journal of Chromatography. A 646, 417–427.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Felsenstein J (1985) Confidence-limits on phylogenies – an approach using the bootstrap. Evolution 39, 783–791.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes – Application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113–118.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gaya E, Lutzoni F, Zoller S, Navarro-Rosines P (2003) Phylogenetic study of Fulgensia and allied Caloplaca and Xanthoria species (Teloschistaceae, lichen-forming Ascomycota). American Journal of Botany 90, 1095–1103.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Grube M, Arup U (2001) Molecular and morphological evolution in the Physciaceae (Lecanorales, Lichenized Ascomycotina), with special emphasis on the genus Rinodina. Lichenologist 33, 63–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grube M, Hawksworth DL (2007) Trouble with lichen: the re-evaluation and re-interpretation of thallus form and fruit body types in the Molecular Era. Mycological Research 111, 1116–1132.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hale ME (1984) An historical review of the genus concept in lichenology. Beiheft zur Nova Hedwigia 79, 11–23. open url image1

Hale ME (1989) A monograph of the lichen genus Karoowia Hale (Ascomycotina: Parmeliaceae). Mycotaxon 35, 177–198. open url image1

Hale ME (1990) A synopsis of the lichen genus Xanthoparmelia (Vainio) Hale (Ascomycotina, Parmeliaceae). Smithsonian Contributions to Botany 74, 1–250. open url image1

Hale BW, DePriest PT (1999) Mason E. Hale’s list of epithets in the parmelioid genera. The Bryologist 102, 462–544.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hawksworth DL, Crespo A (2002) Proposal to conserve the name Xanthoparmelia against Chondropsis Nom. Cons. (Parmeliaceae). Taxon 51, 807.
Crossref | GoogleScholarGoogle Scholar | open url image1

Högnabba F (2006) Molecular phylogeny of the genus Stereocaulon (Stereocaulaceae, Lichenized Ascomycetes). Mycological Research 110, 1080–1092.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

James PW , Henssen A (1976) The morphological and taxonomic significance of cephalodia. In ‘Lichenology: Progress and Problems’. (Eds DH Brown, DL Hawksworth and RH Bailey) pp. 27–77. (Academic Press: London)

Llimona X, Hladun NL (2001) Checklist of the lichens and lichenicolous fungi of the Iberian Peninsula and Balearic Islands. Bocconea 14, 1–581. open url image1

Lohtander K, Myllys L, Sundin R, Källersjö M, Tehler A (1998) The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): analyses based on ITS sequences. The Bryologist 101, 404–411.
CAS |
open url image1

Lumbsch HT, Hipp AL, Divakar PK, Blanco O, Crespo A (2008) Accelerated evolutionary rates in tropical and oceanic parmelioid lichens (Ascomycota). BMC Evolutionary Biology 8, 257.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung G-H, Lücking R, Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim Y-W, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany 91, 1446–1480.
Crossref | GoogleScholarGoogle Scholar | open url image1

Myllys L, Lohtander K, Källersjö M, Tehler A (1999) Sequence insertions and ITS data provide congruent information on Roccella canariensis and R. tuberculata (Arthoniales, Euascomycetes) phylogeny. Molecular Phylogenetics and Evolution 12, 295–309.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nash TH III , Elix JA (2004) Xanthoparmelia. In ‘Lichen Flora of the Greater Sonoran Desert Region, Vol. 2’. (Eds TH III Nash, BD Ryan, P Diederich, C Gries, F Bungartz) pp. 566–604. (Lichens Unlimited, Arizona State University: Arizona)

Nash TH, Hafellner J, Common RS (1990) Omphalora, a new genus in the Parmeliaceae. Lichenologist 22, 355–365.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nash TH, Gries C, Elix JA (1995) A revision of the lichen genus Xanthoparmelia in South America. Bibliotheca Lichenologica 56, 1–158. open url image1

Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2007) AWTY (Are We There Yet?): a system for graphical exploration of mcmc convergence in bayesian phylogenetics. Bioinformatics 24, 581–583.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.
CAS | PubMed |
open url image1

Parnmen S, Rangsiruji A, Mongkolsuk P, Boonpragob K, Elix JA, Lumbsch HT (2010) Morphological plasticity in Cladoniaceae: the foliose genus Heterodea evolved from fruticose Cladia species (Lecanorales, Ascomycota). Taxon 59, 841–849. open url image1

Poelt J, Vězda A (1981) Bestimmungsschlüssel europäischer Flechten. Ergänzungsheft II. Bibliotheca Lichenologica 16, 1–390. open url image1

Samson RA, Stalpers JA, Verkerke W (1979) A simplified technique to prepare fungal specimens for scanning electron microscopy. Cytobios 24, 7–11.
CAS | PubMed |
open url image1

Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) Tree-Puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shimodaira H, Hasegawa M (2001) Consel: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246–1247.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Søchting U, Lutzoni F (2003) Molecular phylogenetic study at the generic boundary between the lichen-forming fungi Caloplaca and Xanthoria (Ascomycota, Teloschistaceae). Mycological Research 107, 1266–1276.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Strimmer K, Rambaut A (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the Royal Society of London. Series B. Biological Sciences 269, 137–142.
Crossref | GoogleScholarGoogle Scholar | open url image1

Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and other methods) 4.0 Beta. (Sinauer Associates: Sunderland, MA)

Tehler A, Irestedt M (2007) Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales, Ascomycota). Cladistics 23, 432–454.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thell A, Feuerer T, Kärnefelt I, Myllys L, Stenroos S (2004) Monophyletic groups within the parmeliaceae identified by ITS rDNA, β-tubulin and GAPDH sequences. Mycological Progress 3, 297–314.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thell A, Feuerer T, Elix JA, Kärnefelt I (2006) A contribution to the phylogeny and taxonomy of Xanthoparmelia (Ascomycota, Parmeliaceae). The Journal of the Hattori Botanical Laboratory 100, 797–807. open url image1

Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172, 4238–4246.
CAS | PubMed |
open url image1

White TJ , Bruns TD , Lee SB , Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR Protocols’. (Eds MA Innis, DH Gelfand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press: San Diego, CA)

Zoller S, Scheidegger C, Sperisen C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31, 511–516. open url image1

Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas, Austin.