Abstract
We present a review of the documented fungal colonizations of presumably symbiotic nature in lycophytes and ferns (“pteridophytes”). The sampling covers ca. 11 % (1287 spp.) of the estimated global diversity of these taxa (ca. 12,000 spp.) and shows an average presence of fungal endophytes of 68 %, which is significantly lower than the average presence of mycorrhiza of 80–85 % for the remaining tracheophytes. Above-average colonization rates up to 100 % among ferns are mainly found in phylogenetically old lineages, whereas below-average mycorrhization characterizes the Polypod I clade and the Aspleniaceae of the derived leptosporangiate ferns. Arbuscular Mycorrhizal Fungi (AMF) are found in 54 % of the species, to which 6 % of unspecified records of mycorrhizae should probably be added. Dark Septate Endophytes (DSE) are found in 13 % of the species, in about half the cases (6 %) together with AMF. Ectomycorrhizae have not been confirmed for pteridophytes so far, and basidiomycetes are found very rarely in mycoheterotropic gametophytes. Fungal endophytes are unevenly distributed across the life forms and most frequent with 75 % in the terrestrial species, followed with 69 % in saxicolous and with 58 % in epiphytic species. Although AMF have a low dispersal potential and thus are considered unreliable symbiotic partners for epiphytes, they are still present in 27 % of the investigated epiphytic pteridophytes. The occurrence of mycorrhizae across the taxa of pteridophytes bears a phylogenetic signal, as the derived ferns show a notable trend towards a growing independence from AM, in epiphytes more pronouncedly so than in terrestrial taxa.
Similar content being viewed by others
References
Abbott LK, Robson AD (1984) The effect of mycorrhizae on plant growth. In: Powell CL, Bagyaraj DJ (eds) VA mycorrhiza. CRC Press, Boca Raton
Allen MF, Swenson W, Querejeta JI, Egerton-Warburton LM, Treseder KK (2003) Ecology of mycorrhizae: a conceptual framework for complex interactions among plants and fungi. Annu Rev Phytopathol 41:271–303
Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141(4):612–619
Amatangelo KL, Vitousek PM (2008) Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia 157:619–627
Beck-Nielsen D, Madsen TV (2001) Occurrence of vesicular-arbuscular mycorrhiza in aquatic macrophytes from lakes and rivers. Aquat Bot 71:141–148
Berch SM, Kendrick B (1982) Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74:769–776
Bhat PR, Kaveriappa KM (2003) Occurrence of vesicular arbuscular mycorrhizal fungi in Marsilea minuta L. Mycorrhiza News 15(4):11–13
Bidartondo MI, Duckett JG (2010) Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. P Roy Soc B-Biol Sci 277:485–492
Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Letters 7(4):574–577
Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sc 13:492–498
Boullard B (1958) La mycotrophie chez pteridophytes: sa frequence, ses caracteres. sa signification. Drouillard, Bordeaux
Boullard B (1979) Considerations Sur la symbiose fongique chez les pteridophytes. Syllogeus 19:1–61
Brownsey PJ, Smith-Dodsworth J (2000) New Zealand ferns and allied plants. New revised edition, Bateman, Wellington, NZ
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304
Brundrett MC (2004) Diversity and classification of mycorrhizal associations. Bot Rev 79:473–495
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Cairney JW (2000) Evolution of mycorrhiza systems. Naturwissenschaften 87:467–475
Christenhusz MJ, Chase MW (2014) Trends and concepts in fern classification. Ann Bot 113(4):571–594
Christenhusz MJM, Zhang X-C, Schneider H (2011) A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa 19:7–54
Cooper KM (1976) A field survey of mycorrhizas in New Zealand ferns. New Zeal J Bot 14:169–181
