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5 The Geosiphon–Nostoc Endosymbiosis and Its Role as a Model for Arbuscular Mycorrhiza Research

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Fungal Associations

Part of the book series: The Mycota ((MYCOTA,volume 9))

Abstract

The only known endosymbiosis with cyanobacteria (endocyanosis) formed by a fungus is that of Geosiphon pyriformis with Nostoc punctiforme. The obligatory symbiotic fungus, G. pyriformis, belongs in the Glomeromycota, members of which form arbuscular mycorrhiza (AM) with the majority of vascular land plants and also with many ‘lower’ plants, thus driving most terrestrial ecosystems. There are many parallels between the Geosiphon–Nostoc and the AM symbioses. The fungal hyphae absorb soil nutrients and water, which they provide to the photoautotrophic partner. In turn, the plant supplies the biotrophic fungus with energy-rich soluble carbohydrates derived from photosynthesis. Here, the knowledge about the Geosiphon symbiosis is reviewed, as well as its role as a model symbiosis for the AM, a symbiosis inherently difficult to study. This is turned into relation to the probably >450 million years long-lasting co-evolution of AM fungi and land plants, and the functioning and ecology of the AM symbiosis.

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References

  • Bilger W, Büdel B, Mollenhauer R, Mollenhauer D (1994) Photosynthetic activity of two developmental stages of a Nostoc strain (cyanobacteria) isolated from Geosiphon pyriforme (Mycota). J Phycol 30:225–230

    Article  CAS  Google Scholar 

  • Bonfante P, Grippiolo R (1984) Cytochemical and biochemical observations on the cell wall of the spore of Glomus epigaeum. Protoplasma 123:140–151

    Article  Google Scholar 

  • Cai CY, Ouyang S, Wang Y, Fang ZJ, Rong JY, Geng LY, Li XX (1996) An early Silurian vascular plant. Nature 379:592

    Article  CAS  Google Scholar 

  • Dotzler N, Krings M, Hass H, Walker C, Taylor TN, Agerer R (2009) Acaulosporoid glomeromycotan spores with germination shields from 400-million-year-old Rhynie chert. Mycol Prog 8:9–18

    Article  Google Scholar 

  • Erdmann N, Schiewer U (1984) Cell size changes as indicator of salt resistance of blue green algae. Arch Hydrobiol Suppl (Algol Stud) 67:431–439

    Google Scholar 

  • Gehrig H, Schüßler A, Kluge M (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43:71–81

    Article  PubMed  CAS  Google Scholar 

  • Grilli Caiola M (1992) Cyanobacteria in symbiosis with bryophytes and tracheophytes. In: Reisser W (ed) Algae and symbiosis: plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 231–253

    Google Scholar 

  • Hawksworth DL, Honegger R (1994) The lichen thallus: a symbiotic phenotype of nutritionally specialized fungi and its response to gall producers. In: Williams MAJ (ed) Plant galls. Organisms, interactions, populations, Systematics association, special vol 49. Clarendon, Oxford, pp 77–98

    Google Scholar 

  • Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A Versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823

    Article  PubMed  CAS  Google Scholar 

  • James TY, Kauff F, Schoch C, Matheny B, Hofstetter V, Cox C, Celio G, Guiedan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of the Fungi using a six-gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • Johansson C, Bergman B (1992) Early events during the establishment of the Gunnera/Nostoc symbiosis. Planta 188:403–413

    Article  Google Scholar 

  • Kluge M, Mollenhauer D, Mollenhauer R (1991) Photosynthetic carbon assimilation in Geosiphon pyriforme (Kützing) F.v. Wettstein, an endosymbiotic association of fungus and cyanobacterium. Planta 185:311–315

    Article  CAS  Google Scholar 

  • Kluge M, Mollenhauer D, Mollenhauer R, Kape R (1992) Geosiphon pyriforme, an endosymbiotic consortium of a fungus and a cyanobacterium (Nostoc), fixes nitrogen. Bot Acta 105:343–344

    CAS  Google Scholar 

  • Knapp E (1933) Über Geosiphon pyriforme Fr.v. Wettst., eine intrazelluläre Pilz-Algen-Symbiose. Ber Dtsch Bot Ges 51:210–217

    Google Scholar 

  • Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species-level. New Phytol 193:970–984

    Article  PubMed  Google Scholar 

  • Kuga Y, Saito K, Nayuki K, Peterson RL, Saito M (2008) Ultrastructure of rapidly frozen and freeze-substituted germ tubes of an arbuscular mycorrhizal fungus and localization of polyphosphate. New Phytol 178:189–200

    Article  PubMed  CAS  Google Scholar 

  • Ligrone R (1988) Ultrastructure of a fungal endophyte in Phaeoceros laevis (L.) Prosk. (Anthocerophyta). Bot Gaz 149:92–100

