Mycorrhizal diversity in Apostasia (Orchidaceae)indicates the origin and evolution of orchid mycorrhiza

American Journal of Botany

Volumn 96, Issue 11, 2009, Pages 1997-2009

  Yukawa, Tomohisa ^a   Ogura Tsujita, Yuki ^a   Shefferson, Richard P ^b   Yokoyama, Jun ^c  

^a DEPARTMENT OF BOTANY   (Japan)

^b UNIVERSITY OF GEORGIA   (United States)

^c YAMAGATA UNIVERSITY   (Japan)

Author keywords

Apostasia; Asparagales; Basidiomycota; Botryobasidiaceae; Cantharellales; Ceratobasidiaceae; Evolution; Mycorrhiza; Orchidaceae

Indexed keywords

CLADISTICS; COMMON ANCESTRY; DIVERSITY INDEX; DNA; EVOLUTIONARY BIOLOGY; FUNGUS; HERB; MOLECULAR ANALYSIS; MYCORRHIZA; SYMBIOSIS; TAXONOMY;

APOSTASIA; ARBUSCULAR; ASPARAGALES; BASIDIOMYCOTA; BOTRYOBASIDIACEAE; CANTHARELLALES; CERATOBASIDIACEAE; COMMELINIDS; FUNGI; GLOMEROMYCOTA; ORCHIDACEAE;

EID: 70350716386     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.0900101     Document Type: Article

References (87)

