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The Physiological Ecology of Mycoheterotrophy

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Mycoheterotrophy

Abstract

The purpose of this chapter is to provide a practical and theoretical framework for the study of the ecophysiology of mycoheterotrophic plants. We accomplish this by providing a comparative overview of our current knowledge on carbon and nitrogen isotope natural abundance in partially and fully mycoheterotrophic plants associated with ectomycorrhizal, wood- and litter-decomposer saprotrophic, and arbuscular mycorrhizal fungi, and discuss their ecophysiological implications. We present a meta-analysis of all stable carbon and nitrogen isotope values from the majority of species of partially and fully mycoheterotrophic plants investigated thus far. We summarize our current understanding of the ecophysiology of fully mycoheterotrophic plants in the families Orchidaceae and Ericaceae as well as nonvascular plants, and species from the tropics that associate with arbuscular mycorrhizal fungi. We also review the occurrence of initial mycoheterotrophy among orchids and ericaceous plants that are autotrophic upon reaching adulthood. We highlight current studies of cryptic or partial mycoheterotrophy in green plants that appear to be fully autotrophic, but meet some portion of their C demands via fungi in a mixotrophic nutrition. Furthermore, we explore the utility of ecophysiological methods such as radioactive and stable isotope probing, measuring plant assimilatory and respiratory responses to environmental gradients such as light availability, and natural abundance stable isotope analysis for future studies of mycoheterotrophic food webs. Finally, methodological limitations and considerations for the study of physiological ecology of mycoheterotrophy are also outlined in this chapter.

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References

  • Abadie J-C, Püttsepp Ü, Gebauer G, Faccio A, Bonfante P, Selosse M-A (2006) Cephalanthera longifolia (Neottieae, Orchidaceae) is mixotrophic: a comparative study between green and non-photosynthetic individuals. Can J Bot 84:1462–1477

    Article  CAS  Google Scholar 

  • Adamec L (1997) Mineral nutrition of carnivorous plants: a review. Bot Rev 63:273–299

    Article  Google Scholar 

  • Allen EB, Allen MF (1990) The mediation of competition by mycorrhizae in successional and patchy environments. In: Grace JR, Tilman D (eds) Perspectives on plant competition. Academic, New York, pp 367–389

    Google Scholar 

  • Allen EB, Temple PJ, Bytnerowicz A, Arbaugh MJ, Sirulnik AG, Rao LE (2007) Patterns of understory diversity in mixed coniferous forests of southern California impacted by air pollution. ScientificWorldJournal 7, http://www.thescientificworld.com

  • Baldrian P (2009) Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia 161:657–660

    Article  PubMed  Google Scholar 

  • Bannister P, Strong GL (2001) Carbon and nitrogen isotope ratios, nitrogen content and heterotrophy in New Zealand mistletoes. Oecologia 126:10–20

    Article  Google Scholar 

  • Beau C (1920) Sur le role trophique des endophytes d’orchid6es. Comp Rend Acad Sci 171:675–677

    Google Scholar 

  • Bennett JR, Mathews S (2006) Phylogeny of the parasitic plant family Orobanchaceae inferred from phytochrome A. Am J Bot 93:1039–1051

    Article  PubMed  CAS  Google Scholar 

  • Bernard N (1899) Sur la germination du Neottia nidus-avis. C R Hebd Seances Acad Sci 128:1253–1255

    Google Scholar 

  • Bernard N (1908) La culture des orchidées dans ses rapports avec la symbiose. Société Royale d’Agriculture et de Botanique de Gand, Gand

    Google Scholar 

  • Bidartondo MI, Bruns TD (2005) On the origins of extreme mycorrhizal specificity in the Monotropoideae (Ericaceae): performance trade-offs during seed germination and seedling development. Mol Ecol 14:1549–1560

    Article  PubMed  CAS  Google Scholar 

  • Bidartondo MI, Read DJ (2008) Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17:3707–3716

    PubMed  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sérsic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392

    Article  PubMed  CAS  Google Scholar 

  • Bidartondo MI, Bruns TD, Weiß M, Sérgio C, Read DJ (2003) Specialized cheating of the ectomycorrhizal symbiosis by a epiparasitic liverwort. Proc Biol Sci 270:835–842

    Article  PubMed  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 Biol Sci 271:1799–1806

    Article  PubMed  CAS  Google Scholar 

  • Björkman E (1960) Monotropa hypopitys L.—an epiparasite on tree roots. Physiol Plant 13:308–327

    Article  Google Scholar 

  • Bonnardeaux Y, Brundrett M, Batty A, Dixon K, Koch J, Sivasithamparam K (2007) Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycol Res 111:51–61

    Article  PubMed  Google Scholar 

  • Booth MG (2004) Mycorrhizal networks mediate overstorey-understorey competition in a temperate forest. Ecol Lett 7:538–546

    Article  Google Scholar 

  • Bougoure J, Ludwig M, Brundrett M, Grierson P (2009) Identity and specificity of the fungi forming mycorrhizas with the rare mycoheterotrophic orchid Rhizanthella gardneri. Mycol Res 113:1097–1106

    Article  PubMed  CAS  Google Scholar 

  • Bougoure JJ, Brundrett MC, Grierson PF (2010) Carbon and nitrogen supply to the underground orchid, Rhizanthella gardneri. New Phytol 186:947–956

    Article  PubMed  CAS  Google Scholar 

  • Boullard B (1979) Considérations sur la symbiose fongique chez les Ptéridophytes. Syllogeus 19:1–58

    Google Scholar 

  • Bruce JG, Beitel JM (1979) A community of Lycopodium gametophytes in Michigan. Am Fern J 69:33–41

    Article  Google Scholar 

  • Bruns TD, Read DJ (2000) In vitro germination of nonphotosynthetic, myco-heterotrophic plants stimulated by fungi isolated from the adult plants. New Phytol 148:335–342

    Article  Google Scholar 

  • Burgeff H (1932) Saprophytismus und Symbiose. Studien an tropischen Orchideen. Gustav Fischer, Jena, Germany

    Google Scholar 

  • Burgeff H (1936) Samenkeimung der Orchideen. Gustav Fischer, Jena, Germany

    Google Scholar 

  • Burgeff H (1959) Mycorrhiza of orchids. In: Withner CL (ed) The orchids. Ronald Press, New York, pp 361–395

    Google Scholar 

  • Cameron DD, Bolin JF (2010) Isotopic evidence of partial mycoheterotrophy in the Gentianaceae: Bartonia virginica and Obolaria virginica as case studies. Am J Bot 97:1272–1277

