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

Molecular phylogeny reveals the true colours of Myeloconidaceae (Ascomycota: Ostropales)

Matthew P. Nelsen A B F , Robert Lücking B , Carrie J. Andrew B , André Aptroot C , Marcela E. S. Cáceres D , Joel A. Mercado-Díaz E , Eimy Rivas Plata B and H. Thorsten Lumbsch B

A Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th Street, Chicago, IL 60637, USA.

B Science & Education, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605, USA.

C ABL Herbarium, Gerrit van der Veenstraat 107, NL-3762 XK Soest, the Netherlands.

D Departamento de Biociências, Universidade Federal de Sergipe, CEP: 49.500-000, Itabaiana, Sergipe, Brazil.

E Herbario, Jardín Botánico, Universidad de Puerto Rico, 1187 Calle Flamboyán, San Juan, 00926-1177, Puerto Rico.

F Corresponding author. Email: mpnelsen@gmail.com

Australian Systematic Botany 27(1) 38-47 http://dx.doi.org/10.1071/SB13040
Submitted: 11 September 2013  Accepted: 14 February 2014   Published: 30 June 2014

Abstract

The lichen-forming fungal family Myeloconidaceae, with the single genus Myeloconis, has been suggested to share affinities with Porinaceae (Lecanoromycetes: Ostropales). We examined its position relative to this family by using molecular data from the mitochondrial small-subunit and nuclear large-subunit rDNA. Our results revealed that Myeloconis forms a monophyletic group nested within Porinaceae, closely related to Porina farinosa. Neither Porina s.str. nor Clathroporina sensu Harris form monophyletic groups; instead, two strongly supported clades were recovered, which differ in ascospore septation (septate v. muriform), with the clade producing muriform ascospores including Myeloconis. We therefore reduce Myeloconidaceae to synonymy with Porinaceae; however, because generic delimitations within Porinaceae remain unclear, we retain Myeloconis as a separate genus within the family. The species concept currently used in the genus, based largely on secondary metabolites and ascospore measurements, is supported by the phylogeny.


References

Altschul SF, Madden TL, Schäffer ZJ, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI–BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
Gapped BLAST and PSI–BLAST: a new generation of protein database search programs.CrossRef | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=76caa785641f1f84fc284efda12da3f4CAS | 9254694PubMed | open url image1

Aptroot A (2002) Porina. In ‘Lichen of the Greater Sonoran Desert region. Vol. 1’. (Eds TH Nash III, BD Ryan, C Gries, F Bungartz) pp. 402–405. (Lichens Unlimited: Tempe, AZ)

Aptroot A, Sipman HJM (1993) Trichotheliaceae (lichens). In ‘Flora of the Guianas Series E: Fungi and Lichens, Fascicle 2’. (Ed ARA Gorts-van Rijn) pp. 1–57. (Koeltz Scientific Books: Konigstein, Germany)

Baloch E, Grube M (2006) Evolution and phylogenetic relationships within Porinaceae (Ostropomycetidae), focusing on foliicolous species. Mycological Research 110, 125–136.
Evolution and phylogenetic relationships within Porinaceae (Ostropomycetidae), focusing on foliicolous species.CrossRef | 1:CAS:528:DC%2BD28XjsFOrtr0%3D&md5=7199e01485109a2f2bae8c60ceeb5334CAS | 16376532PubMed | open url image1

Baloch E, Lücking R, Lumbsch HT, Wedin M (2010) Major clades and phylogenetic relationships between lichenized and non-lichenized lineages in Ostropales (Ascomycota: Lecanoromycetes). Taxon 59, 1483–1494.

Bhattacharya D, Lutzoni F, Reeb V, Simon D, Nason J, Fernandez F (2000) Widespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes. Molecular Biology and Evolution 17, 1971–1984.
Widespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes.CrossRef | 1:CAS:528:DC%2BD3cXptVWrtro%3D&md5=aaee53871ab17f87ac98bec6458af76fCAS | 11110913PubMed | open url image1

Church SH, Ryan JF, Dunn C (2014) Sowhat. GitHub repository. Available at https://github.com/josephryan/sowh.pl [Verified 25 February 2014]

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.CrossRef | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=cb5c1add9aa11a9a28fb7566d4607ea8CAS | 15034147PubMed | open url image1