1. Abadie, J. C., Ü. Püttsepp, G. Gebauer, A. Faccio, P. Bonfante, and M. A. Selosse. 2006. Cephalanthera longifolia (Neottieae, Orchidaceae) is mixotrophic: A comparative study between green and nonphotosynthetic individuals. Canadian Journal of Botany 84: 1462-1477.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
3. Arditti, J. 1992. Fundamentals of orchid biology. John Wiley, New York, New York, USA.
4. Bernard, N. 1899. Sur la germination du Neottia nidus-avis. Compte Rendu Hebdomadaire des S é ances de l'Acadé mie des Sciences, Paris 128: 1253-1255.
5. Bidartondo, M. I., and T. D. Bruns.2002. Fine-levelmycorrhizalspecificity in the Monotropoideae (Ericaceae): Specificity for fungal spe- cies groups. Molecular Ecology 11: 557-569.
6. Bidartondo, M. I., B. Burghardt, G. Gebauer, T. D. Bruns, and D. J. Read. 2004. Changing partners in the dark: Isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees.Proceedings of the Royal Society of London, B, Biological Sciences 271: 1799-1806.
7. Bidartondo, M. I., and D. J. Read. 2008. Fungal specificity bottlenecks during orchid germination and development. Molecular Ecology 17: 3707-3716.
8. Binder, M., D. S. Hibbett, K. H. Larsoon, E. Larsoon, E. Langer, and G. Langer. 2005. The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes). Systematics and Biodiversity 3: 113-157.
9. Bonnardeaux, Y., M. Brundrett, A. Batty, K. Dixon, J. Koch, and K. Sivasithamparam. 2007. Diversity of mycorrhizal fungi in terrestrial orchids: Compatibility webs, brief encounters, lasting relationships and alien invasions. Mycological Research 111: 51-61.
10. Bougoure, J. J., D. S. Bougoure, J. W. G. Cairney, and J. D. W. Dearnaley. 2005. ITS-RFLP and sequence analysis of endophytes from Acianthus, Caladenia and Pterostylis (Orchidaceae) in south- eastern Queensland. Mycological Research 109: 452-460.
11. Bougoure, J. J., and J. D. W. Dearnaley. 2005. The fungal endophytes of Dipodium variegatum (Orchidaceae). Australasian Mycologist 24: 15-19.
12. Brundrett, M. C. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytologist 154: 275-304.
13. Cameron, K. M. 2004. Utility of plastid psaB gene sequences for investigating intrafamilial relationships within Orchidaceae. Molecular Phylogenetics and Evolution 31: 1157-1180.
14. Cameron, K. M., M. W. Chase, W. M. Whitten, P. J. Kores, D. C. Jarrell, V. A. Albert, T. Yukawa, et al. 1999. A phylogenetic analysis of the Orchidaceae: Evidence from rbcL nucleotide sequences. American Journal of Botany 86: 208-224.
15. Chase, M. W., M. F. Fay, D. S. Devey, O. Maurin, N. R ønsted, T. J. Davies, Y. Pillon, et al.2006. Multi-geneanalysesofmonocotrelationships: A summary. Aliso 22: 63-75.
16. Chase, M. W., J. V. Freudenstein, and K. M. Cameron. 2003. DNA data and Orchidaceae systematics: A new phylogenetic classification. In K. W. Dixon, S. P. Kell, R. L. Barrett, and P. J. Cribb [eds], Orchid conservation, 69-89. Natural History Publications, Kota Kinabalu, Sabah, Malaysia.
17. Cribb, P., and R. Govaerts. 2005. Just how many orchids are there? In A. Raynal-Roques and A. Roguenant [eds], Proceedings of the 18th World Orchid Conference, Dijon, France, 161-172. Naturalia Publications, Turriers, France.
18. Currah, R. S., C. D. Zelmer, S. Hambleton, and K. A. Richardson. 1997. Fungi from orchid mycorrhizas. In J. Arditti and A. M. Pridgeon [eds], Orchid biology: Reviews and perspectives, VII, 117-170. Kluwer, Dordrecht, Netherlands.
19. Dearnaley, J. D. W. 2006. The fungal endophytes of Erythrorchis cassythoides -Is this orchid saprophytic or parasitic? Australasian Mycologist 25: 51-57.
20. Dearnaley, J. D. W., and A. F. Le Brocque. 2006. Molecular identification of the primary root fungal endophytes of Dipodium hamiltonianum (yellow hyacinth orchid). Australian Journal of Botany 54: 487-491.
21. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
