1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Lichenized Fungi and the Evolution of Symbiotic Organization

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Martin Grube1, Mats Wedin2
  • Editors: Joseph Heitman3, Barbara J. Howlett4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute of Plant Sciences, University of Graz, 8010 Graz, Austria; 2: Department of Botany, Swedish Museum of Natural History, 104 05 Stockholm, Sweden; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: School of Biosciences, The University of Melbourne, Victoria, NSW 3010, Australia
    • Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
  • Received 10 May 2016 Accepted 08 July 2016 Published 16 December 2016
  • Mats Wedin, [email protected]
image of Lichenized Fungi and the Evolution of Symbiotic Organization
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Lichenized Fungi and the Evolution of Symbiotic Organization, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0011-2016-1.gif /docserver/preview/fulltext/microbiolspec/4/6/FUNK-0011-2016-2.gif

  • Abstract:

    Lichen symbioses comprise a fascinating relationship between algae and fungi. The lichen symbiotic lifestyle evolved early in the evolution of ascomycetes and is also known from a few basidiomycetes. The ascomycete lineages have diversified in the lichenized stage to give rise to a tremendous variety of morphologies. Their thalli are often internally complex and stratified for optimized integration of algal and fungal metabolisms. Thalli are frequently colonized by specific nonlichenized fungi and occasionally also by other lichens. Microscopy has revealed various ways these fungi interact with their hosts. Besides the morphologically recognizable diversity of the lichen mycobionts and lichenicolous (lichen-inhabiting) fungi, many other microorganisms including other fungi and bacterial communities are now detected in lichens by culture-dependent and culture-independent approaches. The application of multi-omics approaches, refined microscopic techniques, and physiological studies has added to our knowledge of lichens, not only about the taxa involved in the lichen interactions, but also about their functions.

  • Citation: Grube M, Wedin M. 2016. Lichenized Fungi and the Evolution of Symbiotic Organization. Microbiol Spectrum 4(6):FUNK-0011-2016. doi:10.1128/microbiolspec.FUNK-0011-2016.