    Article  Google Scholar 

  • Ligrone R, Lopes C (1989) Cytology and development of a mycorrhiza-like infection in the gametophyte of Conocephalum conicum (L.) Dum. (Marchantiales, Hepatophyta). New Phytol 111:423–433

    Article  Google Scholar 

  • Long L, Yao Q, Ai Y, Deng M, Zhu H (2009) Detection of a novel bacterium associated with spores of the arbuscular mycorrhizal fungus Gigaspora margarita. Can J Microbiol 55:771–775

    Article  PubMed  CAS  Google Scholar 

  • Maetz M, Przybylowicz WJ, Mesjasz-Przybylowicz J, Schüßler A, Traxel K (1999a) Low dose nuclear microscopy as a necessity for accurate quantitative microanalysis of biological samples. Nucl Instrum Method B 158:292–298

    Article  CAS  Google Scholar 

  • Maetz M, Schüßler A, Wallianos A, Traxel K (1999b) Subcellular trace element distribution in Geosiphon pyriforme. Nucl Instrum Method B 150:200–207

    Article  CAS  Google Scholar 

  • Maia LC, Kimbrough JW, Erdos G (1993) Problems with fixation and embedding of arbuscular mycorrhizal fungi (Glomales). Mycologia 85:323–330

    Article  Google Scholar 

  • Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and evolutionary significance of mycorrhizal symbiosis in vascular plants (a review). Proc Natl Acad Sci USA 77:2113–2118

    Article  PubMed  CAS  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Mollenhauer D (1992) Geosiphon pyriforme. In: Reisser W (ed) Algae and symbiosis: plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 339–351

    Google Scholar 

  • Mollenhauer D, Mollenhauer R (1997) Endosymbiosis between Nostoc and Geosiphon pyriforme. Institut für den Wissenschaftlichen Film, Göttingen, Film C1955

    Google Scholar 

  • Mollenhauer D, Mollenhauer R, Kluge M (1996) Studies on initiation and development of the partner association in Geosiphon pyriforme (Kütz.) v. Wettstein, a unique endocytobiotic system of a fungus (Glomales) and the cyanobacterium Nostoc punctiforme (kütz.) Hariot. Protoplasma 193:3–9

    Article  Google Scholar 

  • Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders, Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of Glomaceae. Mycotaxon 37:471–491

    Google Scholar 

  • Naumann M, Schüßler A, Bonfante P (2010) The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME J 4:862–871

    Article  PubMed  Google Scholar 

  • Peterson RL, Howarth MJ, Whittier DP (1981) Interactions between a fungal endophyte and gametophyte cells in Psilotum nudum. Can J Bot 59:711–720

    Article  Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6:153–164

    Article  PubMed  CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in lower land plants. Philos Trans R Soc B 355:815–831

    Article  CAS  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000a) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  PubMed  CAS  Google Scholar 

  • Redecker D, Morton JB, Bruns TD (2000b) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14:276–284

    Article  PubMed  CAS  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    Article  PubMed  CAS  Google Scholar 

  • Rubinstein CV, Gerrienne P, De La Puente GS, Astini RA, Steemans P (2010) Early middle Ordovician evidence for land plants in Argentina (Eastern Gondwana). New Phytol 188:365–369

    Article  PubMed  CAS  Google Scholar 

  • Sawaki H, Sugawara K, Saito M (1999) Phylogenetic position of an arbuscular mycorrhizal fungus, Acaulospora gerdemannii, and its synanamorph Glomus leptotichum, based upon 18S rRNA gene sequence. Mycoscience 39:477–480

    Article  Google Scholar 

  • Scheloske S, Maetz M, Schüßler A (2001) Heavy metal uptake of Geosiphon pyriforme. Nucl Instrum Method B 181:659–663

    Article  CAS  Google Scholar 

  • Schmid E, Oberwinkler F (1993) Mycorrhiza-like interactions between the achlorophyllous gametophyte of Lycopodium clavatum L. and its fungal endophyte studied by light and electron microscopy. New Phytol 124:69–81

    Article  Google Scholar 

  • Schnepf E (1964) Zur Feinstruktur von Geosiphon pyriforme. Arch Mikrobiol 49:112–131

    Article  Google Scholar 

  • Schüßler A (1999) Glomales SSU rRNA gene diversity. New Phytol 144:205–207

    Article  Google Scholar 

  • Schüßler A (2000) Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10:15–20

    Article  Google Scholar 

  • Schüßler A (2002) Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75–83

    Article  Google Scholar 

  • Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. Arthur Schüßler, Christopher Walker, Gloucester. Published in libraries at the Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University; freely available online at www.amf-phylogeny.com

