Plant and Soil

, Volume 244, Issue 1–2, pp 75–83 | Cite as

Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi

  • Arthur Schüßler

Abstract

Geosiphon pyriformis(Kütz.) v. Wettstein is the only known example of a fungus living in endocytobiotic association with a cyanobacterium. The close phylogenetic relationship of Geosiphonwith some arbuscular mycorrhizal fungi (AMF) and the phylogenetic position of Geosiphonare shown in detail. Comprehensive small subunit (SSU) rRNA sequence analyses allow the erection of a new, molecular phylogeny-based taxonomic system for the AMF, including Geosiphon (Geosiphonaceae). Within the recently described phylum Glomeromycota (with one class, Glomeromycetes), a system including four orders was proposed. The erection of several new families will also be necessary. Evolutionary implications are discussed, referring to different possibilities of the influence of AMF on the colonization of the terrestrial habitat by plants.

arbuscular mycorrhiza evolution Geosiphon pyriformis Glomeromycota molecular phylogeny taxonomy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Benjamin R K 1979 Zygomycetes and their spores. In The Whole Fungus Vol 2. Ed. B Kendrick. pp 573-622. National Museum of Natural Sciences and National Museum of Canada, Ottawa.Google Scholar
  2. Benny G L, Humber R A and Morton J B 2001 Zygomycota: Zygomycetes. In The Mycota VII part A. Eds. McLaughlin, Mc Laughlin, Lemke. pp 113-146. Springer, Berlin, Heidelberg.Google Scholar
  3. Cavalier-Smith T 1998 A revised six-kingdom system of life. Biol. Rev. 73, 203-266.Google Scholar
  4. Ciferri R and Tomaselli R (1957) Prospetto di una sistematica microlichenologica. ATTI Series 5, Vol. XIV (1-3), pp 247-262. Istituto Botanico della Università Laboratorio Crittogamico Pavia, Pavia.Google Scholar
  5. Drude O and Schorler B 1916 Beiträge zur Flora Saxonica-III. Ñber eine merkwürdige Alge Sachsens [Geosiphon pyriformis (Ktz.) F. v. Wettst.]. Sitzungsberichte und Abhandlungen der Naturwissenschaftlichen Gesellschaft ISIS e.V., Dresden, pp 58-61.Google Scholar
  6. Engler A and Gilg E 1924 Geosiphonaceae (Siphonales). Syllabus der Pflanzenfamilien, Verlag von Gebrüder Borntraeger, Berlin, p. 24.Google Scholar
  7. Gao L L, Delp G and Smith S E 2001 Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytol. 151, 477-491.Google Scholar
  8. Gehrig H, Schüßler A and Kluge M, 1996 Geosiphon pyriformis, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the Glomerales: evidence by SSU rRNA analysis. J. Mol. Evol. 43, 71-81.Google Scholar
  9. Hawksworth D and Honegger R 1994 The lichen thallus: a symbiotic phenotype of nutritionally specialized fungi and its response to gall producers. In Plant Galls-Organisms, Interactions, Populations. Ed. M A J Williams. pp 77-98. The Systematics Association Special Volume No. 49, Clarendon Press, Oxford.Google Scholar
  10. Heckman D S, Geiser D M, Eidell B R, Stauffer R L, Kardos N L and Hedges S B 2001 Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129-1133.Google Scholar
  11. Knapp E 1933 Ñber Geosiphon pyriformis Fr. v. Wettst., eine intrazelluläre Pilz-Algen-Symbiose. Ber. Dtsch. Bot. Ges. 51, 210-217.Google Scholar
  12. Kützing F T 1849 Botrydium pyriformis. In Species algarum. Ed. F A Brockhaus. p 486. Lipsiae, Leipzig.Google Scholar
  13. Kramadibrata K, Walker C, Schwarzott D and Schüßler A 2000 A new species of Scutellospora with a coiled germination shield. Ann. Bot. 86, 21-27.Google Scholar
  14. Lutzoni F, Pagel M and Reeb V 2001 Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937-940.Google Scholar
  15. Malloch D W, Pirozynski K A and Raven P H 1980 Ecological and evolutionary significance of mycorrhizal symbiosis in vascular plants (a review). Proc. Natl. Acad. Sci. USA 77, 2113-2118.Google Scholar
  16. Mattick F (1954) XIII. Abteilung: Lichenes. Flechten. In A. Engler's Syllabus der Pflanzenfamilien-I. Allgemeiner Teil Bakterien bis Gymnospermen. Eds. H Melchior and E Werdermann. pp 204-218. Gebrüder Borntraeger, Berlin.Google Scholar
  17. Mollenhauer D 1992 Geosiphon pyriformis. In Algae and Symbiosis: Plants, Animals, Fungi, Viruses, Interactions Explored. Ed. W Reisser. pp 339-351 Biopress, Bristol.Google Scholar