Key Concept Ranking

Confocal Laser Scanning Microscopy
0.45540437
0.45540437

References

1. Schwendener S. 1869. Die Algentypen der Flechtengonidien. Schultze, Basel, Switzerland.
2. Frank AB. 1877. Über die biologischen Verhältnisse des Thallus einiger Krustenflechten. Beitr Biol Pflanzen 2:123–200.
3. de Bary A. 1879. Die Erscheinung der Symbiose. Verlag von Karl J. Trübner Strasburg, Austria.
4. Sipman HJM, Aptroot A. 2001. Where are the missing lichens? Mycol Res 105:1433–1439 http://dx.doi.org/10.1017/S0953756201004932.
5. Piercey-Normore MD, Deduke C. 2011. Fungal farmers or algal escorts: lichen adaptation from the algal perspective. Mol Ecol 20:3708–3710 http://dx.doi.org/10.1111/j.1365-294X.2011.05191.x.
6. Honegger R, Edwards D, Axe L. 2013. The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol 197:264–275 http://dx.doi.org/10.1111/nph.12009.
7. Prieto M, Wedin M. 2013. Dating the diversification of the major lineages of Ascomycota ( Fungi). PLoS One 8:e65576. http://dx.doi.org/10.1371/journal.pone.0065576. [PubMed]
8. Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW. 2005. Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci USA 102:3141–3146 http://dx.doi.org/10.1073/pnas.0407716102. [PubMed]
9. Kranner I, Beckett RP, Hochman A, Nash TH III. 2008. Desiccation tolerance in lichens: a review. Bryologist 111:576–593 http://dx.doi.org/10.1639/0007-2745-111.4.576.
10. 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. Mycol Res 111:1116–1132 http://dx.doi.org/10.1016/j.mycres.2007.04.008. [PubMed]
11. Kohlmeyer J, Hawksworth DL, Volkmann-Kohlmeyer B. 2004. Observations on two marine and maritime “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol Prog 3:51–56 http://dx.doi.org/10.1007/s11557-006-0076-x.
12. Muggia L, Gueidan C, Knudsen K, Perlmutter G, Grube M. 2013. The lichen connections of black fungi. Mycopathologia 175:523–535 http://dx.doi.org/10.1007/s11046-012-9598-8. [PubMed]
13. Pérez-Ortega S, Garrido-Benavent I, Grube M, Olmo R, de los Rios A. 2016. Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales ( Dothideomyceta). Fungal Divers 80:285–300 http://dx.doi.org/10.1007/s13225-016-0361-1.
14. Hawksworth DL. 1988. The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linn Soc 96:3–20 http://dx.doi.org/10.1111/j.1095-8339.1988.tb00623.x.
15. Aptroot A. 1991. A Monograph of the Pyrenulaceae (excluding Anthracothecium and Pyrenula ) and the Requienellaceae , with Notes on the Pleomassariaceae , the Trypetheliaceae and Mycomicrothelia (Lichenized and Non-lichenized Ascomycetes). Bibl Lichenol 44:1–178.
16. Aguirre-Hudson B. 1991. A taxonomic study of the species referred to the ascomycete genus Leptorhaphis. Bull Br Mus Nat Hist Botany 21:85–192.
17. Wedin M, Döring H, Gilenstam G. 2004. Saprotrophy and lichenization as options for the same fungal species on different substrata: environmental plasticity and fungal lifestyles in the Stictis- Conotrema complex. New Phytol 164:459–465 http://dx.doi.org/10.1111/j.1469-8137.2004.01198.x.
18. Vainio EA. 1890. Étude sur classification naturelle et morphologie des lichens du Brésil. Acta Soc Fauna Flora Fennica, Helsinki 7:1–256.
19. Zahlbruckner A. 1907. Lichenes (Flechten) B. Spezieller Teil, p 49–249. In Engler A, Prantl K (ed), Die natürlichen Pflanzenfamilien. Teil, Leipzig, Germany.
20. Zahlbruckner A. 1926. Lichenes (Flechten) B. Spezieller Teil, p 61–270. In Engler A, Prantl K (ed), Die natürlichen Pflanzenfamilien. 2, vol 8. Auflage, Leipzig, Germany.
21. Nannfeldt JA. 1932. Studien über die Morphologie und Systematik der nicht-lichenisierten inoperculaten Discomyceten. Nov Act Reg Soc Upsal 8:1–368.
22. Santesson R. 1952. Foliicolous lichens I. A revision of the taxonomy of the obligately foliicolous, lichenized fungi. Symbolae Bot Upsal 12:1–590.
23. Santesson R.1953. The new systematics of lichenized fungi, p 809-810. In Osvald H, Aberg E (ed) Proceedings of the 7th International Botanical Congress, Stockholm 1950, Almquist and Wiksell, Waltham, MA.
24. Santesson R. 1954. Fungal symbionts of lichens. Taxon 3:147–148 http://dx.doi.org/10.2307/1217328.
25. Henssen A, Jahns M. 1974. Lichenes. Eine Einführung in die Flechtenkunde. G. Thieme, Stuttgart, Germany.
26. Henssen A, Keuck G, Renner B, Vobis G. 1981. The lecanoralean centrum, p 138–234. In Reynolds DR (ed), Ascomycete Systematics. The Luttrellian Concept. Springer-Verlag, New York, NY. http://dx.doi.org/10.1007/978-1-4612-5844-5_10
27. Döring H, Lumbsch HT. 1998. Ascoma ontogeny: is this character set of any use in the systematics of lichenized ascomycetes. Lichenologist 30:489–500.
28. Hafellner J. 1984. Studien in Richtung einer natürlicheren Gliederung der Sammelfamilien Lecanoraceae und Lecideaceae. Beihefte zur. Nova Hedwigia 79:241–371.
29. Rambold G, Triebel D. 1992. The inter-lecanoralean associations. Bibl Lichenol 48:1–201.
30. Hafellner J, Hertel H, Rambold G, Timdal E. 1993. A new outline of the Lecanorales. First International Workshop on Ascomycete Systematics, Paris, France. http://dx.doi.org/10.13140/RG.2.2.29682.91847.
31. Gargas A, DePriest PT, Grube M, Tehler A. 1995. Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268:1492–1495 http://dx.doi.org/10.1126/science.7770775. [PubMed]
