Journal of Plant Research

, Volume 122, Issue 5, pp 485–496 | Cite as

Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum

Regular Paper

Abstract

Many lineages of land plants (from lycopsids to angiosperms) have non-photosynthetic life cycle phases that involve obligate mycoheterotrophic arbuscular mycorrhizal (AM) associations where the plant host gains organic carbon through glomalean symbionts. Our goal was to isolate and phylogenetically identify the AM fungi associated with both the autotrophic and underground mycoheterotrophic life cycle phases of Psilotum nudum. Phylogenetic analyses recovered 11 fungal phylotypes in four diverse clades of Glomus A that form AM associations with P. nudum mycoheterotrophic gametophytes and autotrophic sporophytes, and angiosperm roots found in the same greenhouse pots. The correspondence of identities of AM symbionts in P. nudum sporophytes, gametophytes and neighboring angiosperms provides compelling evidence that photosynthetic heterospecific and conspecific plants can serve as the ultimate sources of fixed carbon for mycoheterotrophic gametophytes of P. nudum, and that the transfer of carbon occurs via shared fungal networks. Moreover, broader phylogenetic analyses suggest greenhouse Psilotum populations, like field-surveyed populations of mycoheterotrophic plants, form AM associations with restricted clades of Glomus A. The phylogenetic affinities and distribution of Glomus A symbionts indicate that P. nudum greenhouse populations have the potential to be exploited as an experimental system to further study the physiology, ecology and evolution of mycoheterotrophic AM associations.

Keywords

Arbuscular mycorrhizal associations Psilotum nudum Mycoheterotrophy Glomus 

Supplementary material

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Supplementary material 1 (PDF 576 kb)
10265_2009_234_MOESM2_ESM.doc (68 kb)
Supplementary material 2 (DOC 68.5 kb)
10265_2009_234_MOESM3_ESM.doc (120 kb)
Supplementary material 3 (DOC 119 kb)

