Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: Novel insights into ancestral plant-fungus symbioses

New Phytologist

Volumn 203, Issue 3, 2014, Pages 964-979

  Strullu Derrien, Christine ^a,c   Kenrick, Paul ^a   Pressel, Silvia ^a   Duckett, Jeffrey G ^a   Rioult, Jean Philippe ^b   Strullu, Désiré Georges ^c  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^b UNIVERSITÉ DE CAEN   (France)

^c UNIVERSITÉ D'ANGERS   (France)

Author keywords

Devonian; Endophytes; Glomeromycota; Horneophyton lignieri; Mucoromycotina; Palaeoendogone gwynne vaughaniae; Palaeoglomus boullardii; Symbioses

Indexed keywords

COEXISTENCE; COLONIZATION; DEVONIAN; ENDOPHYTE; FUNGUS; SPECIES DIVERSITY; SYMBIOSIS; TERRESTRIAL ECOSYSTEM;

SCOTLAND; UNITED KINGDOM;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; FUNGI; GLOMEROMYCOTA; HORNEOPHYTON; HORNEOPHYTON LIGNIERI;

EMBRYOPHYTA; ENDOPHYTE; FUNGUS; GLOMEROMYCOTA; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SPECIES EXTINCTION; SYMBIOSIS; TIME; UNITED KINGDOM;

EMBRYOPHYTA; ENDOPHYTES; EXTINCTION, BIOLOGICAL; FUNGI; GLOMEROMYCOTA; PHYLOGENY; SCOTLAND; SYMBIOSIS; TIME FACTORS;

EID: 84904041502     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12805     Document Type: Article

References (74)