  • Schüßler A, Walker C (2011) Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In: Pöggeler S, Wöstemeyer J (eds) The Mycota XIV. Evolution of fungi and fungal-like organisms. Springer, Berlin, pp 163–185

    Chapter  Google Scholar 

  • Schüßler A, Wolf E (2005) Geosiphon pyriformis—a glomeromycotan soil fungus forming endosymbiosis with cyanobacteria. In: Declerck S, Strullu D-G, Fortin JA (eds) In vitro culture of mycorrhizas, vol 4, Soil Biology. Springer, Berlin, pp 271–289

    Chapter  Google Scholar 

  • Schüßler A, Mollenhauer D, Schnepf E, Kluge M (1994) Geosiphon pyriforme, an endosymbiotic association of fungus and cyanobacteria: the spore structure resembles that of arbuscular mycorrhizal (AM) fungi. Bot Acta 107:36–45

    Google Scholar 

  • Schüßler A, Schnepf E, Mollenhauer D, Kluge M (1995) The fungal bladders of the endocyanosis Geosiphon pyriforme, a Glomus-related fungus: cell wall permeability indicates a limiting pore radius of only 0.5 nm. Protoplasma 185:131–139

    Article  Google Scholar 

  • Schüßler A, Bonfante P, Schnepf E, Mollenhauer D, Kluge M (1996) Characterization of the Geosiphon pyriforme symbiosome by affinity techniques: confocal laser scanning microscopy (CLSM) and electron microscopy. Protoplasma 190:53–67

    Article  Google Scholar 

  • Schüßler A, Meyer T, Gehrig H, Kluge M (1997) Variations of lectin binding sites in extracellular glycoconjugates during the life cycle of Nostoc punctiforme, a potentially endosymbiotic cyanobacterium. Eur J Phycol 32:233–239

    Google Scholar 

  • Schüßler A, Gehrig H, Schwarzott D, Walker C (2001a) Analysis of partial Glomales SSU rRNA genes: implications for primer design and phylogeny. Mycol Res 105:5–15

    Article  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001b) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    Article  PubMed  Google Scholar 

  • Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2007) Arbuscular mycorrhiza – studies on the Geosiphon symbiosis lead to the characterization of the first glomeromycotan sugar transporter. Plant Signal Behav 2:431–434

    Article  PubMed  Google Scholar 

  • Schüßler A, Martin H, Cohen D, Wipf D (2008) The Geosiphon–Nostoc symbiosis as a tool to characterize symbiotic nutrient transporters in the arbuscular mycorrhiza symbiosis. In: Lorito M, Woo S, Scala F (eds) Biology of molecular plant–microbe interactions, vol 6. International Society for Molecular Plant–Microbe Interactions, St. Paul, pp 1–6, paper 24

    Google Scholar 

  • Schüßler A, Krüger M, Walker C (2011) Revealing natural relationships among arbuscular mycorrhizal fungi: culture line BEG47 represents Diversispora epigaea, not Glomus versiforme. PLoS One 6:e23333

    Article  PubMed  Google Scholar 

  • Schwarzott D, Walker C, Schüßler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is non-monophyletic. Mol Phylogenet Evol 21:190–197

    Article  PubMed  CAS  Google Scholar 

  • Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  • Smith SA, Beaulieu JM, Donoghue MJ (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Nat Acad Sci USA 107:5897–5902

    Article  PubMed  CAS  Google Scholar 

  • Stahl M (1949) Die Mycorrhiza der Lebermoose mit besonderer Berücksichtigung der thallösen Formen. Planta 37:103–148

    Article  Google Scholar 

  • von Wettstein F (1915) Geosiphon Fr. v. Wettst., eine neue, interessante siphonee. Österr Bot Z 65:145–156

    Article  Google Scholar 

  • Wolf E, Schüßler A (2005) Phycobiliprotein fluorescence of Nostoc punctiforme changes during the life cycle and chromatic adaptation: characterization by spectral confocal laser scanning microscopy and spectral unmixing. Plant Cell Environ 28:480–491

    Article  CAS  Google Scholar 

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  1. Genetics, Biocenter of the Ludwig-Maximilians-University Munich, Großhaderner Str. 2-4, 82152, Planegg-Martinsried, Germany

    A. Schüßler

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Correspondence to A. Schüßler .

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  1. Technical University of Munich, Alte Akademie 6, Freising, 85354, Bayern, Germany

    Bertold Hock

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Schüßler, A. (2012). 5 The Geosiphon–Nostoc Endosymbiosis and Its Role as a Model for Arbuscular Mycorrhiza Research. In: Hock, B. (eds) Fungal Associations. The Mycota, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30826-0_5

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