32. Lutzoni F, Pagel M, Reeb V. 2001. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937–940 http://dx.doi.org/10.1038/35082053.
33. Schoch CL, et al. 2009. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239 http://dx.doi.org/10.1093/sysbio/syp020. [PubMed]
34. Jaklitsch W, Baral HO, Lücking R, Lumbsch HT. 2016. Syllabus of Plant Families. Part 1/2 Ascomycota. Borntraeger Science Publishers, Stuttgart, Germany.
35. Gueidan C, Aptroot A, Da Silva Cáceres ME, Badali H, Stenroos S. 2014. A reappraisal of orders and families within the subclass Chaetothyriomycetidae ( Eurotiomycetes, Ascomycota). Mycol Prog 13:990. http://dx.doi.org/10.1007/s11557-014-0990-2.
36. James TY, et al. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822 http://dx.doi.org/10.1038/nature05110. [PubMed]
37. Nelsen MP, Lücking R, Mbatchou JS, Andrew CJ, Spielmann AA, Lumbsch HT. 2011. New insights into relationships of lichen-forming Dothideomycetes. Fungal Divers 51:155–162 http://dx.doi.org/10.1007/s13225-011-0144-7.
38. Prieto M, Baloch E, Tehler A, Wedin M. 2013. Mazaedium evolution in the Ascomycota ( Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29:296–308 http://dx.doi.org/10.1111/j.1096-0031.2012.00429.x.
39. Lücking R, Dal-Forno M, Sikaroodi M, Gillevet PM, Bungartz F, Moncada B, Yánez-Ayabaca A, Chaves JL, Coca LF, Lawrey JD. 2014. A single macrolichen constitutes hundreds of unrecognized species. Proc Natl Acad Sci USA 111:11091–11096 http://dx.doi.org/10.1073/pnas.1403517111.
40. Dal-Forno M, Lawrey JD, Sikaroodi M, Bhattarai S, Gillevet PM, Sulzbacher M, Lücking R. 2013. Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema ( Agaricales: Hygrophoraceae). Fungal Biol 117:584–598 http://dx.doi.org/10.1016/j.funbio.2013.05.006.
41. Grube M. 1998. Classification and phylogeny in the Arthoniales (lichenized Ascomycetes). Bryologist 101:377–391 http://dx.doi.org/10.1639/0007-2745(1998)101[377:CAPITA]2.0.CO;2.
42. Ertz D, Tehler A. 2011. The phylogeny of Arthoniales ( Pezizomycotina) inferred from nucLSU and RPB2 sequences. Fungal Divers 49:47–71 http://dx.doi.org/10.1007/s13225-010-0080-y.
43. Frisch A, Thor G, Ertz D, Grube M. 2014. The Arthonialean challenge: restructuring Arthoniaceae. Taxon 63:727–744 http://dx.doi.org/10.12705/634.20.
44. Schoch CL, et al. 2009. A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15, S10 http://dx.doi.org/10.3114/sim.2009.64.01. [PubMed]
45. Gueidan C, Villaseñor CR, de Hoog GS, Gorbushina AA, Untereiner WA, Lutzoni F. 2008. A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud Mycol 61:111–119 http://dx.doi.org/10.3114/sim.2008.61.11. [PubMed]
46. Lumbsch HT, Schmitt I, Palice Z, Wiklund E, Ekman S, Wedin M. 2004. Supraordinal phylogenetic relationships of Lecanoromycetes based on a Bayesian analysis of combined nuclear and mitochondrial sequences. Mol Phylogenet Evol 31:822–832 http://dx.doi.org/10.1016/j.ympev.2003.11.001.
47. Wedin M, Wiklund E, Crewe A, Döring H, Ekman S, Nyberg A, Schmitt I, Lumbsch HT. 2005. Phylogenetic relationships of Lecanoromycetes ( Ascomycota) as revealed by analyses of mtSSU and nLSU rDNA sequence data. Mycol Res 109:159–172 http://dx.doi.org/10.1017/S0953756204002102.
48. Ekman S, Andersen HL, Wedin M. 2008. The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized Ascomycota). Syst Biol 57:141–156 http://dx.doi.org/10.1080/10635150801910451.
49. Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J, Reeb V, Hodkinson BP, Kukwa M, Lücking R, Hestmark G, Otalora MG, Rauhut A, Büdel B, Scheidegger C, Timdal E, Stenroos S, Brodo I, Perlmutter GB, Ertz D, Diederich P, Lendemer JC, May P, Schoch CL, Arnold AE, Gueidan C, Tripp E, Yahr R, Robertson C, Lutzoni F. 2006. New insights into classification and evolution of the Lecanoromycetes ( Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98:1088–1103 http://dx.doi.org/10.3852/mycologia.98.6.1088.
50. Tibell L. 1998. Practice and prejudice in lichen classification. Lichenologist 30:439–453 http://dx.doi.org/10.1017/S0024282992000434.
51. Tibell L. 1984. A reappraisal of the taxonomy of Caliciales. Beih Nova Hedwigia 79:597–713.
52. Schmull M, Miadlikowska J, Pelzer M, Stocker-Wörgötter E, Hofstetter V, Fraker E, Hodkinson BP, Reeb V, Kukwa M, Lumbsch HT, Kauff F, Lutzoni F. 2011. Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner ( Lecanoromycetes, Ascomycota). Mycologia 103:983–1003 http://dx.doi.org/10.3852/10-234.
53. Wedin M, Wiklund E, Jørgensen PM, Ekman S. 2009. Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens ( Peltigerales, Ascomycetes). Mol Phylogenet Evol 53:862–871 http://dx.doi.org/10.1016/j.ympev.2009.08.013.
54. Otálora MAG, Aragón G, Molina MC, Martínez I, Lutzoni F. 2010. Disentangling the Collema-Leptogium complex through a molecular phylogenetic study of the Collemataceae ( Peltigerales, lichen-forming Ascomycota). Mycologia 102:279–290 http://dx.doi.org/10.3852/09-114.
55. 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. Mol Phylogenet Evol 44:812–824 http://dx.doi.org/10.1016/j.ympev.2006.11.029.
56. Divakar PK, et al. 2015. Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytol 208:1217–1226 http://dx.doi.org/10.1111/nph.13553.