1. Andrade ACS, Queiroz MH, Hermes RAL, Oliveira VL. 2000. Mycorrhizal status of some plants of the Araucaria forest and the Atlantic rainforest in Santa Catarina, Brazil. Mycorrhiza 10: 131-136.
2. Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG. 2011. The dawn of symbiosis between plants and fungi. Biology Letters 7: 574-577.
3. Bonfante P, Genre A. 2008. Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science 13: 492-498.
4. Boullard B. 1957. La mycotrophie chez les ptéridophytes; sa fréquence, ses caractères, sa signification. Botaniste 41: 1-185.
5. Boullard B, Lemoigne Y. 1971. Les champignons endophytes du Rhynia gwynne-vaughanii K. & L. Étude morphologique et déductions sur leur biologie. Botaniste 54: 49-89.
6. Bruchmann H. 1898. Uber die prothallien und die keimpflanzen mehrerer europaischer Lycopodien, und zwar über die von Lycopodium clavatum, L.annotinum, L.complanatum und L.Selago. Gotha, Germany: F.A. Perthes.
7. Burgeff H. 1938. Mycorrhiza. In: Verdoorn F, ed. Manual of pteridology. The Hague, the Netherlands: Martinus Nijhoff, 159-191.
8. Carafa A, Duckett JG, Ligrone, 2003. Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytologist 160: 185-197.
9. Channing A, Edwards D. 2013. Wetland megabias: ecological and ecophysiological filtering dominâtes the fossil record of hot spring flora. Palaeontology 56: 523-526.
10. Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G. 2004. MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology 50: 19-22.
11. Desirò A, Duckett JG, Pressel S, Villareal JC, Bidartondo M. 2013. Fungal symbiose in hornworts: a chequerel history. Proceedings of the Royal Society B 280(1759): 2010207.
12. Duckett JG, Carafa A, Ligrone R. 2006. A highly differentiated glomeromycotean association with the mucilage-secreting, primitive antipodean liverwort Treubia (Treubiaceae): clues to the origins of mycorrhizas. American Journal of Botany 93: 797-813.
13. 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 of the gametophyte-sporophyte junction. Canadian Journal of Botany 70: 58-72.
14. Duckett JG, Ligrone R. 2005. A comparative cytological analysis of fungal endophytes in the sporophyte rhizomes and vascularized gametophytes of Tmesipteris and Psilotum. Canadian Journal of Botany 83: 1443-1456.
15. Duckett JG, Russell AJ, Ligrone R. 1996. Trichomes in the Hymenophyllaceae. In: Camus JM, Gibby M, Johns RJ, eds. Pteridology in perspective. Kew, UK: Royal Botanic Gardens, 511-514.
16. Fayers SR, Trewin NH. 2004. A review of the palaeoenvironments and biota of the Windyfield Chert. Transactions of the Royal Society of Edinburgh: Earth Sciences 94: 325-339.
17. Fonseca HMAC, Berbara RLL, Ferreira ML. 2006. Lunularia cruciata, a potential in vitro host for Glomus proliferum and Glomus intraradices. Mycorrhiza 16: 503-508.
18. Goebel K. 1891. Morphologische und biologische Studien, IV. Uber Javanische Lebermoose. I. Treubia. Annales du Jardin Botanique de Buitenzorg 9: 1-10.
19. Harper CJ, Taylor TN, Krings M, Taylor EL. 2013. Mycorrhizal symbiosis in the Paleozoic seed fern Glossopteris from Antarctica. Review of Palaeobotany and Palynology 192: 22-31.
20. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Stalpers JA etal. 2007. A higher-level phylogenetic classification of the Fungi. Mycological Research 111: 509-547.
21. Horn K, Francke T, Unterseher M, Schnittler M, Beenken L. 2013. Morphological and molecular analyses of fungal endophytes of achlorophyllose gametophytes of Diphasiastrum alpinum (Lycopodiaceae). American Journal of Botany 100: 2158-2174.
22. Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, Beerling D. 2010. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nature Communications 1: 103.
23. James YT, Kauff K, Scoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J etal. 2006. Reconstructing the early evolution of Fungi using a six gene phylogeny. Nature 443: 818-822.
24. Karatygin IV, Snigirevskaya NS, Demchenko KN. 2006. Species of the genus Glomites as plant symbionts in Early Devonian ecosystems. Paleontological Journal 40: 572-579.
25. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A etal. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
26. Kottke I, Nebel M. 2005. The evolution of mycorrhiza-like associations in liveworts: an update. New Phytologist 167: 330-334.
27. Kovács GM, Balǎzs T, Pénzes Z. 2007. Molecular study of arbuscular mycorrhizal fungi colonizing the sporophyte of the eusporangiate rattlesnake fern (Botrychium virginianum, Ophioglossaceae). Mycorrhiza 17: 597-605.
28. Kovács GM, Kottke I, Oberwinkler F. 2003. Light and electron microscopy study of the mycorrhizae of sporophytes of Botrychium virginianum - arbuscular-like structure resembling fossil forms. Plant Biology 5: 574-580.
29. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ. 2007a. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist 174: 648-657.
30. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ. 2007b. An alternative mode of early land plant colonization by putative endomycorrhizal fungi. Plant Signaling and Behaviour 2: 125-126.
31. Lang WH. 1899. The prothallus of Lycopodium clavatum. Annals of Botany 13: 279-318.
32. Ligrone L, Carafa A, Lumini E, Bianciotto V, Bonfane P, Duckett JG. 2007. Glomeromycota associations in liverworts: a molecular, cellular, and taxonomic analysis. American Journal of Botany 94: 1756-1777.
33. Ligrone L, Lopes C. 1989. Cytology and development of mycorrhiza-like infection in the gametophyte of Conocephalum conicum (L.) Dum. (Marchantiales, Hepatophyta). New Phytologist 111: 423-433.
34. Ligrone R. 1988. Ultrastructure of a fungal endophyte in Phaeoceros laevis (L.) Prosk. (Anthocerotophyta). Botanical Gazette 149: 92-100.
