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Phylogenetic distribution and evolution of mycorrhizas in land plants

Abstract

A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants. A plant phylogeny was then used to map the mycorrhizal information to examine evolutionary patterns. Several findings from this survey enhance our understanding of the roles of mycorrhizas in the origin and subsequent diversification of land plants. First, 80 and 92% of surveyed land plant species and families are mycorrhizal. Second, arbuscular mycorrhiza (AM) is the predominant and ancestral type of mycorrhiza in land plants. Its occurrence in a vast majority of land plants and early-diverging lineages of liverworts suggests that the origin of AM probably coincided with the origin of land plants. Third, ectomycorrhiza (ECM) and its derived types independently evolved from AM many times through parallel evolution. Coevolution between plant and fungal partners in ECM and its derived types has probably contributed to diversification of both plant hosts and fungal symbionts. Fourth, mycoheterotrophy and loss of the mycorrhizal condition also evolved many times independently in land plants through parallel evolution.

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References

  • Ane JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Levy J, Debelle F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Denarie J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    PubMed  Article  CAS  Google Scholar 

  • Baylis GTS (1970) Root hairs and phycomycetous mycorrhizas in phosphorus-deficient soil. Plant Soil 33:713–716

    Article  Google Scholar 

  • Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352

    PubMed  Article  Google Scholar 

  • Bidartondo MI, Bruns TD (2002) Fine-level mycorrhizal specificity in the Monotropoideae (Ericaceae): specificity for fungal species groups. Mol Ecol 11:557–569

    PubMed  Article  CAS  Google Scholar 

  • Bidartondo MI, Bruns TD, Weiß M, Sergio C, Read DJ (2003) Specialized cheating of the ectomycorrhizal symbiosis by an epiparasitic liverwort. Proc R Soc Lond B 270:835–842

    Article  Google Scholar 

  • 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 271:1799–1806

    Article  CAS  Google Scholar 

  • Boullard B (1988) Observations on the coevolution of fungi and hepatics. In: Pirozynski KA, Hawksworth DL (eds) Coevolution of fungi with plants and animals. Academic, London, pp 107–124

    Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • Bruns TD, Shefferson RP (2004) Evolutionary studies of ectomycorrhizal fungi: recent advances and future directions. Can J Bot 82:1122–1132

    Article  CAS  Google Scholar 

  • Cameron KM, Chase MW, Whitten WM, Kores PJ, Jarrell DC, Albert VA, Yukawa T, Hills HG, Goldman DH (1999) A phylogenetic analysis of the Orchidaceae: evidence from rbcL nucleotide sequences. Am J Bot 86:208–224

    Article  Google Scholar 

  • Carafa A, Duckett JG, Ligrone R (2003) Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytol 160:185–197

    Article  Google Scholar 

  • Cronquist A (ed) (1981) An integrated system of classification of flowing plants. Columbia Univ Press, New York

    Google Scholar 

  • Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol 163:381–392

    Article  CAS  Google Scholar 

  • Dombrovska O, Qiu Y-L (2004) Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol Phylogenet Evol 32:246–263

    PubMed  Article  CAS  Google Scholar 

  • Duckett JG, Renzaglia KS, Pell K (1991) A light and electron microscope study of rhizoid–ascomycete associations and flagelliform axes in British hepatics with observations on the effects of the fungi on host morphology. New Phytol 118:233–257

    Article  Google Scholar 

  • Fitter AH, Moyersoen B (1996) Evolutionary trends in root–microbe symbioses. Philos Trans R Soc Lond B 351:1367–1375

    Article  Google Scholar 

  • Gao C (2000) Takakiaceae. In: Yunnanica F (ed) Kunming Institute of Botany, Chinese Academy of Sciences , vol. 17, Bryophyta: Hepaticae, Anthocerotae. Science, Beijing, pp 1–2

    Google Scholar 

  • Gemma JN, Koske RE, Flynn T (1992) Mycorrhizae in Hawaiian pteridophytes: occurrence and evolutionary significance. Am J Bot 79:843–852

    Article  Google Scholar 

  • Grolle R (1983) Nomina generica Hepaticarum; references, types and synonymies. Acta Bot Fenn 121:1–62

    Google Scholar 

  • Groth-Malonek M, Pruchner D, Grewe F, Knoop V (2005) Ancestors of trans-spliced mitochondrial introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol Biol Evol 22:117–125

    PubMed  Article  CAS  Google Scholar 

  • Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102

    Article  Google Scholar 

  • Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389

    PubMed  Article  CAS  Google Scholar 

  • Hibbett DS, Gilbert L-B, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbiosis in basidiomycetes. Nature 407:506–508

    PubMed  Article  CAS  Google Scholar 

  • Hickey LJ, Doyle JA (1977) Early Cretaceous fossil evidence for angiosperm evolution. Bot Rev 43:3–104

    Article  Google Scholar 

  • Horton TR, Bruns TD (1998) Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata). New Phytol 139:331–339

    Article  Google Scholar 

  • Kenrick P, Crane PR (1997) The origin and early diversification of land plants: a cladistic study. Smithsonian Institution, Washington DC

    Google Scholar 

  • Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386

    Article  CAS  Google Scholar 

  • Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163

    PubMed  Article  Google Scholar 

  • Kerp H, Trewin NH, Hass H (2004) New gametophytes from the Early Devonian Rhynie chert. Trans R Soc Edinb Earth Sci 94:411–428