57. Gaya E, Högnabba F, Holguin A, Molnar K, Fernández-Brime S, Stenroos S, Arup U, Søchting U, Van den Boom P, Lücking R, Sipman HJM, Lutzoni F. 2012. Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales ( Pezizomycotina, Ascomycota). Mol Phylogenet Evol 63:374–387 http://dx.doi.org/10.1016/j.ympev.2012.01.012.
58. Arup U, Søchting U, Frödén P. 2013. A new taxonomy of the family Teloschistaceae. Nordic J Bot 31:016–083.
59. 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.
60. Resl P, Schneider K, Westberg M, Printzen C, Palice Z, Thor G, Fryday A, Mayrhofer H, Spribille T. 2015. Diagnostics for a troubled backbone: testing topological hypotheses of trapelioid lichenized fungi in a large-scale phylogeny of Ostropomycetidae ( Lecanoromycetes). Fungal Divers 73:239–258 http://dx.doi.org/10.1007/s13225-015-0332-y.
61. Miadlikowska J, Kauff F, Högnabba F, Oliver JC, Molnár K, Fraker E, Gaya E, Hafellner J, Hofstetter V, Gueidan C, Otálora MAG, Hodkinson B, Kukwa M, Lücking R, Björk C, Sipman HJM, Burgaz AR, Thell A, Passo A, Myllys L, Goward T, Fernández-Brime S, Hestmark G, Lendemer J, Lumbsch HT, Schmull M, Schoch CL, Sérusiaux E, Maddison DR, Arnold AE, Lutzoni F, Stenroos S. 2014. A multigene phylogenetic synthesis for the class Lecanoromycetes ( Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Mol Phylogenet Evol 79:132–168 http://dx.doi.org/10.1016/j.ympev.2014.04.003.
62. Lumbsch HT, Parnmen S, Kraichak E, Papong KB, Lücking R. 2014. High frequency of character transformations is phylogenetically structured within the lichenized fungal family Graphidaceae ( Ascomycota: ostropales). Syst Biodivers 12:271–291 http://dx.doi.org/10.1080/14772000.2014.905506.
63. Stenroos S, Laukka T, Huhtinen S, Döbbeler P, Myllys L, Syrjänen K, Hyvönen J. 2010. Multiple origins of symbioses between ascomycetes and bryophytes suggested by a five-gene phylogeny. Cladistics 26:281–300 http://dx.doi.org/10.1111/j.1096-0031.2009.00284.x.
64. Leavitt SD, Grewe F, Widhelm T, Muggia L, Wray B, Lumbsch HT. 2016. Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Sci Rep 6:22262. http://dx.doi.org/10.1038/srep22262.
65. Park SY, Jeong MH, Wang HY, Kim JA, Yu NH, Kim S, Cheong YH, Kang S, Lee YH, Hur JS. 2013c. Agrobacterium tumefaciens-mediated transformation of the lichen fungus, Umbilicaria muehlenbergii. PLoS One 8:e83896. http://dx.doi.org/10.1371/journal.pone.0083896.
66. Armaleo D, Sun X, Culberson C. 2011. Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 103:741–754 http://dx.doi.org/10.3852/10-335. [PubMed]
67. Abdel-Hameed M, Bertrand RL, Piercey-Normore MD, Sorensen JL. 2016. Putative identification of the usnic acid biosynthetic gene cluster by de novo whole-genome sequencing of a lichen-forming fungus. Fungal Biol 120:306–316 http://dx.doi.org/10.1016/j.funbio.2015.10.009.
68. Kampa A, Gagunashvili AN, Gulder TA, Morinaka BI, Daolio C, Godejohann M, Miao VP, Piel J, Andrésson Ó. 2013. Metagenomic natural product discovery in lichen provides evidence for a family of biosynthetic pathways in diverse symbioses. Proc Natl Acad Sci USA 110:E3129–E3137 http://dx.doi.org/10.1073/pnas.1305867110.
69. McDonald TR, Dietrich FS, Lutzoni F. 2012. Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification. Mol Biol Evol 29:51–60 http://dx.doi.org/10.1093/molbev/msr123.
70. McDonald TR, Mueller O, Dietrich FS, Lutzoni F. 2013. High-throughput genome sequencing of lichenizing fungi to assess gene loss in the ammonium transporter/ammonia permease gene family. BMC Genomics 14:225. http://dx.doi.org/10.1186/1471-2164-14-225.
71. Wang YY, Zhang T, Zhou QM, Wei JC. 2011. Construction and characterization of a full-length cDNA library from mycobiont of Endocarpon pusillum (lichen-forming Ascomycota). World J Microbiol Biotechnol 27:2873–2884 http://dx.doi.org/10.1007/s11274-011-0768-5.
72. Wang Y, Zhang X, Zhou Q, Zhang X, Wei J. 2015. Comparative transcriptome analysis of the lichen-forming fungus Endocarpon pusillum elucidates its drought adaptation mechanisms. Sci China Life Sci 58:89–100 http://dx.doi.org/10.1007/s11427-014-4760-9.
73. Miao VPW, Manoharan SS, Snæbjarnarson V, Andrésson ÓS. 2012. Expression of lec-1, a mycobiont gene encoding a galectin-like protein in the lichen Peltigera membranacea. Symbiosis 57:23–31 http://dx.doi.org/10.1007/s13199-012-0175-1.
74. Junttila S, Rudd S. 2012. Characterization of a transcriptome from a non-model organism, Cladonia rangiferina, the grey reindeer lichen, using high-throughput next generation sequencing and EST sequence data. BMC Genomics 13:575. http://dx.doi.org/10.1186/1471-2164-13-575.
75. Schneider T, Schmid E, de Castro JV Jr, Cardinale M, Eberl L, Grube M, Berg G, Riedel K. 2011. Structure and function of the symbiosis partners of the lung lichen ( Lobaria pulmonaria L. Hoffm.) analyzed by metaproteomics. Proteomics 11:2752–2756 http://dx.doi.org/10.1002/pmic.201000679.
76. Junttila S, Laiho A, Gyenesei A, Rudd S. 2013. Whole transcriptome characterization of the effects of dehydration and rehydration on Cladonia rangiferina, the grey reindeer lichen. BMC Genomics 14:870. http://dx.doi.org/10.1186/1471-2164-14-870. [PubMed]