35. Ligrone R, Duckett JG. 1994. Thallus differentiation in the marchantialean liverwort Asterella wilmsii (Steph.) with particular reference to longitudinal arrays of endoplasmic microtubules in the inner cells. Annals of Botany 73: 577-586.
36. Mark DF, Rice CM, Trewin NH. 2013. Discussion on 'a High-precision U-Pb age constraint on the Rhynie chert Konservat-Lagerstätte: time scale and other implications'. Journal of the Geological Society 170: 701-703.
37. Nebel M, Kreier HP, Preussung M, Weiss M. 2004. Symbiotical fungal associations of liveworts are the possible ancestors of mycorrhizae. In: Agerer R, Piepenpenbring M, Blanz P, eds. Frontiers in basidiomycote mycology. Ecking, Germany: HIW Verlag, 339-360.
38. Ogura-Tsujita Y, Sakoda A, Ebihara A, Yukawa T, Imaichi R. 2013. Arbuscular mycorrhiza formation in cordate gametophyes of two ferns, Angiopteris lygodiifolia and Osmunda japonica. Journal of Plant Research 126: 41-50.
39. Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Review Microbiology 10: 763-775.
40. Phipps CJ, Taylor TN. 1996. Mixed arbuscular mycorrhizae from the Triassic of Antarctica. Mycologia 88: 707-714.
41. Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Biosystems 6: 153-164.
42. Pressel S, Bidartondo MI, Ligrone R, Duckett JG. 2010. Fungal symbioses in bryophytes: new insights into the twenty-first century. Phytotaxa 9: 238-253.
43. Read DJ, Duckett JG, Francis R, Ligrone R, Russell A. 2000. Symbiotic fungal associations in 'lower' land plants. Philosophical Transactions of the Royal Society B 355: 815-831.
44. Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovician. Science 289: 1920-1921.
45. Redecker D, Kodner R, Graham LE. 2002. Palaeoglomus grayi from the Ordovician. Mycotaxon 84: 33-37.
46. Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences, USA 91: 11841-11843.
47. Rice CM, Trewin NH, Anderson LI. 2002. Geological setting of the Early Devonian Rhynie cherts, Aberdeenshire, Scotland: an early terrestrial hot spring system. Journal of the Geological Society 159: 203-214.
48. Robert V, Stegehuis G, Stalpers J. 2005. The MycoBank engine and related databases. [WWW document] URL http://www.mycobank.org [accessed].
49. Russell J, Bulman S. 2005. The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytologist 165: 567-579.
50. Schmid E, Oberwinkler F. 1993. Mycorrhiza-like interaction between the achlorophyllus gametophyte of Lycopodium clavatum L. and its fungal endophye studied by light and electron microscopy. New Phytologist 124: 69-81.
51. Schmid E, Oberwinkler F. 1994. Light and electron microscopy of the host-fungus interaction in the achlorophyllous gametophyte of Botrychium lunaria. Canadian Journal of Botany 72: 182-188.
52. Schmid E, Oberwinkler F. 1995. A light- and electron-microsocpe study on a vesicular-arbuscular host-fungus interaction in gametophytes and young sporophytes of the Gleicheniacae (Filicales). New Phytologist 129: 317-324.
53. Schmid E, Oberwinkler F. 1996. Light and electron microscopy of a distinctive VA mycorrhiza in mature sporophytes of Ophioglossum reticulatum. Mycological Research 100: 843-849.
54. Schüßler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
55. Selosse M, Le Tacon F. 1998. The land flora: a phototrophfungus partnership? Trends in Ecology and Evolution 13: 15-20.
56. Selosse MA, Rousset F. 2011. The plant-fungal marketplace. Science 333: 828-829.
57. Simon L. 1996. Phylogeny of the Glomales: deciphering the past to understand the present. New Phytologist 133: 95-101.
58. Simon L, Bousquet J, Lévesque C, Lalonde M. 1993. Origin and diversification of endomycorrhizal fungi with vascular plants. Nature 363: 67-69.
59. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Cambridge, UK: Academic Press.
60. Strullu DG. 1985. Les mycorhizes, Handbuch der Pflanzenanatomie. Berlin, Germany: Gebrüder Borntraeger.
61. Strullu DG, Gourret JP, Garrec JP. 1981. Microanalyse des granules vacuolaires des ectomycorhizes, endomycorhizes et endomycothalles. Physiologie Végétale 19: 367-378.
62. Strullu-Derrien C, Rioult JP, Strullu DG. 2009. Mycorrhizas in Upper Carboniferous Radiculites-type Cordaitalean rootlets. New Phytologist 182: 561-564.
63. Strullu-Derrien C, Strullu DG. 2007. Mycorrhization of fossil and living plants. Comptes Rendus Palevol 6-7: 483-494.
64. Taylor TN, Kerp H, Hass H. 2005. Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences, USA 102: 5892-5897.
65. Taylor TN, Klavins SD, Krings M, Taylor EL, Kerp H, Hass H. 2004. Fungi from the Rhynie Chert: a view from the dark side. Transactions of the Royal Society of Edinburgh: Earth Sciences 94: 457-473.
66. Taylor TN, Krings M, Dotzler N, Galtier J. 2011. The advantage of thin-section preparations over acetate peels in the study of Late Paleozoic fungi and other microorganisms. Palaios 26: 239-244.
67. Taylor TN, Remy W, Hass H, Kerp H. 1995. Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87: 560-573.
68. Trappe JM. 1982. Synoptic keys to the genera and species of zygomycetous (vesicular-arbuscular) mycorrhizal fungi. Phytopathology 72: 1102-1108.
69. Trewin NH. 1994. Depositional environment and preservation of biota in the Lower Devonian hot-springs of Rhynie, Aberdeenshire, Scotland. Transactions of the Royal Society of Edinburgh: Earth Sciences 84: 433-442.
70. Trewin NH, Rice CM. 2004. The Rhynie hot-spring system. Geology, biota and mineralisation. Proceedings of the Conference held in 2003. Transactions of the Royal Society of Edinburgh: Earth Sciences 94.
71. Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.
72. Winther JL, Friedman WE. 2007a. Asrbuscular mycorrhizal associations in Lycopodiaceae. New Phytologist 177: 790-801.
73. Winther JL, Friedman WE. 2007b. Arbuscular mychorrhizal symbionts in Botrychium (Ophioglossaceae). American Journal of Botany 94: 1248-1255.
74. Winther JL, Friedman WE. 2009. Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. Journal of Plant Research 122: 485-496.