References

  1. Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6:769–779CrossRefPubMedGoogle Scholar
  2. Antoniolli ZI, Schachtman DP, Ophel-Keller K, Smith SE (2000) Variation in rDNA its sequences in Glomus mosseae and Gigaspora margarita spores from a permanent pasture. Mycol Res 104:708–715CrossRefGoogle Scholar
  3. Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352CrossRefPubMedGoogle Scholar
  4. Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominquez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392CrossRefPubMedGoogle Scholar
  5. Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc Lond B Biol Sci 271:1799–1806CrossRefGoogle Scholar
  6. Bierhorst DW (1953) Structure and development of the gametophyte of Psilotum nudum. Am J Bot 40:649–658CrossRefGoogle Scholar
  7. Bierhorst DW (1954a) The gametangia and embryo of Psilotum nudum. Am J Bot 41:274–281CrossRefGoogle Scholar
  8. Bierhorst DW (1954b) The subterranean sporophytic axes of Psilotum nudum. Am J Bot 5:72–78Google Scholar
  9. Bierhorst DW (1955) A note on spore germination in Psilotum nudum. Va J Sci 6:96Google Scholar
  10. Bierhorst DW (1968) On the Stromatopteridaceae (fam nov.) and the Psilotaceae. Phytomorphology 18:232–268Google Scholar
  11. Bierhorst DW (1971) Morphology of vascular plants. Macmillan, New YorkGoogle Scholar
  12. Bierhorst DW (1977) Systematic position of Psilotum and Tmesipteris. Brittonia 29:3–13CrossRefGoogle Scholar
  13. Bower FO (1935) Primitive land plants: also known as the archegoniate. Hafner, New YorkGoogle Scholar
  14. Brundrett MC (2002) Tansley review no. 134. Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  15. Brundrett MC (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495CrossRefPubMedGoogle Scholar
  16. Carafa A, Duckett JG, Ligrone R (2003) Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbor a unique type of endophytic association with aseptate fungi. New Phytol 160:185–197CrossRefGoogle Scholar
  17. Carey EV, Marler MJ, Callaway RM (2004) Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol 172:133–141CrossRefGoogle Scholar
  18. Clapp JP, Young JPW, Merryweather JH, Fitter AH (1995) Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259–265CrossRefGoogle Scholar
  19. DeSalle R, Gilbert G, Wheeler W (2002) Techniques in molecular systematics and evolution. Birkhauser, BaselGoogle Scholar
  20. Dominguez L, Sersic A, Melville L, Peterson RL (2005) ‘Prepackaged symbioses’: propagules on roots of the myco-heterotrophic plant Arachnitis uniflora. New Phytol 169:191–198CrossRefGoogle Scholar
  21. Duckett JG, Ligrone R (1992) A light and electron-microscope study of the fungal endophytes in the sporophyte and gametophyte of Lycopodium-Cernuum with observations on the gametophyte sporophyte junction. Can J Bot 70:58–72CrossRefGoogle Scholar
  22. Duckett JG, Ligrone R (2005) A comparative cytological analysis of fungal endophytes in the sporophyte rhizomes and vascularized gametophytes of Tmesipteris and Psilotum. Can J Bot 83:1443–1456CrossRefGoogle Scholar
  23. Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12:406–412CrossRefGoogle Scholar
  24. Franke T, Beenken L, Doring M, Kocyan A, Agerer R (2006) Arbuscular mycorrhizal fungi of the Glomus-group A lineage (Glomerales; Glomeromycota) detected in myco-heterotrophic plants from tropical Africa. Mycol Prog 5:24–31CrossRefGoogle Scholar
  25. Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117CrossRefPubMedGoogle Scholar
  26. Harrier LA (2001) The arbuscular mycorrhizal symbiosis: a molecular review of the fungal dimension. J Exp Bot 52:469–478PubMedGoogle Scholar
  27. Harrison M (1998) Development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 1:360–365CrossRefPubMedGoogle Scholar
  28. Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol 50:361–389CrossRefGoogle Scholar
  29. Hauk WD, Parks CR, Chase MW (2003) Phylogenetic studies of Ophioglossaceae: evidence from rbcl and trnL-F plastid DNA sequences and morphology. Mol Phylogenet Evol 28:131–151CrossRefPubMedGoogle Scholar
  30. Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196CrossRefPubMedGoogle Scholar
  31. Helgason T, Fitter AH (2005) The ecology and evolution of the arbuscular mycorrhizal fungi. Mycologist 19:96–101CrossRefGoogle Scholar
  32. Hijri I, Sykorova Z, Oehl F, Ineichen K, Mader P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289CrossRefPubMedGoogle Scholar
  33. Holloway JE (1918) The prothallus and young plant of Tmesipteris. Trans Proc N Z Inst 50:1–44Google Scholar
  34. Holloway JE (1939) The gametophyte, embryo, and young rhizome of Psilotum triquetrum swartz. Ann Bot 53:313–319Google Scholar
  35. Huelsenbeck JF, Ronquist J (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754CrossRefPubMedGoogle Scholar
  36. Imhof S (1999a) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39CrossRefGoogle Scholar
  37. Imhof S (1999b) Subterranean structures and mycorrhiza of the achlorophyllous Burmannia tenella (Burmanniaceae). Can J Bot 77:637–643CrossRefGoogle Scholar
  38. Imhof S (2004) Morphology and development of the subterranean organs of the achlorophyllous Sciaphila polygyna (Triuridaceae). Bot J Linn Soc 146:295–301CrossRefGoogle Scholar
  39. Jansa JA, Mozafar S, Banke B, McDonald A, Frossard E (2002) Intra- and intersporal diversity of its rDNA sequences in Glomus intraradices assessed by cloning and sequencing, and by SSCP analysis. Mycol Res 106:670–681CrossRefGoogle Scholar
  40. Kaplan DR (1977) Morphological status of shoot systems of Psilotaceae. Brittonia 29:30–53CrossRefGoogle Scholar
  41. Kjoller R, Rosendahl S (2001) Molecular diversity of glomalean (arbuscular mycorrhizal) fungi determined as distinct Glomus specific DNA sequences from roots of field grown peas. Mycol Res 105:1027–1032CrossRefGoogle Scholar
  42. Kovacs GM, Balazs T, Penzes Z (2007) Molecular study of arbuscular mycorrhizal fungi colonizing the sporophyte of the eusporangiate rattlesnake fern (Botrychium virginianum,Ophiogloassaceae). Mycorrhiza 17:597–605CrossRefPubMedGoogle Scholar
  43. Leake JR (1993) Tansley review no. 69. The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216CrossRefGoogle Scholar