Cornwell WK, Bedford BL, Chapin CT (2001) Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am J Bot 88:1824–1829
Cullings KW (1996) Single phylogenetic origin of ericoid mycorrhizae within the Ericaceae. Can J Bot 74:1896–1909
Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: a chequered history. P Roy Soc Lond B Bio 280(1759):20130207
Dhillion SS (1993) Vesicular-arbuscular mycorrhizas of Equisetum species in Norway and the USA: occurrence and mycotrophy. Mycol Res 97:656–660
Dubuisson JY, Schneider H, Hennequin S (2009) Epiphytism in ferns: diversity and history. CR Biol 332:120–128
Dubuisson JY, Bary S, Ebihara A, Carnero-Diaz E, Boucheron-Dubuisson E, Hennequin S (2013) Epiphytism, anatomy and regressive evolution in trichomanoid filmy ferns (Hymenophyllaceae). Bot J Linn Soc 173:573–593
Fernández N, Fontenla S, Messuti MI (2010) Mycorrhizal status of obligate and facultative epiphytic ferns in a Valdivian temperate forest of Patagonia, Argentina. Amer Fern J 100:16–26
Field KJ, Rimington WR, Bidartondo MI, Allinson KE, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2015) First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2. New Phytol 205(2):743–756
Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99
Fröhlich-Nowoisky J, Burrows SM, Xie Z, Engling G, Solomon PA, Fraser MP, Mayol-Bracero OL, Artaxo P, Begerow D, Conrad R, Andreae MO, Després VR, Pöschl U (2012) Biogeography in the air: fungal diversity over land and oceans. Biogeosciences 9:1125–1136
Gemma JN, Koske RE (1995) Mycorrhizae in Hawaiian epiphytes. Pac Sci 49:175–180
Gemma JN, Koske RE, Flynn T (1992) Mycorrhizae in Hawaiian pteridophytes: occurrence and evolutionary significance. Am J Bot 79:843–852
Genre A, Bonfante P (2010) The making of symbiotic cells in arbuscular mycorrhizal roots. In: Koltay H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Netherlands, pp. 57–71
Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162
Hennequin S, Schuettpelz E, Pryer KM, Ebihara A, Dubuisson JY (2008) Divergence times and the evolution of epiphytism in filmy ferns (Hymenophyllaceae) revisited. Int J Plant Sci 169:1278–1287
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547
Hietz P, Hietz-Seifert U (2009) Structure and ecology of epiphyte communities of a cloud forest in Central Veracruz, Mexico. J Veg Sci 6:719–728
Hoshizaki BJ, Moran RC (2001) Fern Grower's manual. Timber Press, Portland, Oregon, Revised and Expanded Edition
Iqbal SH, Yousaf M, Younus M (1981) A field survey of mycorrhizal associations in ferns of Pakistan. New Phytol 87:69–79
Janos DP (1993) Vesicular-arbuscular mycorrhizae of epiphytes. Mycorrhiza 4:1–4
Johansson D (1974) Ecology of vascular epiphytes in west African rain forest. Acta Phytogeog Suec 59:1–136
Jones DL, Clemensha SC (1976) Australian ferns and fern allies. A.H. and A.W, Reed, Sidney
Jones VAS, Dolan L (2012) The evolution of root hairs and rhizoids. Ann Bot 110:205–212
Jumpponen ARI (2001) Dark septate endophytes–are they mycorrhizal? Mycorrhiza 11(4):207–211
Jurkiewicz A, Ryszka P, Anielska T, Waligórski P, Białońska D, Góralska K, Tsimilli-Michael M, Turnau K (2010) Optimization of culture conditions of Arnica montana L.: effects of mycorrhizal fungi and competing plants. Mycorrhiza 20(5):293–306
Kenrick P, Strullu-Derrien C (2014) The origin and early evolution of roots. Plant Physiol 166(2):570–580
Kessler M, Jonas R, Cicuzza D, Kluge J, Piatek K, Naks P, Lehnert M (2010a) A survey of the mycorrhization of southeast Asian ferns and lycophytes. Plant Biol 12:788–793
Kessler M, Jonas R, Strasberg D, Lehnert M (2010b) Mycorrhizal colonizations of ferns and lycophytes on the island of La Réunion in relation to nutrient availability. BAE 11:329–336
Kessler M, Güdel R, Salazar L, Homeier J, Kluge J (2014) Impact of mycorrhization on the abundance, growth and leaf nutrient status of ferns along a tropical elevational gradient. Oecologia 175:887–900