Ernst-Russell MA, Chai CLL, Elix JA, McCarthy PM (2000) Myeloconone A2, a new phenalenone from the lichen Myeloconis erumpens. Australian Journal of Chemistry 53, 1011–1013.
Myeloconone A2, a new phenalenone from the lichen Myeloconis erumpens.CrossRef | 1:CAS:528:DC%2BD3MXktlSitrs%3D&md5=9c5a042d44e6d6a56c930dc1c439fc26CAS | open url image1

Galloway DJ (2007) ‘Flora of New Zealand: Lichens’, revised 2nd edn. (Manaaki Whenua Press: Lincoln, New Zealand)

Gelman A, Rubin D (1992) Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–472.
Inference from iterative simulation using multiple sequences.CrossRef | open url image1

Goldman N, Anderson JP, Rodrigo AG (2000) Likelihood-based tests of topologies in phylogenetics. Systematic Biology 49, 652–670.
Likelihood-based tests of topologies in phylogenetics.CrossRef | 1:STN:280:DC%2BD38zntVOjtw%3D%3D&md5=d6e4c1d0de9cb692c3e90fd92438e9b4CAS | 12116432PubMed | open url image1

Grube M, Baloch E, Lumbsch HT (2004) The phylogeny of Porinaceae (Ostropomycetidae) suggests a neotenic origin of perithecia in Lecanoromycetes. Mycological Research 108, 1111–1118.
The phylogeny of Porinaceae (Ostropomycetidae) suggests a neotenic origin of perithecia in Lecanoromycetes.CrossRef | 1:CAS:528:DC%2BD2cXot1Clu7w%3D&md5=28612ce5fd0c9d9b66ba37781eadde20CAS | 15535063PubMed | open url image1

Hafellner J, Kalb K (1995) Studies in Trichotheliales ordo novus. Bibliotheca Lichenologica 57, 161–186.

Hafellner J, Türk R (2001) Die lichenisierten Pilze Österreichs – eine Checkliste der bisher nachgewiesenen Arten mit Verbretungsangaben. Stapfia 76, 1–167.

Harris RC (1995) ‘More Florida Lichens: Including the 10¢ Tour of the Pyrenolichens.’ (R. C. Harris: New York)

Harris RC (2005) Some name changes in Porina s.lat. Opuscula Philolichenum 2, 15–16.

Henssen A, Jahns HM (1974) ‘Lichenes.’ (Georg Thieme Verlag: Stuttgart, Germany)

Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Beny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level classification of the fungi. Mycological Research 111, 509–547.
A higher-level classification of the fungi.CrossRef | 17572334PubMed | open url image1

Huelsenbeck JP, Larget B, Alfaro ME (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molecular Biology and Evolution 21, 1123–1133.
Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo.CrossRef | 1:CAS:528:DC%2BD2cXksVymu70%3D&md5=93ee1aa7feda5f044947a8e9e4ae0493CAS | 15034130PubMed | open url image1

Janex-Favre MC (1971) Recherches sur l’ontogenie, l’organisation et les asques de quelques pyrenolichens. Revue Bryologique et Lichénologique 37, 421–469.

Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.CrossRef | 1:CAS:528:DC%2BD38XlslOqu7s%3D&md5=ba90dc9439a36328ead61c836187a47fCAS | 12136088PubMed | open url image1

Kauff F, Lutzoni F (2002) Phylogeny of the Gyalectales and Ostropales (Ascomycota: Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Molecular Phylogenetics and Evolution 25, 138–156.
Phylogeny of the Gyalectales and Ostropales (Ascomycota: Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits.CrossRef | 1:CAS:528:DC%2BD38XnsVeru7c%3D&md5=283ee10175964debe7b99fae9c84ebe9CAS | 12383757PubMed | open url image1

Kauff F, Lutzoni F (2003) Compat.py – a program to detect topological conflict between supported clades in phylogenetic trees. Available at http://www.lutzonilab.net/pages/download.shtml [Verified 25 February 2014].

Kroken S, Taylor JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93, 38–53.
A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia.CrossRef | 1:CAS:528:DC%2BD3MXktVSgtro%3D&md5=ba78a72fafca4a1f7c6fa46df71efe1aCAS | open url image1

Lakner C, van der Mark P, Huelsenbeck J, Larget B, Ronquist F (2008) Efficiency of Markov chain Monte Carlo tree proposals in Bayesian phylogenetics. Systematic Biology 57, 86–103.
Efficiency of Markov chain Monte Carlo tree proposals in Bayesian phylogenetics.CrossRef | 18278678PubMed | open url image1

Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16, 750–759.
Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees.CrossRef | 1:CAS:528:DyaK1MXjslGitb8%3D&md5=4d882594f0872de6d3e0f9daf914aad5CAS | open url image1

Lücking R (1998) Additions and corrections to the knowledge of the foliicolous lichen flora of Costa Rica. The genus Trichothelium (lichenized Ascomycetes: Trichotheliaceae). Nova Hedwigia 66, 375–417.