22. Gardes, M., and T. D. Bruns. 1993. ITS primers with enhanced specificity for basidiomycetes-Application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
23. 15 N and 13 C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytologist 160: 209-223.
24. Girlanda, M., M. A. Selosse, D. Cafasso, F. Brilli, S. Delfine, R. Fabbian, S. Ghignone, et al. 2006. Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Molecular Ecology 15: 491-504.
25. Givnish, T. J., J. C. Pires, S. W. Graham, M. A. McPherson, L. M. Prince, T. B. Patterson, H. S. Rai, et al. 2006. Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: Evidence for widespread concerted convergence. Aliso 22: 28-51.
26. González, D., M. A. Cubeta, and R. Vilgalys. 2006. Phylogenetic utility of indels within ribosomal DNA and beta-tubulin sequences from fungi in the Rhizoctonia solani species complex. Molecular Phylogenetics and Evolution 40: 459-470.
27. Graham, S. W., J. M. Zgurski, M. A. McPherson, D. M. Cherniawsky, J. M. Saarela, E. F. C. Horne, S. Y. Smith, et al. 2006. Robust inference of monocot deep phylogeny using an expanded multigene plastid data set. Aliso 22: 3-21.
28. Hadley, G. 1982. Orchid mycorrhiza. In J. Arditti [ed], Orchid biology: Reviews and perspectives, II, 85-118. Cornell University Press, Ithaca, New York, USA.
29. Hall, I. R. 1976. Vesicular mycorrhizas in the orchid Corybas macranthus. Transactions of the British Mycological Society 66: 160.
30. Hibbett, D. S., M. Binder, J. F. Bischoff, M. Blackwell, P. F. Cannon, O. E. Eriksson, S. Huhndorff,et al.2007. Ahigher-levelphylogenetic classification of the fungi. Mycological Research 111: 509-547.
31. Illyes, Z., S. Rudnoy, and Z. Bratek. 2005. Aspects of in situ, in vitro germination and mycorrhizal partners of Liparis loeselii. Acta Biologica Szegediensis 49: 137-139.
32. Irwin, M. J., J. J. Bougoure, and J. D. W. Dearnaley. 2007. Pterostylis nutans (Orchidaceae) has a specific association with two Ceratobasidium root-associated fungi across its range in eastern Australia. Mycoscience 48: 231-239.
33. Janos, D. P. 1993. Vesicular-arbuscular mycorrhizae of epiphytes.Mycorrhiza 4: 1-4.
34. Julou, T., B. Burghardt, G. Gebauer, D. Berveiller, C. Damesin, and M.-A. Selosse. 2005. Mixotrophy in orchids: Insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytologist 166: 639-653.
35. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
36. Kocyan, A., Y. L. Qiu, P. K. Endress, and E. Conti. 2004. A phylogenetic analysis of Apostasioideae (Orchidaceae) based on ITS, trnL-F and matK sequences. Plant Systematics and Evolution 247: 203-213.
37. Kress, W. J. 1986. The systematic distribution of vascular epiphytes: An update. Selbyana 9: 2-22.
38. Kristiansen, K. A., J. V. Freudenstein, F. N. Rasmussen, and H. N. Rasmussen. 2004. Molecular identification of mycorrhizal fungi in Neuwiedia veratrifolia (Orchidaceae). Molecular Phylogenetics and Evolution 33: 251-258.
39. Kristiansen, K. A., F. N. Rasmussen, and H. N. Rasmussen. 2001a. Seedlings of Neuwiedia (Orchidaceae subfamily Apostasioideae) have typical orchidaceous mycotrophic protocorms. American Journal of Botany 88: 956-959.
40. Kristiansen, K. A., D. L. Taylor, R. Kjoller, H. N. Rasmussen, and S. Rosendahl. 2001b. Identification of mycorrhizal fungi from single pelotons of Dactylorhiza majalis (Orchidaceae) using single-strand conformation polymorphism and mitochondrial ribosomal large sub- unit DNA sequences. Molecular Ecology 10: 2089-2093.
41. Langer, G., E. Langer, and C.-J. Chen. 2000. Botryobasidium musaisporum sp. nov. collected in Taiwan. Mycological Research 104: 510-512.
42. Leake, J. R. 1994. The biology of myco-heterotrophic ('saprophytic') plants. New Phytologist 127: 171-216.
43. Matheny, P. B., Z. Wang, M. Binder, J. M. Curtis, Y. W. Lim, R. H. Nilsson, K. W. Hughes, et al. 2007. Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Molecular Phylogenetics and Evolution 43: 430-451.
