Orchid Mycorrhizal Interactions on the Pacific Side of the Andes from Chile. A Review

  • Héctor Herrera
  • Inmaculada García-Romera
  • Claudio Meneses
  • Guillermo Pereira
  • César ArriagadaEmail author


In order to confront the constant decline in global biological diversity, amelioration strategies are needed for threatened species to design reintroduction policies, particularly in plants with critical reproduction steps, such as orchids. Orchids are part of a highly diverse plant family, with several species under imminent extinction risk. This is the case of Chilean Orchidaceae, which has shown a constant decay in their populations due to an increase in the alteration processes of their natural distribution habitats. Successful orchid reintroductions require a full understanding of orchid mycorrhizal fungi and their dynamic according to different developmental stages and environmental conditions because orchid seeds need mycorrhizal fungi to obtain nutritional compounds at early developmental stages. This article performed a critical literature review of the ecological studies conducted on Chilean orchids and their relationships with mycorrhizal fungi in order to focus on the best scientific approach to achieve successful restoration programs involving orchid seeds and compatible mycorrhizal fungi.


Mycorrhiza Rhizoctonia-like fungi Andean orchids Mycoheterotrophy Seed germination 



This work was supported by the “Fondo Nacional de Desarrollo Científico y Tecnológico” of Chile (grant number 1170931 to C.A.) and the “Séptimo Concurso de Valorización de Investigacion en La Universidad, FONDEF VIU” of Chile (grant number 17E0185 to H.H.). This study is dedicated for the memory of the Professor of Environmental Microbiology, Yoav Bashan (1952–2018) of the Bashan Institute of Science, Auburn, USA.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. Abbott L, Manning D (2015) Soil health and related ecosystem services in organic agriculture. SAR 4:116CrossRefGoogle Scholar
  2. Aguilera P, Cornejo P, Borie F, Barea J, von Baer E, Oehl F (2014) Diversity of arbuscular mycorrhizal fungi associated with Triticum aestivum L. plants growing in an Andisol with high aluminum level. Agric Ecosyst Environ 186:178–184CrossRefGoogle Scholar
  3. Aguilera P, Cumming J, Oehl F, Cornejo P, Borie F (2015) Diversity of arbuscular mycorrhizal fungi in acidic soils and their contribution to aluminum phytotoxicity alleviation. In: Panda SK, Baluška F (eds) Aluminum stress adaption in plants. Springer, Cham, pp 203–228CrossRefGoogle Scholar
  4. Armesto J, Manuschevich D, Mora A, Smith-Ramirez C, Rozzi R, Abarzúa A, Marquet P (2010) From the Holocene to the Anthropocene: a historical framework for land cover change in southwestern South America in the past 15,000 years. Land Use Policy 27:148–160CrossRefGoogle Scholar
  5. Atala, C., Pereira, G., Romero, C., Muñoz-Tapia, L., Vargas, R., Suz, L.M. 2015. Orchidioid fungi of the form-genus Rhizoctonia associated with the roots of Chloraea cuneata Lindl. from Araucanía. Gayana Bot 72, 145Google Scholar
  6. Athipunyakom P, Manoch L, Piluek C (2004) Isolation and identification of mycorrhizal fungi from eleven terrestrial orchids. Kasetsart J (Nat Sci) 38:216–228Google Scholar
  7. Barea J, Jeffries P (1995) Arbuscular mycorrhizas in sustainable soil-plant systems. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin Heidelberg, pp 521–560CrossRefGoogle Scholar
  8. Barrett C, Freudenstein J, Lee Taylor D, Kõljalg U (2010) Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. Am J Bot 97:628–643CrossRefPubMedGoogle Scholar
  9. Batty A, Brundrett M, Dixon K, Sivasithamparam K (2006a) In situ symbiotic seed germination and propagation of terrestrial orchid seedlings for establishment at field sites. Austral J Bot 54:375–381CrossRefGoogle Scholar
  10. Batty A, Brundrett M, Dixon K, Sivasithamparam K (2006b) New methods to improve symbiotic propagation of temperate terrestrial orchid seedlings from axenic culture to soil. Austral J Bot 54:367–374CrossRefGoogle Scholar
  11. Batty A, Dixon K, Brundrett M, Sivasithamparam K (2001) Long-term storage of mycorrhizal fungi and seed as a tool for the conservation of endangered Western Australian terrestrial orchids. Austral J Bot 49:619–628CrossRefGoogle Scholar