    Article  PubMed  Google Scholar 

  • Cameron DD, Leake JR (2007) A different kind of parasitic plant: a brief history of mycoheterotrophy and epi-parasitism. Haustorium 50:4–6

    Google Scholar 

  • Cameron KM, Chase MW, Rudall PJ (2003) Recircumscription of the monocotyledonous family Petrosaviaceae to include Japanolirion. Brittonia 55:214–225

    Article  Google Scholar 

  • Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhiza in orchids: evidence from the plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytol 171:405–416

    Article  PubMed  CAS  Google Scholar 

  • Cameron DD, Johnson I, Read DJ, Leake JR (2008) Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytol 180:176–184

    Article  PubMed  CAS  Google Scholar 

  • Cameron DD, Preiss K, Gebauer G, Read DJ (2009) The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytol 183:358–364

    Article  PubMed  CAS  Google Scholar 

  • Camp WH (1940) Aphyllous forms in pyrola. Bull Torrey Bot Club 67:453–465

    Article  Google Scholar 

  • Campbell EO (1962) The mycorrhiza of Gastrodia cunninghamii Hook. F. Trans R Soc New Zealand 1:289–296

    Google Scholar 

  • Campbell EO (1964) The fungal association in a colony of Gastrodia sesamoides. R Br Trans R Soc New Zealand 2:237–246

    Google Scholar 

  • Cha JY, Igarashi T (1995) Armillaria species associated with Gastrodia elata in Japan. Eur J Forest Pathol 25:319–326

    Article  Google Scholar 

  • Cha JY, Igarashi T (1996) Armillaria jezoensis, a new symbiont of Galeola septentrionalis (Orchidaceae) in Hokkaido. Mycoscience 37:21–24

    Article  Google Scholar 

  • Chou H (1974) In propagation of Gastrodia elata Bl. Acta Bot Sin 16:288–290

    Google Scholar 

  • Christoph H (1921) Untersuchungen über mykotrophen Verhältnisse der “Ericales” und die Keimung von Pirolaceen. Beihefte Botan Centralblatt 38:115–157

    Google Scholar 

  • Courty P-E, Walder F, Boller T, Ineichen K, Wiemken A, Selosse M-A (2011) C and N metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis. Plant Physiol 156:952–961

    Article  PubMed  CAS  Google Scholar 

  • Currah RS, Zelmer CD, Hambleton S, Richardson KA (1997) Fungi from orchid mycorrhizas. In: Arditti J, Pridgeon AM (eds) Orchid biology: reviews and perspectives, VII. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 117–170

    Chapter  Google Scholar 

  • Curtis JT (1943) Germination and seedling development in five species of Cypripedium. Am J Bot 30:199–206

    Article  Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559

    Article  Google Scholar 

  • Dearnaley JDW (2006) The fungal endophytes of Erythrorchis cassythoides—is this orchid saprophytic or parasitic? Aust Mycol 25:51–57

    Google Scholar 

  • Dearnaley JDW, Bougoure JJ (2010) Isotopic and molecular evidence for saprotrophic Marasmiaceae mycobionts in rhizomes of Gastrodia sesamoides. Fungal Ecol 3:288–294

    Article  Google Scholar 

  • Dearnaley JDW, Martos F, Selosse M-A (2012) Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects. In: Hock B (ed) Fungal associations, The mycota IX, 2nd edn. Springer-Verlag, Berlin

    Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Douhan GW, Vincenot L, Selosse M-A (2011) Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biol 115:569–597

    Article  PubMed  Google Scholar 

  • Downie DG (1959) Rhisoctonia solani and orchid seed. Trans Bot Soc Edinb 37:279–285

    Article  Google Scholar 

  • Eriksson O, Kainulainen K (2011) The evolutionary ecology of dust seeds. Perspect Plant Ecol Evol Syst 13:73–87

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624

    Article  PubMed  CAS  Google Scholar 

  • Finlay RD, Read DJ (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants: 1. Translocation of C-14-labeled carbon between plants interconnected by a common mycelium. New Phytol 103:143–156

    Article  Google Scholar 

  • 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 12:406–412

    Article  Google Scholar 

  • Francis R, Read DJ (1984) Direct transfer of carbon between plants connected by vesicular arbuscular mycorrhizal mycelium. Nature 307:53–56

    Article  CAS  Google Scholar 

  • Frank AB (1885) Neue Mittheilungen über die Mycorrhiza der Bäume und der Monotropa hypopitys. Ber Dtsch Bot Ges 3:27–33

    Google Scholar 

  • Freudenstein JV (1999) Relationships and character transformation in Pyroloideae (Ericaceae) based on ITS sequences, morphology, and development. Syst Bot 24:398–408

    Article  Google Scholar 

  • Freudenstein JV, Doyle JJ (1994) Character transformation and relationships in Corallorhiza (Orchidaceae: Epidendroideae). I. Plastid DNA. Am J Bot 81:1449–1457

    Article  CAS  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York, 308pp

    Google Scholar 

  • Gebauer G (2005) Partnertausch im dunklen Wald—Stabile Isotope geben neue Einblicke in das Ernährungsverhalten von Orchideen. In: Bayer (ed) Auf Spurensuche in der Natur: Stabile Isotope in der ökologischen Forschung. Rundgespräche der Kommission für Ökologie Bd. 30. Akademie der Wissenschaften. Verlag Dr. Friedrich Pfeil, München, Germany, pp 55–67

    Google Scholar 

  • Gebauer G, Dietrich P (1993) Nitrogen isotope ratios in different compartments of a mixed stand of spruce, larch and beech trees and of understorey vegetation including fungi. Isotopenpraxis 29:35–44

    Article  CAS  Google Scholar 

  • Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol 160:209–223

    Article  CAS  Google Scholar 

  • Gebauer G, Schulze E-D (1991) Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia 87:198–207

    Article  Google Scholar 

  • Gebauer G, Taylor AFS (1999) 15N natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization. New Phytol 142:93–101

    Article  Google Scholar 

  • Gebauer G, Rehder H, Wollenweber B (1988) Nitrate, nitrate reduction and organic nitrogen in plants from different ecological and taxonomic groups of Central Europe. Oecologia 75:371–385

    Article  Google Scholar 

  • Girlanda M, Selosse M-A, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F, Cozzolino S, Perotto S (2006) Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Mol Ecol 15:491–504

    Article  PubMed  CAS  Google Scholar 

  • Girlanda M, Segreto R, Cafasso D, Liebel HT, Rodda M, Ercole E, Cozzolino S, Gebauer G, Perotto S (2011) Photosynthetic Mediterranean meadow orchids feature partial mycoheterotrophy and specific mycorrhizal associations. Am J Bot 98:1148–1163