Kirk JT (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press
Klemmedson JO (1992) Decomposition and nutrient release from mixtures of Gambel oak and ponderosa pine leaf litter. Forest Ecol Manag 47:349–361
Knie N, Fischer S, Grewe F, Polsakiewicz M, Knoop V (2015) Horsetails are the sister group to all other monilophytes and Marattiales are sister to leptosporangiate ferns. Mol Phylo Evol 90:140–149
Kottke I, Nebel M (2005) The evolution of mycorrhiza-like associations in liverworts: an update. New Phytol 167:330–334
Kramer KU, Schneller JJ, Wollenweber E (1995) Farne und Farnverwandte: Bau, Systematik, Biologie. Georg Thieme Verlag, Stuttgart
Krömer T, Kessler M (2006) Filmy ferns (Hymenophyllaceae) as high-canopy epiphytes. Ecotropica 12:57–63
Kroon LP, Bakker FT, Van Den Bosch GB, Bonants PJ, Flier WG (2004) Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet Biol 41:766–782
Kubitzki K (ed) (1990) The families and genera of vascular plants, vol 1. In: Kramer KU, Green PS (vol eds) Pteridophytes and Gymnosperms. Springer-Verlag, Berlin
Lara-Pérez LA, Valdés-Baizabal MD, Noa-Carrazana JC, Zulueta-Rodríguez R, Lara-Capistrán L, Andrade-Torres A (2015) Mycorrhizal associations of ferns and lycopods of Central Veracruz, Mexico. Symbiosis 65(2):85–92
Leake JR, Cameron DD, Beerling DJ (2008) Fungal fidelity in the mycoheterotroph to autotroph life cycle of Lycopodiaceae: a case of parental nurture? New Phytol 177:572–576
Lehnert M (2013) Grammitid Ferns I (Polypodiaceae): Melpomene. Flora Neotropica Monograph 112, New York Botanical Garden, USA, 122 pp.
Lehnert M, Kottke I, Setaro S, Pazmiño LF, Suárez JP, Kessler M (2009) Mycorrhizal associations in ferns from southern Ecuador. Am Fern J 99:292–306
Lehtonen S (2011) Towards resolving the complete fern tree of life. PLoS One 6:e24851. doi:10.1371/journal.pone.0024851
Lekberg Y, Rosendahl S, Olsson PA (2015) The fungal perspective of arbuscular mycorrhizal colonization in ‘nonmycorrhizal’plants. New Phytol 205(4):1399–1403
Lesica P, Antibus RK (1990) The occurrence of mycorrhizae in vascular epiphytes of two costa Rican rain forests. Biotropica 1990:250–258
Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse MA (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol Ecol 21:5098–5109
Moteetee A, Duckett JG, Russell AJ (1996) Mycorrhizas in the ferns of Lesotho. In: Gibby M, Johns RJ (eds) Camus JM. Pteridology in perspective. Royal Botanic Gardens, Kew, UK, pp. 621–631
Muthukumar T, Prabha K (2012) Fungal associations in gametophytes and young sporophytic roots of the fern Nephrolepis exaltata. Acta Bot Croat 71(1):139–146
Muthukumar T, Prabha K (2013) Arbuscular mycorrhizal and septate endophyte fungal associations in lycophytes and ferns of South India. Symbiosis 59(1):15–33
Muthukumar T, Udaiyan K (2000) Arbuscular mycorrhizas of plants growing in the western Ghats region, southern India. Mycorrhiza 9:297–313
Nielsen SL (1993) A comparison of aerial and submerged photosynthesis in some Danish amphibious plants. Aquat Bot 45(1):27–40
Ogura-Tsujita Y, Sakoda A, Ebihara A, Yukawa T, Imaichi R (2012) Arbuscular mycorrhiza formation in cordate gametophytes of two ferns, Angiopteris lygodiifolia and Osmunda japonica. J Plant Res 126:1–10
Page CN (2002) Ecological strategies in fern evolution: a neopteridological overview. Rev Paleobot Palynol 119(1):1–33
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbil 6:763–775
Pressel S, Ligrone R, Duckett JG (2008) The ascomycete Rhizoscyphus ericae elicits a range of host responses in the rhizoids of leafy liverworts: an experimental and cytological analysis. Fieldiana Bot 47:59–72
Pressel S, Bidartondo MI, Ligrone R, Duckett JG (2010) Fungal symbioses in bryophytes: new insights in the twenty first century. Phytotaxa 9:238–253
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 91:1582–1598