  12. Bayman P, Otero J (2006) Microbial endophytes of orchid roots. In: Schulz B, Boyle C, Sieber T (eds) Microbial root endophytes. Springer, New York, pp 153–173CrossRefGoogle Scholar
  13. Bidartondo M, Burghardt B, Gebauer G, Bruns T, Read D (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc Lond B Biol Sci 271:1799–1806CrossRefGoogle Scholar
  14. Bidartondo M, Read D (2008) Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17:3707–3716PubMedGoogle Scholar
  15. 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 111:51–61CrossRefPubMedGoogle Scholar
  16. Bougoure J, Ludwig M, Brundrett M, Cliff J, Clode P, Kilburn M, Grierson P (2014) High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid. Plant Cell Environ 37:1223–1230CrossRefPubMedGoogle Scholar
  17. Bravo-Monasterio P, Baeza-Horta G, Penailillo P, Alarcon D, Contreras D (2014) Una nueva especie del género Bipinnula (Orchidaceae) para Chile. Gayana Bot 71:131–139CrossRefGoogle Scholar
  18. Brundrett M (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304CrossRefGoogle Scholar
  19. Brundrett M, Scade A, Batty A, Dixon K, Sivasithamparam K (2003) Development of in situ and ex situ seed baiting techniques to detect mycorrhizal fungi from terrestrial orchid habitats. Mycol Res 107:1210–1220CrossRefPubMedGoogle Scholar
  20. Cameron D, Johnson I, Read D, Leake J (2008) Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytol 180:176–184CrossRefPubMedGoogle Scholar
  21. Cameron D, Leake J, Read D (2006) Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytol 171:405–416CrossRefPubMedGoogle Scholar
  22. Castillo C, Borie F, Godoy R, Rubio R, Sieverding E (2006) Diversity of mycorrhizal plant species and arbuscular mycorrhizal fungi in evergreen forest, deciduous forest and grassland ecosystems of Southern Chile. J Appl Bot Food Qual 80:40–47Google Scholar
  23. Cisternas M, Salazar G, Verdugo G, Novoa P, Calderon X, Negritto M (2012) Phylogenetic analysis of Chloraeinae (Orchidaceae) based on plastid and nuclear DNA sequences. Bot J Linn Soc 168:258–277CrossRefGoogle Scholar
  24. Clements M, Muir H, Cribb P (1986) A preliminary report on the symbiotic germination of European terrestrial orchids. Kew Bull 41:437–445CrossRefGoogle Scholar
  25. Cowden C, Shefferson R (2013) Diversity of root-associated fungi of mature Habenaria radiata and Epipactis thunbergii colonizing manmade wetlands in Hiroshima Prefecture, Japan. Mycoscience 54:327–334CrossRefGoogle Scholar
  26. Cozzolino S, Nardella A, Impagliazzo S, Widmer A, Lexer C (2006) Hybridization and conservation of Mediterranean orchids: should we protect the orchid hybrids or the orchid hybrid zones? Biol Conserv 129:14–23CrossRefGoogle Scholar
  27. Crasta G, Bopaiah A (2017) In vivo germination of encapsulated orchid seeds of Epidendrum radicans. Asian J Biotechnol Bioresour Technol 2:1–4CrossRefGoogle Scholar
  28. Chen W, Chen H (2011) Orchid biotechnology II. World Scientific Publishing Co, Singapore 356 pCrossRefGoogle Scholar
  29. Chen J, Liu S, Kohler A, Yan B, Luo H, Chen X, Guo S (2017) iTRAQ and RNA-Seq analyses provide new insights into regulation mechanism of symbiotic germination of Dendrobium officinale seeds (Orchidaceae). J Proteome Res 16:2174–2187CrossRefPubMedGoogle Scholar
  30. Chen J, Wang H, Guo S (2012) Isolation and identification of endophytic and mycorrhizal fungi from seeds and roots of Dendrobium (Orchidaceae). Mycorrhiza 22:297–307CrossRefPubMedGoogle Scholar
  31. Chen W, Tang C, Kao Y (2009) Ploidy doubling by in vitro culture of excised protocorms or protocorm-like bodies in Phalaenopsis species. Plant Cell Tissue Organ Cult 98:229–238CrossRefGoogle Scholar
  32. da Silva J (2013) Orchids: advances in tissue culture, genetics, phytochemistry and transgenic biotechnology. Floriculture Ornamental Biotech 7:1–52Google Scholar
  33. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou A, Hiiesalu I, Jairus T (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973CrossRefPubMedGoogle Scholar
  34. Dearnaley J, Perotto S, Selosse M (2016) Structure and development of orchid mycorrhizas. In: Martin F (ed) Molecular mycorrhizal symbiosis. Springer-Verlag, Berlin, pp 63–86CrossRefGoogle Scholar