    Article  PubMed  Google Scholar 

  • Gleixner G, Danier H-J, Werner RA, Schmidt H-L (1993) Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing fungi. Plant Physiol 102:1287–1290

    PubMed  CAS  Google Scholar 

  • Haber E (1987) Variability distribution and systematics of pyrola-picta sensu-lato Ericaceae in Western North America. Syst Bot 12:324–335

    Article  Google Scholar 

  • Hadley G (1970) Non-specificity of symbiotic infection in orchid mycorrhiza. New Phytol 69:1015–1023

    Article  Google Scholar 

  • Hamada M (1939) Studien über die Mykorrhiza von Galeola septentrionalis Reichb. F.—Ein neuer Fall der Mycorrhizabildung durch intraradicale Rhizomorpha. Jpn J Bot 10:151–211

    Google Scholar 

  • Hamada M, Nakamura S (1963) Wurzelsymbiose von Galeola altissima Reichb. F., einer chlorophyllfreien Orchidee, mit dem holzzerstörenden Pilz Hymenochaete crocicreas Berk et Br. Science Reports of the Tohoku University, Fourth Series (Biology), vol 29, pp 227–238

    Google Scholar 

  • Harvais G, Hadley G (1967) The relation between host and endophyte in orchid mycorrhiza. New Phytol 66:205–215

    Article  Google Scholar 

  • Hashimoto Y, Kunishi A, Hasegawa S (2005) Interspecific C transfers from Larix kaempferi Carr. to Pyrola incarnata Fischer by way of mycorrhizal fungi. Inoculum (Supplement to Mycologia) 56:23–24

    Google Scholar 

  • Hashimoto Y, Fukukawa S, Kunishi A, Suga H, Richard F, Sauve M, Selosse M-A (2012) Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids. New Phytol 195(3):620–630

    Article  PubMed  Google Scholar 

  • Hofmeister W (1857) Beiträge zur Entwicklungsgeschichte der Gefässkryptogamen. II. Abh Math Phys Cl Königl Sächs Ges Wiss 3:601–682, Taf. 1–13

    Google Scholar 

  • Högberg P (1997) Tansley review no. 95. 15N natural abundance in soil-plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Högberg P, Plamboeck AH, Taylor AFS, Fransson PMA (1999) Natural 13C abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests. Proc Natl Acad Sci U S A 96:8534–8539

    Article  PubMed  Google Scholar 

  • Hunt R, Hope-Simpson JF (1990) Growth of Pyrola rotundifolia ssp. maritima in relation to shade. New Phytol 114:129–137

    Article  Google Scholar 

  • Hynson NA, Bruns TD (2009) Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity. Proc Biol Sci 276:4053–4059

    Article  PubMed  Google Scholar 

  • Hynson NA, Bruns TD (2010) Fungal hosts for mycoheterotrophic plants: a nonexclusive, but highly selective club. New Phytol 185:598–601

    Article  PubMed  Google Scholar 

  • Hynson NA, Preiss K, Gebauer G (2009a) Is it better to give than receive? A stable isotope perspective to orchid-fungal carbon transport in the green orchid species Goodyera repens and Goodyera oblongifolia. New Phytol 182:8–11

    Article  PubMed  CAS  Google Scholar 

  • Hynson NA, Preiss K, Gebauer G, Bruns TD (2009b) Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytol 182:719–726

    Article  PubMed  Google Scholar 

  • Hynson NA, Mambelli S, Amend AS, Dawson TE (2012) Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): a field manipulation and stable isotope approach. Oecologia 169:307–317. doi:10.1007/s00442-011-2198-3

    Article  PubMed  Google Scholar 

  • Illyés Z, Halász K, Rudnóy S, Ouanphanivanh N, Garay T, Bratek Z (2009) Changes in the diversity of the mycorrhizal fungi of orchids as a function of the water supply of the habitat. J Appl Bot Food Qual 83:28–36

    Google Scholar 

  • Imhof S (2008) Specialized mycorrhizal colonization pattern in achlorophyllous Epirixanthes spp. (Polygalaceae). Plant Biol 9:786–792

    Article  Google Scholar 

  • Irmisch T (1855) Bemerkungen über einige Pflanzen der deutschen Flora. Flora 13:625–638

    Google Scholar 

  • Isogai N, Yamamura Y, Mariko S, Nakano T (2003) Seasonal pattern of photosynthetic production in a subalpine evergreen herb, Pyrola incarnata. J Plant Res 116:199–206

    Article  PubMed  Google Scholar 

  • Johnson-Groh CL (1998) Population demographics, underground ecology and phenology of Botrychium mormo. In: Berlin N, Miller P, Borovansky J, Seal US, Byers O (eds) Population and habitat viability assessment (PHVA) for the goblin fern (Botrychium mormo), Final Report. Conservation Biology Specialist Group, Apple Valley, Minnesota, pp 103–108

    Google Scholar 

  • Johnson-Groh CL, Lee JM (2002) Phenology and demography of two species of Botrychium (Ophioglossaceae). Am J Bot 89:1624–1633

    Article  PubMed  Google Scholar 

  • Jones RI (2000) Mixotrophy in planktonic protists: an overview. Freshwater Biol 45:219–226

    Article  Google Scholar 

  • Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse M-A (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and non-photosynthetic mutants of Cephalanthera damasonium. New Phytol 166:639–653

    Article  PubMed  CAS  Google Scholar 

  • Kamienski F (1881) Die Vegetationsorgane der Monotropa hypopitys L. Bot Zeit 29:458–461

    Google Scholar 

  • Kamjunke N, Tittel J (2009) Mixotrophic algae constrain the loss of organic carbon by exudation. J Phycol 45:807–811

    Article  CAS  Google Scholar 

  • Khan AG (1972) Mycorrhizae in the Pakistan Ericales Pak. J Bot 4:183–194

    Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Felbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi G, Higuchi M, Yoshimura H, Morota T, Suzuki A (2008a) In vitro symbiosis between Gastrodia elata Blume (Orchidaceae) and Armillaria Kummer (Tricholomataceae) species isolated from the orchid tuber. J Jpn Bot 83:77–87

    Google Scholar 

  • Kikuchi G, Higuchi M, Morota T, Nagasawa E, Suzuki A (2008b) Fungal symbiont and cultivation test of Gastrodia elata Blume (Orchidaceae). J Jpn Bot 83:88–95