  44. Leake JR (2004) Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr Opin Plant Biol 7:302–308CrossRefGoogle Scholar
  45. Leake JR, Cameron DD, Beerling DJ (2008) Fungal fidelity in the myco-heterotroph-to-autotroph life cycle of Lycopodiaceae: a case of parental nurture? New Phytol 177:572–576CrossRefPubMedGoogle Scholar
  46. Ligrone R, Carafa A, Lumni E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94:1756–1777CrossRefGoogle Scholar
  47. Opik M, Moora M, Liira J, Koljalg U, Zobel M, Sen R (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal Scots pine forest and grassland soils. New Phytol 160:581–593CrossRefGoogle Scholar
  48. Opik M, Moora M, Liira J, Zoebel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790CrossRefGoogle Scholar
  49. Peterson RL, Howarth MJ, Whittier DP (1981) Interactions between a fungal endophyte and gametophyte cells in Psilotum-Nudum. Can J Bot 59:711–720CrossRefGoogle Scholar
  50. Pfeffer PE, Douds DD, Bucking H, Schwartz DP, Shachar-Hill Y (2004) The fungus does not transfer carbon to or between roots in an arbuscular mycorrhizal symbiosis. New Phytol 163:617–627CrossRefGoogle Scholar
  51. Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf P, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–621CrossRefPubMedGoogle Scholar
  52. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598CrossRefGoogle Scholar
  53. Read DJ (1998) Plants on the web. Nature 396:22–23CrossRefGoogle Scholar
  54. Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B Biol Sci 355:815–831CrossRefPubMedGoogle Scholar
  55. Redecker DH, Raab P (2006) Phylogeny of the Glomeromycota (arbuscular mycorrhizal fungi): recent developments and new markers. Mycologia 98:885–895CrossRefPubMedGoogle Scholar
  56. Rosendahl S, Stukenbrock EH (2004) Community structure of arbuscular mycorrhizal fungi in undisturbed vegetation revealed by analyses of LSU rDNA sequences. Mol Ecol 13:3179–3186CrossRefPubMedGoogle Scholar
  57. Russell J, Bulman S (2005) The liverwort Marchantia foliacea forms specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165:567–579CrossRefPubMedGoogle Scholar
  58. Schmid E, Oberwinkler F (1994) Light and electron-microscopy of the host- fungus interaction in the achlorophyllous gametophyte of Botrychium lunaria. Can J Bot 72:182–188CrossRefGoogle Scholar
  59. Schmid E, Oberwinkler F (1996) Light and electron microscopy of a distinctive VA mycorrhiza in mature sporophytes of Ophioglossum reticulatum. Mycol Res 100:843–849CrossRefGoogle Scholar
  60. Schussler AH, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1301–1413Google Scholar
  61. Schwarzott D, Schussler A (2001) A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza 10:203–207CrossRefGoogle Scholar
  62. Schwarzott D, Walker C, Schussler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol Phylogenet Evol 21:190–197CrossRefPubMedGoogle Scholar
  63. Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582CrossRefGoogle Scholar
  64. Simon L, Lalonde M, Bruns T (1992) Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295PubMedGoogle Scholar
  65. Simon L, Levesque RC, Lalonde M (1993) Identification of endomycorrhizal fungi colonizing roots by fluorescent single-strand conformation polymorphism-polymerase chain reaction. Appl Environ Microbiol 59:3011–3015Google Scholar
  66. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San DiegoGoogle Scholar
  67. Smith FA, Smith SE (1997) Tansley review no. 96. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388CrossRefGoogle Scholar
  68. Smith FA, Smith SE (1996) Mutualism and parasitism: diversity in function and structure in the ''arbuscular'' (VA) mycorrhizal symbiosis. Adv Bot Res 22:1–43CrossRefGoogle Scholar
  69. Swofford DL (2002) Paup*: phylogenetic analysis using parsimony. Sinauer, SunderlandGoogle Scholar
  70. Takiguchi Y, Imaichi R, Kato M (1997) Cell division patterns in the apices of subterranean axis and aerial shoot of Psilotum nudum (Psilotaceae): morphological and phylogenetic implications for the subterranean axis. Am J Bot 84:588–596CrossRefGoogle Scholar
  71. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  72. Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564CrossRefPubMedGoogle Scholar
  73. Walker C, Schussler A (2004) Nomenclatural clarifications and new taxa in the Glomeromycota. Mycol Res 108:981–982CrossRefGoogle Scholar
  74. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefPubMedGoogle Scholar
  75. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sminsk JJ, White TJ (eds) PCR protocols, a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  76. Whittier DP (1973) Germination of Psilotum spores in axenic culture. Can J Bot 51:2000–2001CrossRefGoogle Scholar
  77. Whittier DP (1985) Spore germination in Psilotum. Proc R Soc Edinburgh 86:465–466Google Scholar
  78. Whittier DP (1988) Dark-grown Psilotum. Am Fern J 78:109–116CrossRefGoogle Scholar
  79. Whittier DP (1990) Effects of nitrogen-source on spore germination and gametophyte growth in Psilotum. Bot Gaz 151:50–53CrossRefGoogle Scholar
  80. Whittier DP, Braggins JE (1994) Spore germination in the Psilotaceae. Can J Bot 72:688–692CrossRefGoogle Scholar
  81. Whittier DP, Given JE (1987) The germination of Tmesipteris spores. Can J Bot 65:1770–1772CrossRefGoogle Scholar
  82. Whittier DP, Peterson RL (1980) Archegonial opening in Psilotum. Can J Bot 58:1905–1907Google Scholar
  83. Winther JL, Friedman WE (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255CrossRefGoogle Scholar
  84. Winther JL, Friedman WE (2008) Arbuscular mycorrhizal symbionts in Lycopodiaceae. New Phytol 177:790–801CrossRefPubMedGoogle Scholar
  85. Wu BY, Nara K, Hogetsu T (2001) Can C-14-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol 149:137–146CrossRefGoogle Scholar
  86. Wu BY, Nara K, Hogetsu T (2002) Spatiotemporal transfer of carbon-14-labelled photosynthate from ectomycorrhizal Pinus densiflora seedlings to extraradical mycelia. Mycorrhiza 12:83–88CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2009

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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