  35. Dearnaley J (2007) Further advances in orchid mycorrhizal research. Mycorrhiza 17:475–486CrossRefPubMedGoogle Scholar
  36. Dutra D, Johnson T, Kauth P, Stewart S, Kane M, Richardson L (2008) Asymbiotic seed germination, in vitro seedling development, and greenhouse acclimatization of the threatened terrestrial orchid Bletia purpurea. Plant Cell Tissue Organ Cult 94:11–21CrossRefGoogle Scholar
  37. Dutra D, Kane M, Richardson L (2009) Asymbiotic seed germination and in vitro seedling development of Cyrtopodium punctatum: a propagation protocol for an endangered Florida native orchid. Plant Cell Tissue Organ Cult 96:235–243CrossRefGoogle Scholar
  38. Egidi E, May T, Franks A (2018) Seeking the needle in the haystack: undetectability of mycorrhizal fungi outside of the plant rhizosphere associated with an endangered Australian orchid. Fungal Ecol 33:13–23CrossRefGoogle Scholar
  39. Ercole E, Adamo M, Rodda M, Gebauer G, Girlanda M, Perotto S (2015) Temporal variation in mycorrhizal diversity and carbon and nitrogen stable isotope abundance in the wintergreen meadow orchid Anacamptis morio. New Phytol 205:1308–1319CrossRefPubMedGoogle Scholar
  40. Ercole E, Rodda M, Molinatti M, Voyron S, Perotto S, Girlanda M (2013) Cryopreservation of orchid mycorrhizal fungi: a tool for the conservation of endangered species. J Microbiol Methods 93:134–137CrossRefPubMedGoogle Scholar
  41. Fay M (1992) Conservation of rare and endangered plants using in vitro methods. In Vitro Cell Dev Biol Plant 28:1–4CrossRefGoogle Scholar
  42. Fay M, Feustel M, Newlands C, Gebauer G (2018) Inferring the mycorrhizal status of introduced plants of Cypripedium calceolus (Orchidaceae) in northern England using stable isotope analysis. Bot J Linn Soc 186:587–590CrossRefGoogle Scholar
  43. FIA. (2018) Fundación Para la Innovación Agraria. Ministerio de Agricultura. Published on the internet at Retrieved on 22 May 2018
  44. Fochi V, Chitarra W, Kohler A, Voyron S, Singan V, Lindquist E, Barry K, Girlanda M, Grigoriev I, Martin F (2017) Fungal and plant gene expression in the Tulasnella calosporaSerapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas. New Phytol 213:365–379CrossRefPubMedGoogle Scholar
  45. Fracchia S, Aranda-Rickert A, Flachsland E, Terada G, Sede S (2014a) Mycorrhizal compatibility and symbiotic reproduction of Gavilea australis, an endangered terrestrial orchid from south Patagonia. Mycorrhiza 24:627–634CrossRefPubMedGoogle Scholar
  46. Fracchia S, Aranda-Rickert A, Rothen C, Sede S (2016) Associated fungi, symbiotic germination and in vitro seedling development of the rare Andean terrestrial orchid Chloraea riojana. Flora 224:106–111CrossRefGoogle Scholar
  47. Fracchia S, Silvani V, Flachsland E, Terada G (2014b) Symbiotic seed germination and protocorm development of Aa achalensis Schltr., a terrestrial orchid endemic from Argentina. Mycorrhiza 24:35–43CrossRefGoogle Scholar
  48. Gale S, Fischer G, Cribb P, Fay M (2018) Orchid conservation: bridging the gap between science and practice. Bot J Linn Soc 186:425–434CrossRefGoogle Scholar
  49. Gantait S, Bustam S, Sinniah U (2012) Alginate-encapsulation, short-term storage and plant regeneration from protocorm-like bodies of Aranda Wan Chark Kuan ‘Blue’× Vanda coerulea Grifft. ex. Lindl. (Orchidaceae). Plant Growth Regul 68:303–311CrossRefGoogle Scholar
  50. Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol 160:209–223CrossRefGoogle Scholar
  51. Gebauer G, Preiss K, Gebauer AC (2016) Partial mycoheterotrophy is more widespread among orchids than previously assumed. New Phytol 211:11–15CrossRefPubMedGoogle Scholar
  52. Giovannetti M, Volpe V, Salvioli A, Bonfante P (2017) Fungal and plant tools for the uptake of nutrients in arbuscular mycorrhizas. In: Gehring G, Jansa J (eds) Johnson, N. Elsevier, Mycorrhizal Mediation of Soil, pp 107–128Google Scholar
  53. Girlanda M, Segreto R, Cafasso D, Liebel H, 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 98:1148–1163CrossRefPubMedGoogle Scholar
  54. Govaerts R, Bernet P, Kratochvil K, Gerlach G, Carr G, Alrich P, Pridgeon A, Pfahl J, Campacci M, Holland Baptista D (2016) World Checklist of Orchidaceae. Facilitated by the Royal Botanic Gardens. In: KewGoogle Scholar