    Google Scholar 

  • Knudson L (1922) Nonsymbiotic germination of orchid seeds. Bot Gaz 73:1–25

    Article  Google Scholar 

  • Kohzu A, Yoshioka T, Ando T, Takahashi M, Koba K, Wada E (1999) Natural 13C and 15N abundance of field-collected fungi and their ecological implications. New Phytol 144:323–330

    Article  Google Scholar 

  • Kranabetter JM, MacKenzie WH (2010) Contrasts among mycorrhizal plant guilds in foliar nitrogen concentration and d15N along productivity gradients of a boreal forest. Ecosystems 13:108–117

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kunishi A, Hasegawa S, Hashimoto Y (2004) Effects of mycorrhiza on Pyrola incarnata growing in dark forest floor. In: Proceedings of the 51st annual meeting of the Ecological Society of Japan (JES51)

    Google Scholar 

  • Kusano S (1911) Gastrodia elata and its symbiotic association with Armillaria mellea. J Coll Agric Imp Univ Tokyo 4:1–65

    Google Scholar 

  • Leake JR (1994) Tansley review No. 69. The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216

    Article  Google Scholar 

  • Leake JR (2004) Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Curr Opin Plant Biol 7:422–428

    Article  PubMed  CAS  Google Scholar 

  • Leake JR (2005) Plants parasitic on fungi: unearthing the fungi in myco-heterotrophs and debunking the “saprophytic” plant myth. Mycologist 19:113–122

    Google Scholar 

  • Lerat S, Gauci R, Catford JG, Vierheilig H, Piché Y, Lapointe L (2002) 14C transfer between the spring ephemeral Erythronium americanum and sugar maple saplings via arbuscular mycorrhizal fungi in natural stands. Oecologia 132:181–187

    Article  Google Scholar 

  • Levin I, Kromer B (1997) Twenty years of atmospheric 14CO2 observations at Schauinsland Station, Germany. Radiocarbon 39:205–218

    CAS  Google Scholar 

  • Liebel HT, Gebauer G (2011) Stable isotope signatures confirm carbon and nitrogen gain through ectomycorrhizas in the ghost orchid Epipogium aphyllum Swartz. Plant Biol 13:270–275

    Article  PubMed  CAS  Google Scholar 

  • Liebel HT, Preiss K, Gebauer G (2009) Parsiell mycoheterotrofi i norske vintergrønnarter – relevans for vernetiltak av truede vintergrønnarter (partial myco-heterotrophy in Norwegian wintergreen species—relevance for endangered species protection). Blyttia J Norw Bot Soc 67:138–143

    Google Scholar 

  • Liebel HT, Bidartondo MI, Preiss K, Segreto R, Stöckel M, Rodda M, Gebauer G (2010) C and N isotope signatures reveal constraints to nutritional modes in orchids of the Mediterranean and Macaronesia. Am J Bot 97:903–912

    Article  PubMed  CAS  Google Scholar 

  • Lievens B, van Kerckhove S, Justé A, Cammue BPA, Honnay O, Jacquemyn H (2010) From extensive clone libraries to comprehensive DNA arrays for the efficient and simultaneous detection and identification of orchid mycorrhizal fungi. J Microbiol Methods 80:76–85

    Article  PubMed  CAS  Google Scholar 

  • Ligrone R, Pocok 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 

  • Lihnell D (1942) Keimungsversuche mit Pyrola-Samen. Symb Bot Upsal 6:1–37

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, UK

    Google Scholar 

  • Martin F, Selosse M-A (2008) The Laccaria genome: a symbiont blueprint decoded (Tansley review—introduction to a special issue). New Phytol 180:296–310

    Article  PubMed  CAS  Google Scholar 

  • Martos F, Dulormne M, Pailler T, Bonfante P, Faccio A, Fournel J, Dubios M-P, Selosse M-A (2009) Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytol 184:668–681

    Article  PubMed  CAS  Google Scholar 

  • Matsuda Y, Amiya A, Ito S-I (2008) Colonization patterns of mycorrhizal fungi associated with two rare orchids, Cephalanthera falcata and C. erecta.. Ecol Res 24:1023–1031

    Article  Google Scholar 

  • Matsuda Y, Shimizu S, Mori M, Ito S-I, Selosse M-A (2012) Seasonal and spatial changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica growing under different light environments. In revision for Am. J, Bot

    Google Scholar 

  • Matsushita N, Fukuda K, Nagasawa E, Terashita T, Suzuki K (1996) Armillaria species in Japan identified by isozyme patterns with special reference to the biological species of the Northern hemisphere. J For Res 1:155–160

    Article  Google Scholar 

  • Mayor JR, Schuur EAG, Henkel TW (2009) Elucidating the nutritional dynamics of fungi using stable isotopes. Ecol Lett 12:171–183

    Article  PubMed  Google Scholar 

  • McCormick MK, Whigham DF, O’Neill J (2004) Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytol 163:425–438

    Article  Google Scholar 

  • McCormick MK, Taylor DL, Juhaszova K, Burnett RK, Whigham DF, O’Neill JP (2012) Limitations on orchid recruitment: not a simple picture. Mol Ecol 21:1511–1523

    Article  PubMed  Google Scholar 

  • McGuire KL (2007) Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–574

    Article  PubMed  Google Scholar 

  • McKendrick SL, Leake JR, Read DJ (2000) Symbiotic germination and development of myco-heterotrophic plants in nature: transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytol 145:539–548

    Article  Google Scholar 

  • McKendrick SL, Leake JR, Taylor DL, Read DJ (2002) Symbiotic germination and development of the myco-heterotrophic orchid Neottia nidus-avis in nature and its requirement for locally distributed Sebacina spp. New Phytol 154:233–247

    Article  Google Scholar 

  • McNeal JR, Arumugunathan K, Kueh JV, Boore JL, dePamphilis CW (2007) Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biol 5:55

    Article  PubMed  CAS  Google Scholar 

  • Merckx V, Schols P, Van De Kamer HM, Maas HM, Huysmans S, Smets E (2006) Phylogeny and evolution of Burmaniaceae (Dioscoreales) based on nuclear and mitochondrial data. Am J Bot 93:1684–1698

    Article  PubMed  Google Scholar 

  • Merckx V, Stöckel M, Fleischmann A, Bruns TD, Gebauer G (2010) 15N and 13C natural abundance of two mycoheterotrophic and a putative partially mycoheterotrophic species associated with arbuscular mycorrhizal fungi. New Phytol 188:590–596