44. McCormick, M. K., D. F. Whigham, and J. O'Neill. 2004. Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytologist 163: 425-438.
45. McKendrick, S. L., J. R. Leake, D. L. Taylor, and D. J. Read. 2002. Symbiotic germination and development of the mycoheterotrophic orchid Neottia nidusavis in nature and its requirement for locally distributed Sebacina spp. New Phytologist 154: 233-247.
46. Molvray, M., P. J. Kores, and M. W. Chase. 2000. Polyphyly of mycoheterotrophic orchids and functional influences on floral and molecular characters. In K. L. Wilson and D. A. Morrison [eds.], Monocots: Systematics and evolution, 441-448. Commonwealth Scientific and Industrial Research Organisation Publishing, Melbourne, Australia.
47. Moncalvo, J. M., F. M. Lutzoni, S. A. Rehner, J. Johnson, and R. Vilgalys. 2000. Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Systematic Biology 49: 278-305.
48. Moncalvo, J. M., R. H. Nilsson, B. Koster, S. M. Dunham, T. Bernauer, P. B. Matheny, T. M. Porter, et al. 2006. The cantharelloid clade: Dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98: 937-948.
49. Ogura-Tsujita, Y., G. Gebauer, T. Hashimoto, H. Umata, and T. Yukawa. 2009. Evidence for novel and specialised mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proceedings of the Royal Society, B, Biological Sciences 276: 761-767.
50. Ogura-Tsujita, Y., and T. Yukawa. 2008a. High mycorrhizal specificity in a widespread mycoheterotrophic plant, Eulophia zollingeri (Orchidaceae). American Journal of Botany 95: 93-97.
51. Ogura-Tsujita, Y., and T. Yukawa. 2008b. Epipactis helleborine shows strong mycorrhizal preference towards ectomycorrhizal fungi with contrasting geographic distributions in Japan. Mycorrhiza 18: 331-338.
52. Otero, J. T., J. D. Ackerman, and P. Bayman. 2002. Diversity and host specificity of endophytic Rhizoctonia -like fungi from tropical orchids. American Journal of Botany 89: 1852-1858.
53. Otero, J. T., J. D. Ackerman, and P. Bayman. 2004. Differences in mycorrhizal preferences between two tropical orchids. Molecular Ecology 13: 2393-2404.
54. Otero, J. T., and N. S. Flanagan. 2006. Orchid diversity-Beyond deception. Trends in Ecology & Evolution 21: 64-65.
55. Pires, J. C., I. J. Maureira, T. J. Givnish, K. J. Sytsma, O. Seberg, G. Petersen, J. I. Davis, et al. 2006. Phylogeny, genome size, and chromosome evolution of Asparagales. Aliso 22: 287-304.
56. Porras-Alfaro, A., and P. Bayman. 2007. Mycorrhizal fungi of Vanilla: Diversity, specificity, and effects on seed germination and plant growth. Mycologia 99: 510-525.
57. Posada, D., and K. A. Crandall. 1998. Model test: Testing the model of DNA substitution. Bioinformatics 14: 817-818.
58. Rasmussen, H. N. 1995. Terrestrial orchids: From seed to mycotrophic plant. Cambridge University Press, Cambridge, UK.
59. Rasmussen, H. N. 2002. Recent developments in the study of orchid mycorrhiza. Plant and Soil 244: 149-163.
60. Roberts, P. 1999. Rhizoctonia -forming fungi: A taxonomic guide. Royal Botanic Gardens, Kew, Richmond, UK.
61. Saitou, N., and M. Nei. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
62. Selosse, M. A., A. Faccio, G. Scappaticci, and P. Bonfante. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal Septomycetes, including truffles. Microbial Ecology 47: 416-426.
63. Selosse, M. A., M. Weiß, J. L. Jany, and A. Tiller. 2002. Communities and populations of sebacinoid Basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L.C.M. Rich. and neighbouring tree ectomycorrhizae. Molecular Ecology 11: 1831-1844.
64. Sen, R., A. M. Hiet-aletal/et-ala, and C. D. Zelmer. 1999. Common anastomosis and internal transcribed spacer RFLP groupings in binucleate Rhizoctonia isolates representing root endophytes of Pinus sylvestris, Ceratorhiza spp. from orchid mycorrhizas and a phytopathogenic anastomosis group. New Phytologist 144: 331-341.
65. Shefferson, R. P., T. Kull, and K. Tali. 2008. Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills. American Journal of Botany 95: 156-164.