  55. Herrera H, Valadares R, Oliveira G, Fuentes A, Almonacid L, do Nascimento S, Bashan Y, Arriagada C (2018) Adaptation and tolerance mechanisms developed by mycorrhizal Bipinnula fimbriata plantlets (Orchidaceae) in a heavy metal-polluted ecosystem. Mycorrhiza 28:651–663CrossRefPubMedGoogle Scholar
  56. Herrera H, Valadares R, Contreras D, Bashan Y, Arriagada C (2017) Mycorrhizal compatibility and symbiotic seed germination of orchids from the coastal range and Andes in south central Chile. Mycorrhiza 27:175–188CrossRefPubMedGoogle Scholar
  57. Hosomi S, Santos R, Custodio C, Seaton P, Marks T, Machado-Neto N (2011) Preconditioning Cattleya seeds to improve the efficacy of the tetrazolium test for viability. Seed Sci Technol 39:178–189CrossRefGoogle Scholar
  58. Hosomi S, Custódio C, Seaton P, Marks T, Machado-Neto N (2012) Improved assessment of viability and germination of Cattleya (Orchidaceae) seeds following storage. In Vitro Cell Dev Biol Plant 48:127–136CrossRefGoogle Scholar
  59. Hou X, Guo S (2009) Interaction between a dark septate endophytic isolate from Dendrobium sp. and roots of D. nobile seedlings. J Integr Plant Biol 51:374–381CrossRefPubMedGoogle Scholar
  60. IUCN. (2018). The IUCN Red List of Threatened Species, version 2017-2. Published on the internet at Retrieved on 21 May 2018
  61. IUCN/SSC Orchid Specialist Group (1996) Orchids – status survey and conservation action plan. In: Gland and Cambridge: IUCNGoogle Scholar
  62. Jacquemyn H, Brys R, Waud M, Busschaert P, Lievens B (2015) Mycorrhizal networks and coexistence in species-rich orchid communities. New Phytol 206:1127–1134CrossRefPubMedGoogle Scholar
  63. Jacquemyn H, Duffy K, Selosse M (2017) Biogeography of orchid mycorrhizas. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer Cham, Switzerland, pp 159–177CrossRefGoogle Scholar
  64. Jacquemyn H, Waud M, Lievens B, Brys R (2016) Differences in mycorrhizal communities between Epipactis palustris, E. helleborine and its presumed sister species E. neerlandica. Ann Bot 118:105–114CrossRefPubMedPubMedCentralGoogle Scholar
  65. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16Google Scholar
  66. Jersáková J, Malinová T (2007) Spatial aspects of seed dispersal and seedling recruitment in orchids. New Phytol 176:237–241CrossRefPubMedGoogle Scholar
  67. Jiang J, Moore J, Priyadarshi A, Classen A (2017) Plant-mycorrhizal interactions mediate plant community coexistence by altering resource demand. Ecology 98:187–197CrossRefPubMedGoogle Scholar
  68. Johnson T, Stewart S, Dutra D, Kane M, Richardson L (2007) Asymbiotic and symbiotic seed germination of Eulophia alta (Orchidaceae)—preliminary evidence for the symbiotic culture advantage. Plant Cell Tissue Organ Cult 90:313CrossRefGoogle Scholar
  69. Jurkiewicz A, Turnau K, Mesjasz-Przybyłowicz J, Przybyłowicz W, Godzik B (2001) Heavy metal localization in mycorrhizas of Epipactis atrorubens (Hoffm.) Besser (Orchidaceae) from zinc mine tailings. Protoplasma 218:117–124CrossRefPubMedGoogle Scholar
  70. Kaur H, Garg N (2017) Zinc-arbuscular mycorrhizal interactions: effect on nutrient pool, enzymatic antioxidants, and osmolyte synthesis in pigeonpea nodules subjected to cd stress. Commun Soil Sci Plant Anal 48:1684–1700CrossRefGoogle Scholar
  71. Kennedy M, Hedin L, Derry L (2002) Decoupling of unpolluted temperate forests from rock nutrient sources revealed by natural 87Sr/86Sr and 84Sr tracer addition. Proc Natl Acad Sci U S A 99:9639–9644CrossRefPubMedPubMedCentralGoogle Scholar
  72. Khamchatra N, Dixon K, Chayamarit K, Apisitwanich S, Tantiwiwat S (2016a) Using in situ seed baiting technique to isolate and identify endophytic and mycorrhizal fungi from seeds of a threatened epiphytic orchid, Dendrobium friedericksianum Rchb. f. (Orchidaceae). Kasetsart J (Nat Sci) 50:8–13Google Scholar
  73. Khamchatra N, Dixon K, Tantiwiwat S, Piapukiew J (2016b) Symbiotic seed germination of an endangered epiphytic slipper orchid, Paphiopedilum villosum (Lindl.) Stein. from Thailand. S African J Bot 104:76–81CrossRefGoogle Scholar
  74. Kottke I, Suárez J, Herrera P, Cruz D, Bauer R, Haug I, Garnica S (2010) Atractiellomycetes belonging to the ‘rust’lineage (Pucciniomycotina) form mycorrhizae with terrestrial and epiphytic neotropical orchids. Proc R Soc Lond B Biol Sci 277:1289–1298CrossRefGoogle Scholar