    Article  PubMed  CAS  Google Scholar 

  • Mettenius G (1856) Filices Horti Botanici Lipsiensis. L. Voss, Leipzig

    Book  Google Scholar 

  • Milligan MJ, Williams PG (1988) The mycorrhizal relationship of multinucleate rhizoctonias from non-orchids with Microtis (Orchidaceae). New Phytol 108:205–209

    Article  Google Scholar 

  • Montfort C, Küsters E (1940) Saprophytismus und Photosynthese. I. Biochemische und physiologische Studien an Humus-Orchideen. Bot Arch 40:571–633

    CAS  Google Scholar 

  • Motomura H, Yukawa T, Ueno O, Kagawa A (2008) The occurrence of Crassulacean acid metabolism in Cymbidium (Orchidaceae) and its ecological and evolutionary implications. J Plant Res 121:163–177

    Article  PubMed  CAS  Google Scholar 

  • Motomura H, Selosse M-A, Martos F, Kagawa A, Yukawa T (2010) Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae). Ann Bot 106:573–581

    Article  PubMed  Google Scholar 

  • Muir HJ (1989) Germination and mycorrhizal fungus compatibility in European orchids. In: Pritchard HW (ed) Modern methods in orchid conservation: the role of physiology, ecology and management. Cambridge University Press, England, pp 39–56

    Google Scholar 

  • Mursidawati S (2004) Mycorrhizal association, propagation and conservation of the myco-heterotrophic orchid Rhizanthella gardneri. MSc thesis, The University of Western Australia

    Google Scholar 

  • Nakano A, Takahashi K, Kimura M (1999) The carbon origin of arbuscular mycorrhizal fungi estimated from δ13C values of individual spores. Mycorrhiza 9:41–47

    Article  CAS  Google Scholar 

  • Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178

    Article  PubMed  CAS  Google Scholar 

  • Neales TF, Hew CS (1975) Two types of carbon fixation in tropical orchids. Planta 123:303–306

    Article  CAS  Google Scholar 

  • Ogura-Tsujita Y, Yukawa T (2008) High mycorrhizal specificity in a widespread mycoheterotrophic plant, Eulophia zollingeri (Orchidaceae). Am J Bot 95:93–97

    Article  PubMed  Google Scholar 

  • Ogura-Tsujita Y, Gebauer G, Hashimoto T, Umata H, Yukawa T (2009) Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proc Biol Sci 276:761–767

    Article  PubMed  CAS  Google Scholar 

  • Ogura-Tsujita Y, Yokoyama J, Miyoshi K, Yukawa T (2012) Shifts in mycorrhizal fungi during the evolution of autotrophy to mycoheterotrophy in Cymbidium (Orchidaceae). Am J Bot 99(7):1158–1176

    Article  PubMed  Google Scholar 

  • Ota Y, Intini M, Hattori T (2000) Genetic characterization of heterothallic and non-heterothallic Armillaria mellea sensu stricto. Mycol Res 104:1046–1054

    Article  CAS  Google Scholar 

  • Ouanphanivanh N, Merényi Z, Orczán ÁK, Bratek Z, Szigeti Z, Illyés Z (2008) Could orchids indicate truffle habitats? Mycorrhizal association between orchids and truffles. Acta Biol Szeg 52:229–232

    Google Scholar 

  • Parrent JL, James TY, Vasaitis R, Taylor AFS (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol 9:148

    Article  PubMed  CAS  Google Scholar 

  • 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 163:617–627

    Article  Google Scholar 

  • Phillips RD, Barrett MD, Dixon KW, Hopper SD (2011) Do mycorrhizal symbioses cause rarity in orchids? J Ecol 99:858–869

    Article  Google Scholar 

  • Preiss K, Gebauer G (2008) A methodological approach to improve estimates of nutrient gains by partially myco-heterotrophic plants. Isotopes Environ Health Stud 44:393–401

    Article  PubMed  CAS  Google Scholar 

  • Preiss K, Adam IKU, Gebauer G (2010) Irradiance governs exploitation of fungi: fine-tuning of carbon gain by two partially myco-heterotrophic orchids. Proc Biol Sci 277:1333–1336

    Article  PubMed  Google Scholar 

  • Press MC, Graves JD (1995) Parasitic plants. Chapmann & Hall, London

    Google Scholar 

  • Press MC, Smith JD, Stewart GR (1991) Carbon acquisition and assimilation relations in parasitic plants. Funct Ecol 5:278–283

    Article  Google Scholar 

  • Pridgeon A, Cribb PJ, Chase MM (2008) Genera orchidacearum: vol 4: Epidendroidae. Oxford University Press, New York

    Google Scholar 

  • Ramsay RR, Dixon KW, Sivasithamparam K (1986) Patterns of infection and endophytes associated with Western Australian orchids. Lindleyana 1:203–214

    Google Scholar 

  • Rasmussen HN (1995) Terrestrial orchids from seed to mycotrophic plant. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Rasmussen HN (2002) Recent developments in the study of orchid mycorrhiza. Plant Soil 244:149–163

    Article  CAS  Google Scholar 

  • Rayner MC (1927) Mycorrhiza: an account of non-pathogenic infection by fungi in vascular plants and bryophyes. New phytologist reprint no. 15. Wheldon & Wesley, London, UK

    Google Scholar 

  • Reeves P, Chase MW, Goldblatt P, Rudall P, Fay MF, Cox AV, Lejeune B, Souza-Chies T (2001) Molecular systematics of Iridaceae: evidence from four plastid DNA regions. Am J Bot 88:2074–2087

    Article  PubMed  CAS  Google Scholar 

  • Renner O (1938) Über blasse, saprophytische Cephalanthera alba und Epipactis latifolia. Flora 132:225–233

    Google Scholar 

  • Robertson DC, Robertson JA (1985) Ultrastructural aspects of Pyrola mycorrhizae. Can J Bot 63:1089–1098

    Article  Google Scholar 

  • Robinson D, Fitter A (1999) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50:9–13

    CAS  Google Scholar 

  • Roy M, Watthana S, Stier A, Richard F, Vessabutr S, Selosse M-A (2009a) Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biol 7:51

    Article  PubMed  Google Scholar 

  • Roy M, Yagame T, Yamato M, Iwase K, Heinz C, Faccio A, Bonfante P, Selosse M-A (2009b) Ectomycorrhizal Incybe species associate with the mycoheterotrophic orchid Epipogium aphyllum but not its asexual propagules. Ann Bot 104:595–610

    Article  PubMed  Google Scholar 

  • Roy M, Gonneau C, Rocheteau A, Berveiller D, Thomas J-C, Damesin C, Selosse M-A (in press) Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ. Ecol Monographs