66. Shefferson, R. P., D. L. Taylor, M. Wei ß, S. Garnica, M. K. McCormick, S. Adams, H. M. Gray, et al. 2007. The evolutionary history of mycorrhizal specificity among lady' s slipper orchids. Evolution 61: 1380-1390.
67. Shefferson, R. P., M. Weiβ, T. Kull, and D. L. Taylor. 2005. High specificity generally characterizes mycorrhizal association in rare lady' s slipper orchids, genus Cypripedium. Molecular Ecology 14: 613-626
68. Smith, S. E., and D. J. Read. 1997. Mycorrhizal symbiosis. Academic Press, San Diego, California, USA.
69. Stern, W. L., V. I. Cheadle, and J. Thorsch.1993. Apostasiads,systematic anatomy, and the origins of Orchidaceae. Botanical Journal of the Linnean Society 111: 411-455.
70. Stern, W. L., and J. H. Warcup. 1994. Root tubercles in apostasiad orchids. American Journal of Botany 81: 1571-1575.
71. Suárez, J. P., M. Weiß, A. Abele, S. Garnica, F. Oberwinkler, and I. K ottke. 2006. Diverse tulasnelloid fungi form mycorrhizas with epiphytic orchids in an Andean cloud forest. Mycological Research 110: 1257-1270.
72. Swofford, D. L. 2003. PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer, Sunderland, Massachusetts, USA.
73. Tamura, M. N., J. Yamashita, S. Fuse, and M. Haraguchi. 2004. Molecular phylogeny of monocotyledons inferred from combined analysis of plastid matK and rbcL gene sequences. Journal of Plant Research 117: 109-120.
74. Taylor, D. L., and T. D. Bruns. 1997. Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proceedings of the National Academy of Sciences, USA 94: 4510-4515.
75. Taylor, D. L., and T. D. Bruns. 1999. Population, habitat and genetic correlates of mycorrhizal specialization in the 'cheating' orchids Corallorhiza maculata and C. mertensiana. Molecular Ecology 8: 1719-1732.
76. Taylor, D. L., T. D. Bruns, and S. A. Hodges. 2004. Evidence for mycorrhizal races in a cheating orchid. Proceedings of the Royal Society, B, Biological Sciences 271: 35-43.
77. Taylor, D. L., T. D. Bruns, T. M. Szaro, and S. A. Hodges. 2003. Divergence in mycorrhizal specialization within Hexalectris spicata (Orchidaceae), a nonphotosynthetic desert orchid. American Journal of Botany 90: 1168-1179.
78. Taylor, D. L., and M. K. McCormick. 2008. Internal transcribed spacer primers and sequences for improved characterization of basidiomycetous orchid mycorrhizas. New Phytologist 177:1020-1033.
79. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997,The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
80. Wang, B., and Y. L. Qiu. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.
81. Weiss, M., M. A. Selosse, K. H. Rexer, A. Urban, and F. Oberwinkler,2004. Sebacinales: A hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycological Research 108: 1003-1010.
82. White, T. J., T. D. Bruns, S. B. Lee, and J. W. Taylor 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds], PCR protocols: A guide to methods and applications, 315-322. Academic Press, San Diego, California, USA.
83. Xu, J. T., and C. Mu, 1990, The relation between growth of Gastrodia elata protocorms and fungi. Acta Botanica Sinica 32: 26-31.
84. Yamato, M., T. Yagame, and A. Suzuki. 2005. Isolation and identification of mycorrhizal fungi associating with an achlorophyllous plant, Epipogium roseum (Orchidaceae). Mycoscience 46: 73-77.
85. Yukawa, T. 2007, Why are orchids so diverse? Evolution of life forms and nutritional modes in Orchidaceae. Iden 61: 13-19 [in Japanese].
86. Yukawa, T., K. Kita, T. Handa, H. Topik, and M. Ito. 2005. Molecular phylogenetics of Phalaenopsis (Orchidaceae) and allied genera: Reevaluation of generic concepts. Acta Phytotaxonomica Geobotanica 56: 141-161.
87. Zhao, Z. W., Y. M. Xia, X. Z. Qin, X. W. Li, L. Z. Cheng, T. Sha, and G. H. Wang. 2001. Arbuscular mycorrhizal status of plants and the spore density of arbuscular mycorrhizal fungi in the tropical rain forest of Xishuangbanna, southwest China. Mycorrhiza 11: 159-162.