  75. Kuga Y, Sakamoto N, Yurimoto H (2014) Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms. New Phytol 202:594–605CrossRefPubMedGoogle Scholar
  76. Leake J (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216CrossRefGoogle Scholar
  77. Lee Y, Lu C, Chung M, Yeung E, Lee N (2007) Developmental changes in endogenous abscisic acid concentrations and asymbiotic seed germination of a terrestrial orchid, Calanthe tricarinata Lindl. J Am Soc Hortic Sci 132:246–252CrossRefGoogle Scholar
  78. Li D, Pritchard H (2009) The science and economics of ex situ plant conservation. Trends Plant Sci 14:614–621CrossRefPubMedGoogle Scholar
  79. Li Y, Chan C, Stahl C, Yeung E (2018) Recent Advances in Orchid Seed Germination and Micropropagation. In: Lee, Y., Yeung, E. (eds,) Orchid Propagation: From Laboratories to Greenhouses—Methods and Protocols. Springer Science, New York, pp: 497-520Google Scholar
  80. Luo J, Wawrosch C, Kopp B (2009) Enhanced micropropagation of Dendrobium huoshanense CZ Tang et SJ Cheng through protocorm-like bodies: the effects of cytokinins, carbohydrate sources and cold pretreatment. Sci Hortic 123:258–262CrossRefGoogle Scholar
  81. Marín C, Aguilera P, Oehl F, Godoy R (2017) Factors affecting arbuscular mycorrhizal fungi of Chilean temperate rainforests. J Soil Sci Plant Nutr 17:966–984CrossRefGoogle Scholar
  82. Martin K (2003) Clonal propagation, encapsulation and reintroduction of Ipsea malabarica (Reichb. f.) JD Hook., an endangered orchid. In Vitro Cell Dev Biol Plant 39:322–326CrossRefGoogle Scholar
  83. McCarty J (2001) Ecological consequences of recent climate change. Conserv Biol 15:320–331CrossRefGoogle Scholar
  84. McCormick M, Taylor D, Whigham D, Burnett R (2016) Germination patterns in three terrestrial orchids relate to abundance of mycorrhizal fungi. J Ecol 104:744–754CrossRefGoogle Scholar
  85. McCormick M, Whigham D, O'neill J (2004) Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytol 163:425–438CrossRefGoogle Scholar
  86. McCormick M, Whigham D, Sloan D, O'Malley K, Hodkinson B (2006) Orchid–fungus fidelity: a marriage meant to last? Ecology 87:903–911CrossRefPubMedGoogle Scholar
  87. Mehra S, Morrison P, Coates F, Lawrie A (2017) Differences in carbon source utilization by orchid mycorrhizal fungi from common and endangered species of Caladenia (Orchidaceae). Mycorrhiza 27:95–108CrossRefPubMedGoogle Scholar
  88. Mujica M, Saez N, Cisternas M, Manzano M, Armesto J, Pérez F (2016) Relationship between soil nutrients and mycorrhizal associations of two Bipinnula species (Orchidaceae) from central Chile. Ann Bot 118:149–158CrossRefPubMedPubMedCentralGoogle Scholar
  89. Mweetwa A, Welbaum G, Tay D (2008) Effects of development, temperature, and calcium hypochlorite treatment on in vitro germinability of Phalaenopsis seeds. Sci Hortic 117:257–262CrossRefGoogle Scholar
  90. Novoa P, Espejo J, Cisternas M, Rubio M, Dominguez E (2015) Guía de campo de las orquídeas chilenas. Segunda edición ampliada. Corporación Chilena de la Madera (CORMA), Santiago, 123p.Google Scholar
  91. Novotná A, Benítez Á, Herrera P, Cruz D, Filipczyková E, Suárez J (2018) High diversity of root-associated fungi isolated from three epiphytic orchids in southern Ecuador. Mycoscience 59:24–32CrossRefGoogle Scholar
  92. Oberwinkler F, Cruz D, Suárez J (2017) Biogeography and ecology of Tulasnellaceae. In: Tedersoo, L. (ed.). Biogeography of Mycorrhizal Symbiosis. Springer Cham, pp: 237–271Google Scholar
  93. 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 99:1158–1176CrossRefPubMedGoogle Scholar
  94. Oja J, Kohout P, Tedersoo L, Kull T, Kõljalg U (2015) Temporal patterns of orchid mycorrhizal fungi in meadows and forests as revealed by 454 pyrosequencing. New Phytol 205:1608–1618CrossRefPubMedGoogle Scholar
  95. Otero J, Ackerman J, Bayman P (2002) Diversity and host specificity of endophytic Rhizoctonia-like fungi from tropical orchids. Am J Bot 89:1852–1858CrossRefGoogle Scholar
  96. Otero J, Ackerman J, Bayman P (2004) Differences in mycorrhizal preferences between two tropical orchids. Mol Ecol 13:2393–2404CrossRefPubMedGoogle Scholar
  97. Palfner G (2001) Taxonomische Studien an Ektomykorrhizen aus den-Nothofagus-Wäldern Mittelsüdchiles. Bibl Mycol 190:1–243Google Scholar