    Google Scholar 

  • Rudall PJ, Bateman R (2006) Morphological phylogenetic analysis of Pandanales: testing contrasting hypotheses of floral evolution. Syst Bot 31:223–238

    Article  Google Scholar 

  • Sadovsky O (1965) Orchideen im eigenen Garten. Bayerischer Landwirtschaftsverlag, Munich, Germany

    Google Scholar 

  • Salisbury RA (1804) On the germination of the seeds of Orchidaceae. Trans Linn Soc Lond 7:29–32

    Article  Google Scholar 

  • Salmia A (1986) Chlorophyll-free form of Epipactis helleborine (Orchidaceae) in SE Finland. Ann Bot Fenn 23:49–57

    Google Scholar 

  • Salmia A (1989a) Features of endomycorrhizal infection of chlorophyll-free and green forms of Epipactis helleborine (Orchidaceae). Ann Bot Fenn 26:15–26

    Google Scholar 

  • Salmia A (1989b) General morphology and anatomy of chlorophyll-free and green forms of Epipactis helleborine (Orchidaceae). Ann Bot Fenn 26:95–105

    Google Scholar 

  • Schimel DS (1993) Theory and application of tracers. Academic, San Diego, USA

    Google Scholar 

  • Schulze E-D, Lange OL, Ziegler H, Gebauer G (1991) Carbon and nitrogen isotope ratios of mistletoes growing on nitrogen fixing and non-nitrogen fixing hosts and on CAM plants in the Namib desert confirm partial heterotrophy. Oecologia 88:457–462

    Article  Google Scholar 

  • Schulze E-D, Beck E, Müller-Hohenstein K (2005) Plant ecology. Springer, Berlin

    Google Scholar 

  • Sekizaki H, Kuninaga S, Yamamoto M, Asazu SN, Sawa S, Kojoma M, Yokosawa R, Yoshida N (2008) Identification of Armillaria nabsnona in Gastrodia tubers. Biol Pharm Bull 31:1410–1414

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Rousset F (2011) The plant-fungal marketplace. Science 333:828–829

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Roy M (2009) Green plants eating fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Weiss M, Jany JL, Tillier A (2002) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L.C.M. Rich. and neighbouring treeectomycorrhizae. Mol Ecol 11:1831–1844

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, 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

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 22:621–628

    Article  Google Scholar 

  • Selosse M-A, Setaro S, Glatard F, Richard F, Urcelay C, Weiß M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Dubois M-P, Alvarez N (2009) Do Sebacinales commonly associate with plant roots as endophytes? Mycol Res 113:1062–1069

    Article  PubMed  CAS  Google Scholar 

  • Selosse M-A, Martos F, Perry BA, Padamsee M, Roy M, Pailler T (2010) Saprotrophic fungal symbionts in tropical achlorophyllous orchids: finding treasures among the ‘molecular scraps’? Plant Signal Behav 5:1–5

    Article  Google Scholar 

  • Selosse M-A, Boullard B, Richardson D (2011) Noel Bernard (1874–1911): orchids to symbiosis in a dozen years, one century ago. Symbiosis 54:61–68

    Article  Google Scholar 

  • Sharma J, Zettler LW, Van Sambeek JW, Ellersieck MR, Starbuck CJ (2003) Symbiotic seed germination and mycorrhizae of federally threatened Platanthera praeclara (Orchidaceae). Am Midl Nat 149:104–120

    Article  Google Scholar 

  • Shefferson RP, Weiß M, Kull T, Taylor DL (2005) High specificity generally characterizes mycorrhizal association in rare lady’s slipper orchids, genus Cypripedium. Mol Ecol 14:613–626

    Article  PubMed  CAS  Google Scholar 

  • Shefferson RP, Kull T, Tali K (2006) Demographic response to shading and defoliation in two woodland orchids. Folia Geobot 41:95–106

    Article  Google Scholar 

  • Shefferson RP, Taylor DL, Weiß M, Garnica S, McCormick MK, Adams S, Gray HM, McFarland JW, Kull T, Tali K, Yukawa T, Kawahara T, Miyoshi K, Lee Y-I (2007) The evolutionary history of mycorrhizal specificity among lady’s slipper orchids. Evolution 61:1380–1390

    Article  PubMed  Google Scholar 

  • Shefferson RP, Kull T, Tali K (2008) Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills. Am J Bot 95:156–164

    Article  PubMed  Google Scholar 

  • Silvera K, Santiago LS, Cushman JC, Winter K (2010) The incidence of crassulacean acid metabolism in Orchidaceae derived from carbon isotope ratios: a checklist of the flora of Panama and Costa Rica. Bot J Linn Soc 163:194–222

    Article  Google Scholar 

  • Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165

    Article  CAS  Google Scholar 

  • 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 388:579–582

    Article  CAS  Google Scholar 

  • Smith SE (1966) Physiology and ecology of orchid mycorrhizal fungi with reference to seedling nutrition. New Phytol 65:488–499

    Article  Google Scholar 

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

    Google Scholar 

  • Stark JM (2000) Nutrient transformations. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 215–234

    Chapter  Google Scholar 

  • Stark C, Babik W, Durka W (2009) Fungi from the roots of the common terrestrial orchid Gymnadenia conopsea. Mycol Res 113:952–959

    Article  PubMed  Google Scholar 

  • Stöckel M, Meyer C, Gebauer G (2011) The degree of mycoheterotrophic carbon gain in green, variegated and vegetative albino individuals of Cephalanthera damasonium is related to leaf chlorophyll concentrations. New Phytol 189:790–796

    Article  PubMed  Google Scholar 

  • Stokey AG (1950) The gametophyte of the Gleicheniaceae. Bull Torrey Bot Club 77:323–339

    Article  Google Scholar 

  • Struwe L, Kadereit J, Klackenberg J, Nilsson S, Thiv M, von Hagen KB, Albert VA (2002) Systematics, character evolution, and biogeography of Gentianaceae, including a new tribal and subtribal classification. In: Struwe L, Albert VA (eds) Gentianaceae—systematics and natural history. Cambridge University Press, Cambridge, pp 21–309

    Google Scholar 

  • Sung JM, Jung BS, Yang KJ, Lee HK, Harrington TC (1995) Production of Gastrodia elata tuber using Armillaria spp. Korean J Mycol 23:61–70

    Google Scholar 

  • Taylor DL, Bruns TD (1997) Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proc Natl Acad Sci U S A 94:4510–4515