Lücking R (2004) A revised key to foliicolous Porinaceae (Ascomycota: Trichotheliales). In ‘Bibliotheca Lichenologica’, Vol. 88. pp. 409–42. (The New York Botanical Garden Press: Bronx, NY)

Lücking R (2008) Foliicolous lichenized fungi. Flora Neotropica Monograph 103, 1–867.

Lumbsch HT, Huhndorf SM (2010) Myconet Volume 14. Part one. Outline of Ascomycota – 2009. Fieldiana Life and Earth Sciences 1, 1–42.

Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis Version 2.73. Available at http://mesquiteproject.org [Verified 25 February 2014]

Malcolm WM, Vězda A (1995) New foliicolous lichens from New Zealand 1. Folia Geobotanica et Phytotaxonomica 30, 91–96.
New foliicolous lichens from New Zealand 1.CrossRef | open url image1

Mangold A, Martin MP, Lücking R, Lumbsch HT (2008) Molecular phylogeny suggests synonymy of Thelotremataceae within Graphidaceae (Ascomycota: Ostropales). Taxon 57, 476–486.

McCarthy PM (1993) Saxicolous species of Porina Müll Arg. (Trichotheliaceae) in the southern hemisphere. Bibliotheca Lichenologica 52, 1–134.

McCarthy PM (1995) A reappraisal of Clathroporina Müll. Arg. (Trichotheliaceae). Lichenologist 27, 321–350.

McCarthy PM (2001a) Myeloconaceae. In ‘Flora of Australia’, Vol. 58A. pp. 104–105. (CSIRO Publishing and Australian Biological Resources Study: Melbourne)

McCarthy PM (2001b) Appendix: Myeloconaceae. In ‘Flora of Australia’, Vol. 58A. pp. 227. (CSIRO Publishing and Australian Biological Resources Study: Melbourne)

McCarthy PM (2001c) Trichotheliaceae. In ‘Flora of Australia’, Vol. 58A. pp. 105–157. (CSIRO Publishing and Australian Biological Resources Study: Melbourne)

McCarthy PM (2003) Catalogue of the lichen family Porinaceae. Bibliotheca Lichenologica 87, 1–164.

McCarthy PM (2013) Catalogue of Porinaceae. Australian biological resources study, Canberra. Version 4 December 2013. Available http://www.anbg.gov.au/abrs/lichenlist/PORINACEAE.html [Verified 25 February 2014]

McCarthy PM, Elix JA (1996) Myeloconis, a new genus of pyrenocarpous lichens from the tropics. Lichenologist 28, 401–414.

McCarthy PM, Kantvilas G (2000) A new bryophilous Porina from Tasmania, and notes on the diversity, ecological groups and biogeographical affinities of the Tasmanian Trichotheliaceae. Lichenologist 32, 247–256.
A new bryophilous Porina from Tasmania, and notes on the diversity, ecological groups and biogeographical affinities of the Tasmanian Trichotheliaceae.CrossRef | open url image1

McCarthy PM, Malcolm WM (1997) The genera of Trichotheliaceae. Lichenologist 29, 1–8.

McCarthy PM, Kantvilas G, Elix JA (2001) Amphorothecium, a new pyrenocarpous lichen genus from New South Wales, Australia. Lichenologist 33, 291–296.
Amphorothecium, a new pyrenocarpous lichen genus from New South Wales, Australia.CrossRef | open url image1

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA. pp. 1–8. (Institute of Electrical and Electronics Engineers)

Nelsen MP, Rivas Plata E, Andrew CJ, Lücking R, Lumbsch HT (2011a) Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. Journal of Phycology 47, 282–290.
Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi.CrossRef | open url image1

Nelsen MP, Lücking R, Mbatchou JS, Andrew CJ, Spielmann AA, Lumbsch HT (2011b) New insights into relationships of lichen-forming Dothideomycetes. Fungal Diversity 51, 155–162.
New insights into relationships of lichen-forming Dothideomycetes.CrossRef | open url image1