77. Manoharan SS, Miao VPW, Andrésson ÓS. 2012. LEC-2, a highly variable lectin in the lichen Peltigera membranacea. Symbiosis 58:91–98 http://dx.doi.org/10.1007/s13199-012-0206-y. [PubMed]
78. Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G. 2015. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424 http://dx.doi.org/10.1038/ismej.2014.138.
79. Kosugi M, Arita M, Shizuma R, Moriyama Y, Kashino Y, Koike H, Satoh K. 2009. Responses to desiccation stress in lichens are different from those in their photobionts. Plant Cell Physiol 50:879–888 http://dx.doi.org/10.1093/pcp/pcp043.
80. Meessen J, Ott S. 2013. Recognition mechanisms during the precontact state of lichens. I. Mycobiont-photobiont interactions of the mycobiont of Fulgensia bracteata. Symbiosis 59:121–130 http://dx.doi.org/10.1007/s13199-013-0232-4.
81. Meessen J, Eppenstein S, Ott S. 2013. Recognition mechanisms during the precontact state of lichens. II. Influence of algal exudates and ribitol on the response of the mycobiont of Fulgensia bracteata. Symbiosis 59:131–143 http://dx.doi.org/10.1007/s13199-012-0219-6.
82. Dietz S, Hartung W. 1999. The effect of abscisic acid on chlorophyll fluorescence in lichens under extreme water regimes. New Phytol 143:495–501 http://dx.doi.org/10.1046/j.1469-8137.1999.00473.x.
83. Ott S, Krieg T, Spanier U, Schieleit P. 2000. Phytohormones in lichens with emphasis on ethylene biosynthesis and functional aspects on lichen symbiosis. Phyton 40:83–94.
84. Wang XY, Wei XL, Luo H, Kim JA, Jeon HS, Koh YJ, Hur JS. 2010. Plant hormones promote growth in lichen-forming fungi. Mycobiology 38:176–179 http://dx.doi.org/10.4489/MYCO.2010.38.3.176. [PubMed]
85. Honegger R. 1991. Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42:553–578 http://dx.doi.org/10.1146/annurev.pp.42.060191.003005.
86. Honegger R. 2012. The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts, p 287–339. In Hock B (ed), The Mycota 9. Fungal Associations, 2nd ed. Springer, Berlin, Germany. http://dx.doi.org/10.1007/978-3-642-30826-0_15
87. Rikkinen J. 2015. Cyanolichens. Biodivers Conserv 24:973–993 http://dx.doi.org/10.1007/s10531-015-0906-8.
88. James PW, Henssen A. 1976. The morphological and taxonomic significance of cephalodia, p 27–77. In Brown DH, Hawksworth DL, Bailey RH (ed), Lichenology: Progress and Problems. Academic Press, London, United Kingdom. [PubMed]
89. Hyvärinen M, Härdling R, Tuomi J. 2002. Cyanobacterial lichen symbiosis: the fungal partner as an optimal harvester. Oikos 98:498–504 http://dx.doi.org/10.1034/j.1600-0706.2002.980314.x.
90. Henskens FL, Green TGA, Wilkins A. 2012. Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot (Lond) 110:555–563 http://dx.doi.org/10.1093/aob/mcs108.
91. Armaleo D, Clerc P. 1991. Lichen chimeras: DNA analysis suggests that one fungus forms two morphotypes. Exp Mycol 15:1–10 http://dx.doi.org/10.1016/0147-5975(91)90002-U.
92. Magain N, Goffinet B, Sérusiaux E. 2012. Further photomorphs in the lichen family Lobariaceae from Reunion (Mascarene archipelago) with notes on the phylogeny of Dendriscocaulon cyanomorphs. Bryologist 115:243–254 http://dx.doi.org/10.1639/0007-2745-115.2.243.
93. Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE, Joneson S, O’Brien H, Nelsen MP, Duque-Thüs R, Grube M, Friedl T, Brodie J, Andrew CJ, Lücking R, Lutzoni F, Gueidan C. 2011. Revisiting photobiont diversity in the lichen family Verrucariaceae ( Ascomycota). Eur J Phycol 46:399–415 http://dx.doi.org/10.1080/09670262.2011.629788.
94. Blaha J, Baloch E, Grube M. 2006. High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola ( Lecanoraceae, Ascomycota). Biol J Linn Soc Lond 88:283–293 http://dx.doi.org/10.1111/j.1095-8312.2006.00640.x.
95. Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martín MP, Printzen C. 2011. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20:1208–1232 http://dx.doi.org/10.1111/j.1365-294X.2010.04993.x.
96. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416 http://dx.doi.org/10.1038/ismej.2007.106. [PubMed]
97. Wedin M, Maier S, Fernandez-Brime S, Cronholm B, Westberg M, Grube M. 2016. Microbiome change by symbiotic invasion in lichens. Environ Microbiol 18:1428–1439 http://dx.doi.org/10.1111/1462-2920.13032. [PubMed]
98. Rikkinen J, Oksanen I, Lohtander K. 2002. Lichen guilds share related cyanobacterial symbionts. Science 297:357 http://dx.doi.org/10.1126/science.1072961. [PubMed]
99. Rikkinen J. 2003. Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34:99–110.
100. Lawrey JD, Diederich P. 2003. Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106:80–120 http://dx.doi.org/10.1639/0007-2745(2003)106[0080:LFIEAB]2.0.CO;2.
101. Petrini O, Hake U, Dreyfuss MM. 1990. An analysis of fungal communities isolated from fruticose lichens. Mycologia 82:444–451 http://dx.doi.org/10.2307/3760015.
102. Girlanda M, Isocrono D, Bianco C, Luppi-Mosca AM. 1997. Two foliose lichens as microfungal ecological niches. Mycologia 89:531–536 http://dx.doi.org/10.2307/3760987.
103. Prillinger H, Kraepelin G, Lopandic K, Schweigkofler W, Molnár O, Weigang F, Dreyfuss MM. 1997. New species of Fellomyces isolated from epiphytic lichen species. Syst Appl Microbiol 20:572–584 http://dx.doi.org/10.1016/S0723-2020(97)80029-X.
104. Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F. 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297 http://dx.doi.org/10.1093/sysbio/syp001.
105. Crittenden PD, David JC, Hawksworth DL, Campbell FS. 1995. Attempted isolation and success in the culturing of a broad spectrum of lichen-forming and lichenicolous fungi. New Phytol 130:267–297 http://dx.doi.org/10.1111/j.1469-8137.1995.tb03048.x.
106. Fleischhacker A, Grube M, Kopun T, Hafellner J, Muggia L. 2015. Community analyses uncover high diversity of lichenicolous fungi in alpine habitats. Microb Ecol 70:348–360 http://dx.doi.org/10.1007/s00248-015-0579-6. [PubMed]
107. Zhang T, Wei XL, Zhang YQ, Liu HY, Yu LY. 2015. Diversity and distribution of lichen-associated fungi in the Ny-Ålesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Sci Rep 5:14850 http://dx.doi.org/10.1038/srep14850.
108. Werth S, Millanes AM, Wedin M, Scheidegger C. 2013. Lichenicolous fungi show population subdivision by host species but do not share population history with their hosts. Fungal Biol 117:71–84 http://dx.doi.org/10.1016/j.funbio.2012.11.007.
109. Millanes AM, Diederich P, Wedin M. 2016. Cyphobasidium gen. nov., a new lichen-inhabiting lineage in the Cystobasidiomycetes ( Pucciniomycotina, Basidiomycota, Fungi). Fungal Biol 120:1468–1477 doi:10.1016/j.funbio.2015.12.003
110. Cardinale M, Puglia AM, Grube M. 2006. Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495 http://dx.doi.org/10.1111/j.1574-6941.2006.00133.x. [PubMed]
111. Grube M, Berg G. 2009. Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85 http://dx.doi.org/10.1016/j.fbr.2009.10.001.
112. Grube M, Cardinale M, de Castro JV Jr, Müller H, Berg G. 2009. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115 http://dx.doi.org/10.1038/ismej.2009.63.
113. Hodkinson BP, Lutzoni F. 2009. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180 http://dx.doi.org/10.1007/s13199-009-0049-3.
114. Selbmann L, Zucconi L, Ruisi S, Grube M, Cardinale M, Onofri S. 2010. Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance. Polar Biol 33:71–83 http://dx.doi.org/10.1007/s00300-009-0686-2.
115. Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N. 2011. Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314 http://dx.doi.org/10.1128/AEM.02257-10. [PubMed]
116. Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Ovreås L. 2011. Microbial metacommunities in the lichen-rock habitat. Environ Microbiol Rep 3:434–442 http://dx.doi.org/10.1111/j.1758-2229.2010.00206.x. [PubMed]
117. Mushegian AA, Peterson CN, Baker CC, Pringle A. 2011. Bacterial diversity across individual lichens. Appl Environ Microbiol 77:4249–4252 http://dx.doi.org/10.1128/AEM.02850-10. [PubMed]
118. Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F. 2012. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161 http://dx.doi.org/10.1111/j.1462-2920.2011.02560.x.
119. Cardinale M, Vieira de Castro J Jr, Müller H, Berg G, Grube M. 2008. In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71 http://dx.doi.org/10.1111/j.1574-6941.2008.00546.x.
120. Erlacher A, Cernava T, Cardinale M, Soh J, Sensen CW, Grube M, Berg G. 2015. Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6:53. http://dx.doi.org/10.3389/fmicb.2015.00053. [PubMed]
121. Honegger R. 1992. Lichens: mycobiont-photobiont relationships, p 225–275. In Reisser W (ed), Algae and Symbiosis. Biopress, Bristol, United Kingdom.
122. Juntilla S. 2015. Characterisation of Cladonia rangiferina transcriptome and genome, and the effects of dehydration and rehydration on its gene expression. Ann Univ Turkensis, Doctoral thesis.
123. Park SY, Choi J, Kim JA, Jeong MH, Kim S, Lee YH, Hur JS. 2013. Draft genome sequence of Cladonia macilenta KoLRI003786, a lichen-forming fungus producing biruloquinone. Genome Announc 1:e00695-13. http://dx.doi.org/10.1128/genomeA.00695-13
124. Park SY, Choi J, Lee GW, Kim JA, Oh SO, Jeong MH, Yu NH, Kim S, Lee YH, Hur JS. 2014. Draft genome sequence of lichen-forming fungus Cladonia metacorallifera strain KoLRI002260. Genome Announc 2:e01065-13. http://dx.doi.org/10.1128/genomeA.01065-13.
125. Wang YY, Liu B, Zhang XY, Zhou QM, Zhang T, Li H, Yu YF, Zhang XL, Hao XY, Wang M, Wang L, Wei JC. 2014. Genome characteristics reveal the impact of lichenization on lichen-forming fungus Endocarpon pusillum Hedwig (Verrucariales, Ascomycota). BMC Genomics 15:34. http://dx.doi.org/10.1186/1471-2164-15-34.
126. Park SY, Choi J, Kim JA, Yu NH, Kim S, Kondratyuk SY, Lee YH, Hur JS. 2013. Draft genome sequence of lichen-forming fungus Caloplaca flavorubescens strain KoLRI002931. Genome Announc 1:e00678-13. http://dx.doi.org/10.1128/genomeA.00678-13
127. Park SY, Choi J, Lee GW, Jeong MH, Kim JA, Oh SO, Lee YH, Hur JS. 2014. Draft genome sequence of Umbilicaria muehlenbergii KoLRILF000956, a lichen-forming fungus amenable to genetic manipulation. Genome Announc 2:e00357-14. http://dx.doi.org/10.1128/genomeA.00357-14.
128. Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, Cutcheon JP. 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016
2016-12-16
2019-08-22