    Article  PubMed  CAS  Google Scholar 

  • Taylor AFS, Fransson PM, Högberg P, Högberg MN, Plamboeck AH (2003) Species level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol 159:757–774

    Article  CAS  Google Scholar 

  • Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388

    Article  CAS  Google Scholar 

  • Tedersoo L, Pellet P, Kõljalg U, Selosse M-A (2007) Parallel evolutionary paths to mycohetereotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151:206–217

    Article  PubMed  Google Scholar 

  • Tennakoon KU, Pate JS (1996) Heterotrophic gain of carbon from hosts by the xylem-tapping root hemiparasite Olax phyllanthi (Olacaceae). Oecologia 105:369–376

    Article  Google Scholar 

  • Terashima K, Kawashima Y, Cha JY, Miura K (1998) Identification of Armillaria species from Hokkaido by analysis of the intergenic spacer (IGS) region of ribosomal DNA using PCR-RFLP. Mycoscience 39:179–183

    Article  Google Scholar 

  • Terashita T, Chuman S (1987) Fungi inhabiting wild orchids in Japan. IV. Armillariella tabescens, a new symbiont of Galeola septentrionalis. Trans Mycol Soc Jpn 28:145–154

    Google Scholar 

  • Terashita T, Chuman S (1989) Armillarias, isolated from the wild orchid, Galeola septentrionalis. In: Proceedings of the 7th IUFRO international conference on root and butt rots of forest trees, pp 364–370

    Google Scholar 

  • Těšitel J, Plavcová L, Cameron DD (2010) Interactions between hemiparasitic plants and their hosts. The importance of organic carbon transfer. Plant Signal Behav 5:1072–1076

    Article  PubMed  Google Scholar 

  • Těšitel J, Lepš J, Vráblová M, Cameron DD (2011) The role of heterotrophic carbon acquisition by the hemiparasitic plant Rhinanthus alectorolophus in seedling establishment in natural communities: a physiological perspective. New Phytol 192:188–199

    Article  PubMed  Google Scholar 

  • Tesitelova T, Těšitel J, Jersáková J, Říhová G, Selosse M-A (2012) Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology. Am J Bot 99(6):1020–1032

    Article  PubMed  Google Scholar 

  • Teste FP, Simard SW, Durall DM, Guy RD, Jones MD, Schoonmaker AL (2009) Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90:2808–2822

    Article  PubMed  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JP, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  PubMed  CAS  Google Scholar 

  • Toftegaard T, Iason GR, Alexander IJ, Rosendahl S, Taylor AFS (2010) The threatened plant intermediate wintergreen (Pyrola media) associates with a wide range of biotrophic fungi in native Scottish pine woods. Biodivers Conserv 19:3963–3971

    Article  Google Scholar 

  • Tranchida-Lombardo V, Roy M, Bugot E, Santoro G, Püttsepp U, Selosse M-A, Cozzolino S (2010) Spatial repartition and genetic relationship of green and albino individuals in mixed populations of Cephalanthera orchids. Plant Biol 12:659–667

    PubMed  CAS  Google Scholar 

  • Trudell SA, Rygiewicz PT, Edmonds RL (2003) Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host-specificity of certain achlorophyllous plants. New Phytol 160: 391–401

    Article  CAS  Google Scholar 

  • Trumbore SE (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411

    Article  Google Scholar 

  • Umata H (1995) Seed germination of Galeola altissima, an achlorophyllous orchid, with aphyllophorales fungi. Mycoscience 36:369–372

    Article  Google Scholar 

  • Umata H (1997) Formation of endomycorrhizas by an achlorophyllous orchid, Erythrorchis ochobiensis, and Auricularia polytricha. Mycoscience 38:335–339

    Article  Google Scholar 

  • Umata H (1998a) In vitro symbiotic association of an achlorophyllous orchid, Erythrorchis ochobiensis, with orchid and non-orchid fungi. Memoirs of the Faculty of Agriculture, Kagoshima University, vol 34, pp 97–107

    Google Scholar 

  • Umata H (1998b) A new biological function of shiitake mushroom, Lentinula edodes, in a myco-heterotrophic orchid, Erythrorchis ochobiensis. Mycoscience 39: 85–88

    Article  Google Scholar 

  • Umata H (1999) Germination and growth of Erythrorchis ochobiensis (Orchidaceae) accelerated by monokaryons and dikaryons of Lenzites betulinus and Trametes hirsuta. Mycoscience 40:367–371

    Article  Google Scholar 

  • Umata H, Kaneko M, Miyagi T, Nakahira Y (2007) The application and utilization of fungi for the propagation of the endangered achlorophyllous plant, Erythrorchis ochobiensis (Hayata) Garay (Orchidaceae) in natural situations. Research Bulletin of the Kagoshima University Forests 35:31–48

    Google Scholar 

  • Velenovsky J (1892) Über die Biologie und Morphologie der Gattung Moneses. Rozpravy Královské české společnosti nauk, řada, matematicko-přírodovědná 11:147–159

    Google Scholar 

  • Vincenot L, Tedersoo L, Richard F, Horcine H, Kõljalg U, Selosse M-A (2008) Fungal associates of Pyrola rotundifolia, a mixotrophic Ericaceae, from two Estonian boreal forests. Mycorrhiza 19:15–25

    Article  PubMed  Google Scholar 

  • Vujanovic V, St-Arnaut M, Barab D, Thibeault G (2000) Viability testing of orchid seed and the promotion of colouration and germination. Ann Bot 86:79–86

    Article  Google Scholar 

  • Wagner WH Jr, Wagner FS (1981) New species of moonworts, Botrychium subg. Botrychium (Ophioglossaceae), from North America. Am Fern J 71:20–30

    Article  Google Scholar 

  • Warcup JH (1973) Symbiotic germination of some Australian terrestrial orchids. New Phytol 72:387–392

    Article  Google Scholar 

  • Warcup JH (1981) The mycorrhizal relationships of Australian orchids. New Phytol 87:371–381

    Article  Google Scholar 

  • Warcup JH (1988) Mycorrhizal associations of isolates of Sebacina vermifera. New Phytol 110:227–231

    Article  Google Scholar 

  • Warcup JH, Talbot PHB (1967) Perfect states of rhizoctonias associated with orchids. New Phytol 66:631–641

    Article  Google Scholar 

  • Waterman RJ, Bidartondo MI, Stofberg J, Combs JK, Gebauer G, Savolainen V, Barraclough TG, Pauw A (2011) The effects of above- and belowground mutualism in orchid speciation and coexistence. Am Nat 177:E54–E68