  98. Pecoraro L, Caruso T, Cai L, Gupta V, Liu Z (2018) Fungal networks and orchid distribution: new insights from above-and below-ground analyses of fungal communities. IMA fungus 9:1–11CrossRefPubMedPubMedCentralGoogle Scholar
  99. Pereira G, Albornoz V, Muñoz-Tapia L, Romero C, Atala C (2015) Asymbiotic germination of Bipinnula fimbriata (Orchidaceae) seeds in different culture media. Seed Sci Technol 43:367–377CrossRefGoogle Scholar
  100. Pereira G, Albornoz V, Romero C, Lara S, Sánchez-Olate M, Ríos D, Atala C (2017) Asymbiotic germination in three Chloraea species (Orchidaceae) from Chile. Gayana Bot 74:1–9Google Scholar
  101. Pereira G, Romero C, Suz L, Atala C (2014b) Essential mycorrhizal partners of the endemic Chilean orchids Chloraea collicensis and C. gavilu. Flora 209:95–99CrossRefGoogle Scholar
  102. Pereira G, Suz L, Albornoz V, Romero C, García L, Leiva V, Atala C (2018) Hongos micorrícicos asociados a Codonorchis lessonii (Brongn.) Lindl., una orquídea terrestre de Chile. Gayana Bot 75:447–458CrossRefGoogle Scholar
  103. Pereira M, da Silva Coelho I, Valadares R, Oliveira S, Bocayuva M, Pereira O, Araújo E, Kasuya M (2014a) Morphological and molecular characterization of Tulasnella spp. fungi isolated from the roots of Epidendrum secundum, a widespread Brazilian orchid. Symbiosis 62:111–121CrossRefGoogle Scholar
  104. Perotto S, Rodda M, Benetti A, Sillo F, Ercole E, Rodda M, Girlanda M, Murat C, Balestrini R (2014) Gene expression in mycorrhizal orchid protocorms suggests a friendly plant–fungus relationship. Planta 239:1337–1349CrossRefPubMedGoogle Scholar
  105. Peterson R, Uetake Y, Bonfante P, Faccio A (1996) The interface between fungal hyphae and orchid protocorm cells. Can J Bot 74:1861–1870CrossRefGoogle Scholar
  106. Popova E, Kim H, Saxena P, Engelmann F, Pritchard HW (2016) Frozen beauty: the cryobiotechnology of orchid diversity. Biotechnol Adv 34:380–403CrossRefPubMedGoogle Scholar
  107. Pridgeon, A., Cribb, P., Chase, M., Rasmussen, F. 1999. Genera Orchidacearum. Vol 1. General Introduction. Apostasioideae. Cypripedioideae. Oxford University Press, OxfordGoogle Scholar
  108. Ramsay M, Dixon K (2003) Propagation science, recovery and translocation of terrestrial orchids. In: Dixon K, Cribb P, Kell S, Barrett R (eds) Orchid conservation. Kota Kinabalu, Sabah. Natural History Publications, Malaysia, pp 259–288Google Scholar
  109. Rasmussen H (1995) Terrestrial orchids: from seed to mycotrophic plant. Cambridge University Press, Cambridge, UK 444 pCrossRefGoogle Scholar
  110. Rasmussen H, Rasmussen F (2009) Orchid mycorrhiza: implications of a mycophagous life style. Oikos 118:334–345CrossRefGoogle Scholar
  111. Rasmussen H, Whigham D (1993) Seed ecology of dust seeds in situ: a new study technique and its application in terrestrial orchids. Am J Bot:1374–1378Google Scholar
  112. Robbirt K, Davy A, Hutchings M, Roberts D (2011) Validation of biological collections as a source of phenological data for use in climate change studies: a case study with the orchid Ophrys sphegodes. J Ecol 99:235–241CrossRefGoogle Scholar
  113. Roberts D, Dixon K (2008) Orchids. Curr Biol 18:R325–R329CrossRefPubMedGoogle Scholar
  114. Romero C (2012) Orquídeas de Nahuelbuta, Símbolo de la Comuna de Angol. Chile, Fondo de Protección Ambiental, Ministerio de Medioambiente, Gobierno de ChileGoogle Scholar
  115. Romero C, Cuba-Díaz M, Silva R (2017) In vitro culture of Chloraea gavilu Lindl., an endemic terrestrial orchid from Chile. Plant Biosyst 152:612–620CrossRefGoogle Scholar
  116. Roy M, Watthana S, Stier A, Richard F, Vessabutr S, Selosse M (2009) Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biol 7:51CrossRefPubMedPubMedCentralGoogle Scholar
  117. Sarasan V, Cripps R, Ramsay M, Atherton C, McMichen M, Prendergast G, Rowntree J (2006) Conservation in vitro of threatened plants–progress in the past decade. In Vitro Cell Dev Biol Plant 42:206–214CrossRefGoogle Scholar
  118. Schödelbauerová I, Roberts D, Kindlmann P (2009) Size of protected areas is the main determinant of species diversity in orchids. Biol Conserv 142:2329–2334CrossRefGoogle Scholar