Abstract:

Lichen symbioses comprise a fascinating relationship between algae and fungi. The lichen symbiotic lifestyle evolved early in the evolution of ascomycetes and is also known from a few basidiomycetes. The ascomycete lineages have diversified in the lichenized stage to give rise to a tremendous variety of morphologies. Their thalli are often internally complex and stratified for optimized integration of algal and fungal metabolisms. Thalli are frequently colonized by specific nonlichenized fungi and occasionally also by other lichens. Microscopy has revealed various ways these fungi interact with their hosts. Besides the morphologically recognizable diversity of the lichen mycobionts and lichenicolous (lichen-inhabiting) fungi, many other microorganisms including other fungi and bacterial communities are now detected in lichens by culture-dependent and culture-independent approaches. The application of multi-omics approaches, refined microscopic techniques, and physiological studies has added to our knowledge of lichens, not only about the taxa involved in the lichen interactions, but also about their functions.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Lichenized Fungi and the Evolution of Symbiotic Organization
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-1,properties={foaf_givenname=Martin, foaf_name=Martin Grube, foaf_surname=Grube, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-2,properties={foaf_givenname=Mats, foaf_name=Mats Wedin, foaf_surname=Wedin, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-aff2]]}]]
Citation: Grube M, Wedin M. 2016. Lichenized fungi and the evolution of symbiotic organization. microbiolspec 4(6): doi:10.1128/microbiolspec.FUNK-0011-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig1
FIGURE 1