Qiu YL, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson RW, Hendry TA, Taylor DW (2007) A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. Int J Plant Sci 168(5):691–708
Radhinka KP, Rodrigues BF (2007) Arbuscular mycorrhizae in association with aquatic and marshy plants in Goa, India. Aquat Bot 86:291–294
Ragupathy S, Mahadevan A (1993) Distribution of vesicular-arbuscular mycorrhizae in the plants and rhizosphere soils of the tropical plains, Tamil Nadu, India. Mycorrhiza 3:123–136
Raven JA, Osborne BA, Johnston AM (1985) Uptake of CO2 by aquatic vegetation. Plant Cell Environ 8(6):417–425
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. PNAS 91(25):11841–11184
Reyes-Jaramillo I, Camargo-Ricalde SL, Aquiahuatl-Ramos MDLÁ (2008) Mycorrhizal-like interaction between gametophytes and young sporophytes of the fern Dryopteris muenchii (Filicales) and its fungal endophyte. Rev Biol Trop 56:1101–1107
Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book? New Phytol 205(4):1394–1398
Rossman AY, Palm ME (2006) Why are phytophthora and other oomycota not true fungi? Outlook Pest Manag 17:217
Rothfels CJ, Sundue MA, Schuettpelz E, Kato M, Larsson A, Kuo LY, Pryer KM (2012) A revised classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61:515–533
Schmid E, Oberwinkler F (1993) Mycorrhiza-like interaction between the achlorophyllous gametophyte of Lycopodium clavatum L. And its fungal endophyte studied by light and electron-microscopy. New Phytol 124:69–81
Schmid E, Oberwinkler F (1994) Light and electron microscopy of the host– fungus interaction in the achlorophyllous gametophyte of Botrychium lunaria. Can J Bot 72:182–188
Schmid E, Oberwinkler F (1995) A light-and electron-microscopic study on a vesicular–arbuscular host-fungus interaction in gametophytes and young sporophytes of the Gleicheniaceae (Filicales). New Phytol 129:317–324
Schmid E, Oberwinkler F, Gomez LD (1995) Light and electron microscopy of a host-fungus interaction in the roots of some epiphytic ferns from Costa Rica. Can J Bot 73:991–996
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R (2004a) Ferns diversified in the shadow of angiosperms. Nature 428:553–557
Schneider H, Smith AR, Cranfill R, Hildebrand TE, Haufler CH, Ranker TA (2004b) Unraveling the phylogeny of polygrammoid ferns (Polypodiaceae and Grammitidaceae): exploring aspects of the diversification of epiphytic plants. Mol Phylogenet Evol 31:1041–1063
Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, et al. (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239
Schuettpelz E, Pryer KM (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050
Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. PNAS 106:11200–11205
Schuettpelz E, Schneider H, Huiet L, Windham MD, Pryer KM (2007) A molecular phylogeny of the fern family Pteridaceae: assessing overall relationships and the affinities of previously unsampled genera. Mol Phylogenet Evol 44:1172–1185
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiß M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878
Selosse MA, Strullu-Derrien C, Martin FM, Kamoun S, Kenrick P (2015) Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere. New Phytol 206(2):501–506
Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731
Strullu-Derrien C, Strullu DG (2007) Mycorrhization of fossil and living plants. Comptes Rendus Palevol 6(6):483–494
Strullu-Derrien C, Kenrick P, Pressel S, Duckett JG, Rioult JP, Strullu DG (2014) 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 Phytol 203(3):964–979
Sudha K, Ammani K (2010) Arbuscular mycorrhizal fungi in medicinal plants in Thrissur district, Kerala. Mycorrhiza News 21:13–18
Sundue M, Testo W, Ranker TA (2015) Morphological innovation, ecological opportunity, and the radiation of a major vascular epiphyte lineage. Evolution: Online first. doi:10.1111/evo.12749
Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87(4):560–573
Tian Q, Liu JK, Hyde KD, Wanasinghe DN, Boonmee S, Jayasiri SC, Luo ZL, Taylor JE, Phillips AJ, Bhat DJ, Li WJ (2015) Phylogenetic relationships and morphological reappraisal of Melanommataceae (Pleosporales). Fungal Divers 74:267–324
Tisserant B, Gianinazzi S, Gianinazzi-Pearson V (1996) Relationships between lateral root order, arbuscular mycorrhiza development, and the physiological state of the symbiotic fungus in Platanus acerifolia. Can J Bot 74:1947–1955
Tuomisto H, Poulsen AD, Moran RC (1998) Edaphic distribution of some species of the sern genus Adiantum in western Amazonia. Biotropica 30:392–399
Turnau K, Anielska T, Jurkiewicz A (2005) Mycothallic/mycorrhizal symbiosis of chlorophyllous gametophytes and sporophytes of a fern, Pellaea viridis (Forsk.) Prantl (Pellaeaceae, Pteridales). Mycorrhiza 15:121–128
van der Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423
Wäckers, E (1998) Untersuchungen zu Pilz-Wirtsinteraktionen in Wurzeln und Gametophyten von Pteridophyten. Ph.D. thesis, University of Tübingen, Germany. Published by the author; 156 pp
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
Wang B, Yeun L, Xue JY, Liu Y, Ané JM, Qiu YL (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonisation of land by plants. New Phytol 186:514–525
Watkins JE Jr, Cardelús CL (2012) Ferns in an angiosperm world: cretaceous radiation into the epiphytic niche and diversification on the forest floor. Int J Plant Sci 173:695–710
Wei N, Bemmels JB, Dick CW (2014) The effects of read length, quality and quantity on microsatellite discovery and primer development: from Illumina to PacBio. Mol Ecol Res 14:953–965
Wijayawardene NN, Hyde KD, Wanasinghe DN, Papizadeh M, Goonasekara ID, Camporesi E, Bhat DJ, McKenzie EH, Phillips AJ, Diederich P, Tanaka K (2016) Taxonomy and phylogeny of dematiaceous coelomycetes. Fungal Divers 77:1–316
Wilcke W, Yasin S, Valarezo C, Zech W (2001) Nutrient budget of three microcatchments under tropical montane forest in Ecuador-preliminary results. Erde 132(1):61–92
Wilkinson DM (2001) Mycorrhizal evolution. Trends Ecol Evol 16:64–65
Willis A, Rodrigues BF, Harris PJC (2013) The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 32:1–20
Winther JL, Friedman WE (2007a) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytol 177:790–801
Winther JL, Friedman WE (2007b) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255
Winther JL, Friedman WE (2009) Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. J Plant Res 122:485–496
Yukawa T, Ogura-Tsujita Y, Shefferson RP, Yokoyama J (2009) Mycorrhizal diversity in Apostasia (Orchidaceae) indicates the origin and evolution of orchid mycorrhiza. Am J Bot 96:1997–2009
Zhang Y, Guo LD, Liu RJ (2004) Arbuscular mycorrhizal fungi associated with common pteridophytes in Dujiangyan, Southwest China. Mycorrhiza 14:25–30
Zhao Z (2000) The arbuscular mycorrhizas of pteridophytes in Yunnan, Southwest China: evolutionary interpretations. Mycorrhiza 10:145–149
Zotz G (2013) The systematic distribution of vascular epiphytes–a critical update. Bot J Linn Soc 171:453–481
Zubek S, Piatek K, Naks P, Heise W, Wayda M, Mleczko P (2010) Fungal root endophyte colonization of fern and lycophyte species from the Celaque National Park in Honduras. Am Fern J 100:126–136
Acknowledgments
We thank Jürgen Kluge, Rayko Jonas, and Ramona Güdel for their participation in fieldwork and lab analyses.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lehnert, M., Krug, M. & Kessler, M. A review of symbiotic fungal endophytes in lycophytes and ferns – a global phylogenetic and ecological perspective. Symbiosis 71, 77–89 (2017). https://doi.org/10.1007/s13199-016-0436-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-016-0436-5