  119. Schofield E, Jones E, Sarasan V (2018) Cryopreservation without vitrification suitable for large scale cryopreservation of orchid seeds. Bot Stud 59:13CrossRefPubMedPubMedCentralGoogle Scholar
  120. Seaton P, Hu H, Perner H, Pritchard H (2010) Ex situ conservation of orchids in a warming world. Bot Rev 76:193–203CrossRefGoogle Scholar
  121. Selosse M (2014) The latest news from biological interactions in orchids: in love, head to toe. New Phytol 202:337–340CrossRefPubMedGoogle Scholar
  122. Shefferson R, Kull T, Tali K (2008) Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills. Am J Bot 95:156–164CrossRefPubMedGoogle Scholar
  123. Shefferson R, Weiss M, Kull T, Taylor D (2005) High specificity generally characterizes mycorrhizal association in rare lady’s slipper orchids, genus Cypripedium. Mol Ecol 14:613–626CrossRefPubMedGoogle Scholar
  124. Shimura H, Koda Y (2005) Enhanced symbiotic seed germination of Cypripedium macranthos var. rebunense following inoculation after cold treatment. Physiol Plant 123:281–287CrossRefGoogle Scholar
  125. Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31CrossRefGoogle Scholar
  126. Smith S, Read D (2010) Mycorrhizal symbiosis, vol 3. Elsevier Science, London, United KingdomGoogle Scholar
  127. Smith S, Smith F, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20CrossRefPubMedPubMedCentralGoogle Scholar
  128. Sommerville K, Siemon J, Wood C, Offord C (2008) Simultaneous encapsulation of seed and mycorrhizal fungi for long-term storage and propagation of terrestrial orchids. Austral J Bot 56:609–615CrossRefGoogle Scholar
  129. Steinfort U, Verdugo G, Besoain X, Cisternas M (2010) Mycorrhizal association and symbiotic germination of the terrestrial orchid Bipinnula fimbriata (Poepp.) Johnst (Orchidaceae). Flora 205:811–817CrossRefGoogle Scholar
  130. Stewart S, Zettler L, Minso J, Brown P (2003) Symbiotic germination and reintroduction of Spiranthes brevilabris Lindley, an endangered orchid native to Florida. Selbyana 24:64–70Google Scholar
  131. Swarts N, Dixon K (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:543–556CrossRefPubMedPubMedCentralGoogle Scholar
  132. Swarts N, Sinclair E, Francis A, Dixon K (2010) Ecological specialization in mycorrhizal symbiosis leads to rarity in an endangered orchid. Mol Ecol 19:3226–3242CrossRefPubMedGoogle Scholar
  133. Tešitelová T, Tešitel J, Jersáková J, Ríhová G, Selosse M (2012) Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology. Am J Bot 99:1020–1032CrossRefPubMedGoogle Scholar
  134. Thammasiri K (2008) Cryopreservation of some Thai orchid species. Acta Hortic 788:53–62CrossRefGoogle Scholar
  135. The Plant List. 2013. The plant list, version 1. Published on the internet at Retrieved on 22 May 2018
  136. Thomsen P, Willerslev E (2015) Environmental DNA–an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18CrossRefGoogle Scholar
  137. Tsai W, Dievart A, Hsu C, Hsiao Y, Chiou S, Huang H, Chen H (2017) Post genomics era for orchid research. Bot Stud 58:61CrossRefPubMedPubMedCentralGoogle Scholar
  138. Valadares R, Perotto S, Santos E, Lambais M (2014) Proteome changes in Oncidium sphacelatum (Orchidaceae) at different trophic stages of symbiotic germination. Mycorrhiza 24:349–360CrossRefPubMedGoogle Scholar
  139. Valadares R, Pereira M, Otero J, Cardoso E (2012) Narrow fungal mycorrhizal diversity in a population of the orchid Coppensia doniana. Biotropica 44:114–122CrossRefGoogle Scholar
  140. Valadares R (2014) Identification of genes and proteins involved in the regulation of orchid mycorrhiza. In: Dissertation. University of São Paulo, PiracicabaGoogle Scholar
  141. Verdugo G, Marchant J, Cisternas M, Calderón X, Peñaloza P (2007) Caracterización morfométrica de la germinación de Chloraea crispa lindl. (Orchidaceae) usando un análisis de imagen. Gayana Bot 64:232–238CrossRefGoogle Scholar
  142. Wang H, Fang H, Wang Y, Duan L, Guo S (2011) In situ seed baiting techniques in Dendrobium officinale Kimuraet Migo and Dendrobium nobile Lindl.: the endangered Chinese endemic Dendrobium (Orchidaceae). World J Microbiol Biotechnol 27:2051–2059CrossRefGoogle Scholar
  143. Wang X, Li Y, Song X, Meng Q, Zhu J, Zhao J, Yu W (2017) Influence of host tree species on isolation and communities of mycorrhizal and endophytic fungi from roots of a tropical epiphytic orchid, Dendrobium sinense (Orchidaceae). Mycorrhiza 27:709–718CrossRefPubMedGoogle Scholar