    Article  PubMed  Google Scholar 

  • Watson DM (2009) Parasitic plants as facilitators: more dryad than dracula? J Ecol 97:1151–1159

    Article  Google Scholar 

  • Weiss M, Selosse M-A, Rexer K, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    Article  PubMed  Google Scholar 

  • Weiss M, Sýkorová Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F, Bauer R, Redecker D (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One 6:e16793

    Article  PubMed  CAS  Google Scholar 

  • Westwood JH, Yoder JI, Timko MP, dePamphilis CW (2010) The evolution of parasitism in plants. Trends Plant Sci 15:227–235

    Article  PubMed  CAS  Google Scholar 

  • Whittier P (1988) Dark-grown psilotum. Am Fern J 78:109–116

    Article  Google Scholar 

  • Whittier DP, Renzaglia KS (2005) The young gametophyte of Lycopodiella lateralis and the role of the intermediate shaft in development of Lycopodiella gametophytes. Am Fern J 95:153–159

    Article  Google Scholar 

  • Winther JL, Friedman WE (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255

    Article  PubMed  CAS  Google Scholar 

  • Winther JL, Friedman WE (2008) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytol 177:790–801

    Article  PubMed  CAS  Google Scholar 

  • Winther JL, Friedman WE (2009) Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. J Plant Res 122:485–496

    Article  PubMed  Google Scholar 

  • Wright M, Cross R, Dixon K, Huynh T, Lawrie A, Nesbitt L, Pritchard A, Swarts N, Thomson R (2009) Propagation and reintroduction of Caladenia. Aust J Bot 57:373–387

    Article  Google Scholar 

  • Wright MM, Cross R, Cousens RD, May TW, McLean CB (2010) Taxonomic and functional characterisation of fungi from the Sebacina vermifera complex from common and rare orchids in the genus Caladenia. Mycorrhiza 20:375–390

    Article  PubMed  Google Scholar 

  • Wu BY, Nara K, Hogetsu T (2001) Can C-14-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol 149:137–146

    Article  CAS  Google Scholar 

  • Wu J, Ma H, Lü M, Han S, Zhu Y, Jin H, Liang J, Liu L, Xu J (2010) Rhizoctonia fungi enhance the growth of the endangered orchid Cymbidium goeringii. Botany 88:20–29

    Article  CAS  Google Scholar 

  • Xu J, Guo S (2000) Retrospect on the research of the cultivation of Gastrodia elata Bl, a rare traditional Chinese medicine. Chin Med J 113:686–692

    PubMed  CAS  Google Scholar 

  • Yagame T, Yamato M, Mii M, Suzuki A, Iwase K (2007) Developmental processes of achlorophyllous orchid, Epipogium roseum: from seed germination to flowering under symbiotic cultivation with mycorrhizal fungus. J Plant Res 120:229–236

    Article  PubMed  Google Scholar 

  • Yagame T, Fukiharu T, Yamato M, Suzuki A, Iwase K (2008a) Identification of a mycorrhizal fungus in Epipogium roseum (Orchidaceae) from morphological characteristics of basidiomata. Mycoscience 49: 147–151

    Article  Google Scholar 

  • Yagame T, Yamato M, Suzuki A, Iwase K (2008b) Ceratobasidiaceae mycorrhizal fungi isolated from nonphotosynthetic orchid Chamaegastrodia sikokiana. Mycorrhiza 18:97–101

    Article  PubMed  Google Scholar 

  • Yagame T, Orihara T, Selosse M-A, Yamato M, Iwase K (2012) Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza-forming Ceratobasidiaceae fungi. New Phytol 193:178–187

    Article  PubMed  CAS  Google Scholar 

  • Yamato M, Iwase K (2008) Introduction of asymbiotically propagated seedlings of Cephalanthera falcata (Orchidaceae) into natural habitat and investigation of colonized mycorrhizal fungi. Ecol Res 23:329–337

    Article  Google Scholar 

  • Yamato M, Yagame T, Suzuki A, Iwase K (2005) Isolation and identification of mycorrhizal fungi associating with an achlorophyllous plant, Epipogium roseum (Orchidaceae). Mycoscience 46:73–77

    Article  CAS  Google Scholar 

  • Zettler LW, Hofer CJ (1998) Propagation of the little club-spur orchid (Platanthera clavellata) by symbiotic seed germination and its ecological implications. Environ Exp Bot 39:189–195

    Article  Google Scholar 

  • Zettler LW, Stewart SL, Bowles ML, Jacobs KA (2001) Mycorrhizal fungi and cold-assisted symbiotic germination of federally threatened eastern prairie fringed orchid, Platanthera leucophaea (Nuttall) Lindley. Am Midl Nat 145:168–175

    Article  Google Scholar 

  • Zimmer K, Hynson NA, Gebauer G, Allen EB, Allen MF, Read DJ (2007) Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytol 175:166–175

    Article  PubMed  CAS  Google Scholar 

  • Zimmer K, Meyer C, Gebauer G (2008) The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytol 178:395–400

    Article  PubMed  CAS  Google Scholar 

  • Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel K-H (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:e1002290

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, University of Hawaii at Manoa, Honolulu, HI, 96822, USA

    Nicole A. Hynson

  2. Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720, USA

    Thomas P. Madsen

  3. Centre d’Ecologie Fonctionnelle et Evolutive (CEFE-CNRS), Montpellier, France

    Marc-André Selosse & Melanie Roy

  4. Laboratory of Isotope Biogeochemistry, Bayreuth Center of Ecology and Environmental Research (BayCEER), University of Bayreuth, 95440, Bayreuth, Germany

    Iris K. U. Adam & Gerhard Gebauer

  5. Department of Chemical and Biological Sciences, Japan Women’s University, 2-8-1 Mejirodai, Tokyo, 112-8681, Japan

    Yuki Ogura-Tsujita

  6. Laboratoire Evolution et Diversité Biologique (UMR5174 EDB), Université de Toulouse, Toulouse, France

    Melanie Roy

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  1. Nicole A. Hynson
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  2. Thomas P. Madsen
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  3. Marc-André Selosse
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  4. Iris K. U. Adam
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  5. Yuki Ogura-Tsujita
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  6. Melanie Roy
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  7. Gerhard Gebauer
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Correspondence to Nicole A. Hynson .

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  1. , Naturalis Biodiversity Center, Leiden University, Einsteinweg 2, Leiden, 2333, Netherlands

    Vincent Merckx

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Hynson, N.A. et al. (2013). The Physiological Ecology of Mycoheterotrophy. In: Merckx, V. (eds) Mycoheterotrophy. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5209-6_8

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