Diverse shapes of lichen thalli. Coral-like fruticose (shrub-like) thallus of . Photo: Birgitta Strömbäck. Foliose (leaf-like) thalli of and covering the trunk of a in an old-growth spruce-dominated forest. Photo: Mats Wedin. Crustose (crust-like) thallus of growing on a siliceous rock. Photo: Martin Westberg.

microbiolspec/4/6/FUNK-0011-2016-fig1_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig1.gif
Image of FIGURE 1
FIGURE 1

Diverse shapes of lichen thalli. Coral-like fruticose (shrub-like) thallus of . Photo: Birgitta Strömbäck. Foliose (leaf-like) thalli of and covering the trunk of a in an old-growth spruce-dominated forest. Photo: Mats Wedin. Crustose (crust-like) thallus of growing on a siliceous rock. Photo: Martin Westberg.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig2
FIGURE 2

Substantial biomass of lichens. Scandinavian costal lichen heath dominated by reindeer lichens ( spp.). Photo: Birgitta Strömbäck. Lichen-dominated soil crust community on the Great Alvar of Öland (Sweden). Photo: Martin Westberg. Abundant lichen cover dominated by in a New Zealand cool temperate rain forest. Photo: Birgitta Strömbäck.

microbiolspec/4/6/FUNK-0011-2016-fig2_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig2.gif
Image of FIGURE 2
FIGURE 2

Substantial biomass of lichens. Scandinavian costal lichen heath dominated by reindeer lichens ( spp.). Photo: Birgitta Strömbäck. Lichen-dominated soil crust community on the Great Alvar of Öland (Sweden). Photo: Martin Westberg. Abundant lichen cover dominated by in a New Zealand cool temperate rain forest. Photo: Birgitta Strömbäck.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig3
FIGURE 3

Vertical section through a thallus of , a foliose lichen. A distinct layer of green algal cells is clearly visible under the uppermost cortex; all other structures are made up by fungal hyphae. Photo: Einar Timdal.

microbiolspec/4/6/FUNK-0011-2016-fig3_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig3.gif
Image of FIGURE 3
FIGURE 3

Vertical section through a thallus of , a foliose lichen. A distinct layer of green algal cells is clearly visible under the uppermost cortex; all other structures are made up by fungal hyphae. Photo: Einar Timdal.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig4
FIGURE 4

Vegetative dispersal in lichens. Soralia formed along the thallus margins in . These structures produce soredia, small granules of algal cells surrounded by fungal hyphae. Photo: Einar Timdal. Simple, cylindrical isidia formed on the thallus upper surface by . Photo: Einar Timdal.

microbiolspec/4/6/FUNK-0011-2016-fig4_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig4.gif
Image of FIGURE 4
FIGURE 4

Vegetative dispersal in lichens. Soralia formed along the thallus margins in . These structures produce soredia, small granules of algal cells surrounded by fungal hyphae. Photo: Einar Timdal. Simple, cylindrical isidia formed on the thallus upper surface by . Photo: Einar Timdal.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig5
FIGURE 5

Optional lichenization: . Apothecium of a saprotrophic colony on dead aspen () wood. Photo: Lucia Muggia. Lichenized morph on aspen bark. Note the green algal colonies around the young apothecium. Photo: Lucia Muggia.

microbiolspec/4/6/FUNK-0011-2016-fig5_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig5.gif
Image of FIGURE 5
FIGURE 5

Optional lichenization: . Apothecium of a saprotrophic colony on dead aspen () wood. Photo: Lucia Muggia. Lichenized morph on aspen bark. Note the green algal colonies around the young apothecium. Photo: Lucia Muggia.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig6
FIGURE 6

Cephalodia visible as dark structures that include cyanobacteria, on . Photo: Einar Timdal. Phycosymbiodemes with different morphologies: with joined photomorphs. Note green-algal foliose parts growing out from the basal cyanobacterial fruticose parts. Photo: Mats Wedin.

microbiolspec/4/6/FUNK-0011-2016-fig6_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig6.gif
Image of FIGURE 6
FIGURE 6

Cephalodia visible as dark structures that include cyanobacteria, on . Photo: Einar Timdal. Phycosymbiodemes with different morphologies: with joined photomorphs. Note green-algal foliose parts growing out from the basal cyanobacterial fruticose parts. Photo: Mats Wedin.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.fig7
FIGURE 7

Symbiotic invasion. The transition of thallus into thallus by invasion of the latter. Uninfected thallus. Photo: Einar Timdal. thallus with clear infection (whitish areas) with typical apothecia (dark patches in the whitish areas). Photo: Einar Timdal. An almost complete takeover by , with only small remnants of . Photo: Martin Westberg.

microbiolspec/4/6/FUNK-0011-2016-fig7_thmb.gif
microbiolspec/4/6/FUNK-0011-2016-fig7.gif
Image of FIGURE 7
FIGURE 7

Symbiotic invasion. The transition of thallus into thallus by invasion of the latter. Uninfected thallus. Photo: Einar Timdal. thallus with clear infection (whitish areas) with typical apothecia (dark patches in the whitish areas). Photo: Einar Timdal. An almost complete takeover by , with only small remnants of . Photo: Martin Westberg.

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Lichenized Fungi and the Evolution of Symbiotic Organization
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-1,properties={foaf_givenname=Martin, foaf_name=Martin Grube, foaf_surname=Grube, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-2,properties={foaf_givenname=Mats, foaf_name=Mats Wedin, foaf_surname=Wedin, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016-aff2]]}]]
Citation: Grube M, Wedin M. 2016. Lichenized fungi and the evolution of symbiotic organization. microbiolspec 4(6): doi:10.1128/microbiolspec.FUNK-0011-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0011-2016.T1
TABLE 1

Lichenized fungal species for which genome information is available (as of March 2016)

Generic image for table
TABLE 1

Lichenized fungal species for which genome information is available (as of March 2016)

Source: microbiolspec December 2016 vol. 4 no. 6 doi:10.1128/microbiolspec.FUNK-0011-2016

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error