    Google Scholar 

  • Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • Leake JR (1994) The biology of mycoheterotrophic (‘saprophytic’) plants. New Phytol 127:171–216

    Article  Google Scholar 

  • LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil ectomycorrhizae from the Middle Eocene. Am J Bot 84:410–412

    Article  Google Scholar 

  • Le Quere A, Schutzendubel A, Rajashekar B, Canback B, Hedh J, Erland S, Johansson T, Tunlid A (2004) Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus. Mol Ecol 13:3809–3819

    PubMed  Article  CAS  Google Scholar 

  • Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Ligrone R, Pocock K, Duckett JG (1993) A comparative ultrastructural study of endophytic basidiomycetes in the parasitic achlorophyllous hepatic Cryptothallus mirabilis and the closely allied photosynthetic species Aneura pinguis (Metzgeriales). Can J Bot 71:666–679

    Article  Google Scholar 

  • Liu JY, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123

    PubMed  Article  CAS  Google Scholar 

  • Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Hambleton S, Crockett M, Shoemaker R, Sung GH, Lucking R, Lumbsch T, O'Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim YW, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R (2004) Assembling the fungal tree of life: progress, classification and evolution of subcellular traits. Am J Bot 91:1446–1480

    Article  Google Scholar 

  • Mabberley DJ (1987) The plant-book—a portable dictionary of the higher plants. Cambridge Univ Press, Cambridge

    Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community–ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning. Chapman & Hall, London, pp 357–423

    Google Scholar 

  • Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751

    Article  Google Scholar 

  • Newton AC, Haigh JM (1998) Diversity of ectomycorrhizal fungi in Britain: a test of the species–area relationship, and the role of host specificity. New Phytol 138:619–627

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Pocock K, Duckett JG (1985) On the occurrence of branched and swollen rhizoids in British hepatics: their relationships with the substratum and associations with fungi. New Phytol 99:281–304

    Article  Google Scholar 

  • Qiu Y-L, Cho Y, Cox JC, Palmer JD (1998) The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671–674

    PubMed  Article  CAS  Google Scholar 

  • Qiu Y-L, Lee J (2000) Transition to a land flora: a molecular phylogenetic perspective. J Phycol 36:799–802

    Article  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 Lond B 355:815–831

    Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Renzaglia KS, Duff RJ, Nickrent DL, Garbary DJ (2000) Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philos Trans R Soc Lond B 355:769–793

    Article  CAS  Google Scholar 

  • Russell J, Bulman S (2005) The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165:567–579

    PubMed  Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microb Ecol 47:416–426

    PubMed  Article  CAS  Google Scholar 

  • Selosse MA, Le Tacon F (1998) The land flora: a phototroph–fungus partnership? Trends Ecol Evol 13:15–20

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San Diego

    Google Scholar 

  • Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461

    Google Scholar 

  • Stevens PF (2004) Angiosperm phylogeny website. Version 5. http://www.mobot.org/MOBOT/research/APweb/. Cited May 2004

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962

    PubMed  Article  CAS  Google Scholar 

  • Stubblefield SP, Taylor TN, Trappe JM (1987) Vesicular–arbuscular mycorrhizae from the Triassic of Antarctica. Am J Bot 74:1904–1911

    Article  Google Scholar 

  • Taylor TN, Hass H, Remy W (1992) Devonian fungi: interactions with the green alga Paleonitella. Mycologia 84:901–910

    Article  Google Scholar 

  • Taylor TN, Hass H, Kerp H (1999) The oldest fossil ascomycetes. Nature 399:648

    PubMed  Article  CAS  Google Scholar 

  • Taylor TN, Kerp H, Hass H (2005) Life history biology of early land plants: deciphering the gametophyte phase. Proc Natl Acad Sci U S A 102:5892–5897

    PubMed  Article  CAS  Google Scholar 

  • Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC, Boca Raton, pp 5–25

    Google Scholar 

  • Trappe JM (1996) What is a mycorrhiza? In: Azcon-Aguilar C, Barrea J-M (eds) Mycorrhiza in integrated systems–from genes to plant development. Proceedings of the 4th European Symposium on Mycorrhizae, EC Report EUR 16728, Luxembourg, pp 3–6

  • Wellman CH, Osterloff PL, Mohiuddin U (2003) Nature 425:282–285

    PubMed  Article  CAS  Google Scholar 

  • Zhao Z-W (2000) The arbuscular mycorrhizas of pteridophytes in Yunnan, southwest China: evolutionary interpretations. Mycorrhiza 10:145–149

    Article  Google Scholar 

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Acknowledgements

We would like to thank Rong-rong Xu for helping with figure preparation, Malini Jane Sridharan for critically reading the manuscript, and Jim Trappe and two reviewers for their insightful comments. This work was supported by an Early Career Award (DEB 0332298) and ATOL grants (DEB 0431239, DEB 0531689) from NSF to Y-L Qiu.

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Correspondence to Y.-L. Qiu.

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Wang, B., Qiu, YL. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006). https://doi.org/10.1007/s00572-005-0033-6

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  • DOI: https://doi.org/10.1007/s00572-005-0033-6

Keywords

  • Mycorrhizas
  • Land plants
  • Fungi
  • Parallel evolution