Nelsen MP, Lücking R, Andrew CJ, Rivas Plata E, Chaves JL, Cáceres MES, Ventura N (2012) Dismantling Herpothallon: Herpothallon antillarum (Arthoniomycetes: Arthoniaceae) is a member of the genus Diorygma (Lecanoromycetes: Graphidaceae). The Bryologist 115, 313–321.
Dismantling Herpothallon: Herpothallon antillarum (Arthoniomycetes: Arthoniaceae) is a member of the genus Diorygma (Lecanoromycetes: Graphidaceae).CrossRef | open url image1

Nylander JA, Wilgenbusch WC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24, 581–583.
AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics.CrossRef | 1:CAS:528:DC%2BD1cXitVKis7g%3D&md5=bc5ce04ccc0e11394dccf9614316c76dCAS | 17766271PubMed | open url image1

Orange A, Purvis OW, James PW (2009) Porina. In ‘The lichens of Great Britain and Ireland’. (Eds CW Smith, A Aptroot, BJ Coppins, A Fletcher, OL Gilbert, PW James, PA Wolseley) pp. 729–737. (British Lichen Society: London)

Rambaut A, Grassly NC (1997) Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Bioinformatics 13, 235–238.
Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees.CrossRef | 1:CAS:528:DyaK2sXksVGntL4%3D&md5=51c6bf83949435b1399ae13634148f8bCAS | open url image1

Rivas Plata E, Lumbsch HT, Lücking R (2012) A new classification for the lichen family Graphidaceae s.lat. (Ascomycota: Lecanoromycetes: Ostropales). Fungal Diversity 52, 107–121.
A new classification for the lichen family Graphidaceae s.lat. (Ascomycota: Lecanoromycetes: Ostropales).CrossRef | open url image1

Rivas Plata E, Parnmen S, Staiger B, Mangold A, Frisch A, Weerakoon G, Hernández MJE, Cáceres ME, Kalb K, Sipman HJM, Common RS, Nelsen MP, Lücking R, Lumbsch HT (2013) A molecular phylogeny of Graphidaceae (Ascomycota, Lecanoromycetes, Ostropales) including 428 species. MycoKeys 6, 55–94.
A molecular phylogeny of Graphidaceae (Ascomycota, Lecanoromycetes, Ostropales) including 428 species.CrossRef | open url image1

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space.CrossRef | 22357727PubMed | open url image1

Santesson R (1952) Foliicolous lichens I. A revision of the taxonomy of the obligately foliicolous, lichenized fungi. Symbolae Botanicae Upsalienses 12, 1–590.

Santesson R, Moberg R, Nordin A, Tønsberg T, Vitikainen O (2004) ‘Lichen-forming and lichenicolous fungi of Fennoscandia.’ (Museum of Evolution, Uppsala University: Uppsala, Sweden)

Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.
Multiple comparisons of log-likelihoods with applications to phylogenetic inference.CrossRef | 1:CAS:528:DyaK1MXltVyksrg%3D&md5=badc5249ae6db1adb40ad89917174533CAS | open url image1

Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.CrossRef | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=99af42d78c661258cd286bb3f9d2e18dCAS | 16928733PubMed | open url image1

Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.CrossRef | 18853362PubMed | open url image1

Swinscow TDV (1962) Pyrenocarpous lichens. 3. The genus Porina in the British Isles. Lichenologist 2, 6–56.
Pyrenocarpous lichens. 3. The genus Porina in the British Isles.CrossRef | open url image1

Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In ‘Molecular systematics’. (Eds DM Hillis, C Moritz, BK Mable) pp. 407–514. (Sinauer: Sunderland, MA)

Vainio EA (1896) Lichenes Antillarum a W. R. Elliott collecti. Journal of Botany British and Foreign 34, 292–297.

Vainio EA (1915) Additamenta ad lichenographiam Antillarum illustrandum. Annales Academiae Scientiarum Fennicae, Series A 6, 1–226.

Vainio EA (1923) Lichens in insula Trinidad a professore R. Thaxter collecti. Proceedings of the American Academy of Arts and Sciences 58, 131–147.
Lichens in insula Trinidad a professore R. Thaxter collecti.CrossRef | open url image1

Vězda A (1968) Taxonomische revision der Gattung Thelopsis Nyl. (lichenisierte Fungi). Folia Geobotanica et Phytotaxonomica 3, 363–406.

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.

Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available at http://ceb.csit.fsu.edu/awty [Verified 25 February 2014]

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.


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