  144. Waterman R, Bidartondo M (2008) Deception above, deception below: linking pollination and mycorrhizal biology of orchids. J Exp Bot 59:1085–1096CrossRefPubMedGoogle Scholar
  145. Waud M, Busschaert P, Lievens B, Jacquemyn H (2016a) Specificity and localised distribution of mycorrhizal fungi in the soil may contribute to co-existence of orchid species. Fungal Ecol 20:155–165CrossRefGoogle Scholar
  146. Waud M, Busschaert P, Ruyters S, Jacquemyn H, Lievens B (2014) Impact of primer choice on characterization of orchid mycorrhizal communities using 454 pyrosequencing. Mol Ecol Resour 14:679–699CrossRefPubMedGoogle Scholar
  147. Waud M, Wiegand T, Brys R, Lievens B, Jacquemyn H (2016b) Nonrandom seedling establishment corresponds with distance-dependent decline in mycorrhizal abundance in two terrestrial orchids. New Phytol 211:255–264CrossRefPubMedGoogle Scholar
  148. Wood C, Pritchard H, Miller A (2000) Simultaneous preservation of orchid seed and its fungal symbiont using encapsulation-dehydration is dependent on moisture content and storage temperature. Cryo letters 21:125–136PubMedGoogle Scholar
  149. Xing X, Gai X, Liu Q, Hart M, Guo S (2015) Mycorrhizal fungal diversity and community composition in a lithophytic and epiphytic orchid. Mycorrhiza 25:289–296CrossRefPubMedGoogle Scholar
  150. Xing X, Ma X, Deng Z, Chen J, Wu F, Guo S (2013) Specificity and preference of mycorrhizal associations in two species of the genus Dendrobium (Orchidaceae). Mycorrhiza 23:317–324CrossRefPubMedGoogle Scholar
  151. Xu X, Ma X, Lei H, Song H, Ying Q, Xu M, Liu S, Wang H (2015) Proteomic analysis reveals the mechanisms of Mycena dendrobii promoting transplantation survival and growth of tissue culture seedlings of Dendrobium officinale. J Appl Microbiol 118:1444–1455CrossRefPubMedGoogle Scholar
  152. Yam T, Arditti J (2009) History of orchid propagation: a mirror of the history of biotechnology. Plant Biotechnol Rep 3:1CrossRefGoogle Scholar
  153. Yamato M, Yagame T, Suzuki A, Iwase K (2005) Isolation and identification of mycorrhizal fungi associating with an achlorophyllous plant, Epipogium roseum (Orchidaceae). Mycoscience 46:73–77CrossRefGoogle Scholar
  154. Yamazaki J, Miyoshi K (2006) In vitro asymbiotic germination of immature seed and formation of protocorm by Cephalanthera falcata (Orchidaceae). Ann Bot 98:1197–1206CrossRefPubMedPubMedCentralGoogle Scholar
  155. Yeung E (2017) A perspective on orchid seed and protocorm development. Bot Stud 58:33CrossRefPubMedPubMedCentralGoogle Scholar
  156. Zeng X, Li Y, Ling H, Chen J, Guo S (2018) Revealing proteins associated with symbiotic germination of Gastrodia elata by proteomic analysis. Bot Stud 59:8CrossRefPubMedPubMedCentralGoogle Scholar
  157. Zettler L (1997) Terrestrial orchid conservation by symbiotic seed germination: techniques and perspectives. Selbyana 18:188–194Google Scholar
  158. Zettler, L., Sharma, J., Rasmussen, F.P. 2003. Mycorrhizal diversity. In: Dixon, K., Cribb, P., Kell, S., Barrett, R. (eds.) Orchid Conservation. Kota Kinabalu, Sabah, Malaysia: Natural History Publications, pp:185–203Google Scholar
  159. Zi X, Sheng C, Goodale U, Shao S, Gao J (2014) In situ seed baiting to isolate germination-enhancing fungi for an epiphytic orchid, Dendrobium aphyllum (Orchidaceae). Mycorrhiza 24:487–499CrossRefPubMedGoogle Scholar
  160. Zimmer K, Meyer C, Gebauer G (2008) The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytol 178:395–400CrossRefPubMedGoogle Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  • Héctor Herrera
    • 1
  • Inmaculada García-Romera
    • 2
  • Claudio Meneses
    • 3
  • Guillermo Pereira
    • 4
  • César Arriagada
    • 1
    Email author
  1. 1.Laboratorio de Biorremediación, Facultad de Ciencias Agropecuarias y Forestales, Departamento de Ciencias ForestalesUniversidad de La FronteraTemucoChile
  2. 2.Estación Experimental del ZaidínGranadaSpain
  3. 3.Centro de Biotecnología VegetalUniversidad Andres BelloSantiagoChile
  4. 4.Laboratorio Biotecnología de Hongos, Departamento de Ciencias y Tecnología Vegetal, Campus Los ÁngelesUniversidad de ConcepciónLos AngelesChile

Personalised recommendations