  18. Morton J B 2000 Evolution of endophytism in arbuscular mycorrhizal fungi of Glomerales. In Microbial Endophytes. Eds. C W Bacon and J H White. pp 121-140. Marcel Dekker, New York.Google Scholar
  19. Morton J B and Benny G L 1990 Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomerales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomeraceae. Mycotaxon 37, 471-491.Google Scholar
  20. Morton J B and Redecker D 2001 Two new families of Glomerales, Archaeosporaceae and ParaGlomeraceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93, 181-195.Google Scholar
  21. O'Donnell K, Lutzoni F M, Ward T J and Benny G L 2001 Evolutionary relationships among mucoralean fungi (Zygomycota): Evidence for family polyphyly on a large scale. Mycologia 93, 286-296.Google Scholar
  22. Pirozynski K A and Malloch D W 1975 The origin of land plants: a matter of mycotrophism. BioSystems 6, 153-164.Google Scholar
  23. Redecker D, Kodner R and Graham L E 2000a Glomalean fungi from the Ordovician. Science 289, 1920-1921.Google Scholar
  24. Redecker D, Morton J B and Bruns T D 2000b Ancestral lineages of arbuscular mycorrhizal fungi.Mol. Phylogenet. Evol. 14, 276-284.Google Scholar
  25. Remy W, Taylor T N, Hass H and Kerp H 1994 Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91, 11841-11843.Google Scholar
  26. Sawaki H, Sugawara K and Saito M 1998 Phylogenetic position of an arbuscular mycorrhizal fungus, Acaulospora gerdemannii, and its synanamorph Glomus leptotichum, based upon 18S rRNA gene sequence. Mycoscience 39, 477-480.Google Scholar
  27. Sawaki H, Kojima T, Shinozaki N and Saito M 2001 Diversity of deeply branched arbuscular mycorrhizal fungi, Archaeospora spp., and their detection with PCR. Abstract of the Third International Conference on Mycorrhizas 8-13 July 2001, Adelaide, Australia.Google Scholar
  28. Schnepf E 1964 Zur Feinstruktur von Geosiphon pyriformis. Arch. Mikrobiol. 49, 112-131.Google Scholar
  29. Schüßler A 1999 Glomerales SSU rRNA gene diversity. New Phytol. 144, 205-207.Google Scholar
  30. Schüßler A 2000 Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10, 15-21.Google Scholar
  31. Schüßler A and Kluge M 2001 Geosiphon pyriformis, an endocytosymbiosis between fungus and Cyanobacteria, and its meaning as a model system for arbuscular mycorrhizal research. In The Mycota IX. Ed. B Hock. pp 151-161. Springer, Berlin, Heidelberg, New York.Google Scholar
  32. Schüßler A, Mollenhauer D, Schnepf E and Kluge M 1994 Geosiphon pyriformis, an endosymbiotic association of fungus and Cyanobacteria: the spore structure resembles that of arbuscular mycorrhizal (AM) fungi. Bot. Acta 107, 36-45.Google Scholar
  33. Schüßler A, Bonfante P, Schnepf E, Mollenhauer D and Kluge M 1996 Characterization of the Geosiphon pyriformis symbiosome by affinity techniques: confocal laser scanning microscopy (CLSM) and electron microscopy. Protoplasma 190, 53-67.Google Scholar
  34. Schüßler A, Gehrig H, Schwarzott D and Walker C 2001a Analysis of partial Glomerales SSU rRNA genes: implications for primer design and phylogeny. Mycol. Res. 105, 5-15.Google Scholar
  35. Schüßler A, Schwarzott D and Walker C 2001b A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res., in press.Google Scholar
  36. Schwarzott D, Walker C and Schüßler A 2001 Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomerales), is nonmonophyletic. Mol. Phylogenet. Evol., in pressGoogle Scholar
  37. Simon L, Bousquet J, Lévesque R C and Lalonde M 1993 Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67-69.Google Scholar
  38. Smith S E and Read D J 1997 Mycorrhizal symbiosis, 2nd edn. Academic Press, London, UK.Google Scholar
  39. Stubblefield S P, Taylor T N and Trappe J M 1987 Fossil mycorrhizae: a case for symbiosis. Science 237, 59-60.Google Scholar
  40. von Wettstein F 1915 Geosiphon Fr. v. Wettst., eine neue, interessante Siphonee. Österr. Bot. Z. 65, 145-156.Google Scholar
  41. Walker C 1992 Systematics and taxonomy of the arbuscular endomycorrhizal fungi (Glomerales)-a possible way forward. Agronomie 12, 887-897.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Arthur Schüßler
    • 1
  1. 1.Institut für Botanik, FB10Technische Universität DarmstadtDarmstadtGermany

Personalised recommendations