Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza-forming Ceratobasidiaceae fungi

New Phytologist

Volumn 193, Issue 1, 2012, Pages 178-187

  Yagame, Takahiro ^a   Orihara, Takamichi ^b,c   Selosse, Marc André ^d   Yamato, Masahide ^a   Iwase, Koji ^e  

^a TOTTORI UNIVERSITY   (Japan)

^b KANAGAWA PREFECTURAL MUSEUM OF NATURAL HISTORY   (Japan)

^c TOTTORI UNIVERSITY   (Japan)

^d CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^e TEIKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

13C; 15N; Chamaegastrodia sikokiana; Mycoheterotrophy; Rhizanthella gardneri; Rhizoctonias; Specificity; Tribe Orchideae

Indexed keywords

CARBON; NITROGEN; SPACER DNA;

CARBON ISOTOPE; CONIFEROUS TREE; ECTOMYCORRHIZA; FUNGUS; HETEROTROPHY; ISOTOPIC ANALYSIS; MITOCHONDRIAL DNA; MIXOTROPHY; MONOCOTYLEDON; NITROGEN ISOTOPE; PHOTOSYNTHESIS; PHYLOGENETICS; PHYLOGENY; POLYMERASE CHAIN REACTION; SEEDLING; STABLE ISOTOPE; SYMBIONT;

ARTICLE; AUTOTROPHY; BASIDIOMYCETES; BAYES THEOREM; CYTOLOGY; ECOSYSTEM; FRUITING BODY; GENETICS; JAPAN; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; NUCLEOTIDE SEQUENCE; ORCHIDACEAE; PHYLOGENY; PHYSIOLOGY;

AUTOTROPHIC PROCESSES; BASE SEQUENCE; BASIDIOMYCOTA; BAYES THEOREM; CARBON ISOTOPES; DNA, INTERGENIC; ECOSYSTEM; FRUITING BODIES, FUNGAL; JAPAN; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; NITROGEN ISOTOPES; ORCHIDACEAE; PHYLOGENY;

CERATOBASIDIACEAE; FUNGI; HYPHOMYCETES; ORCHIDACEAE; ORCHIDEAE; PINUS DENSIFLORA; PLATANTHERA; RHIZANTHELLA GARDNERI;

EID: 82955163190     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03896.x     Document Type: Article

References (58)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
2. Arditti J, Ghani AKA. 2000. Numerical and physical properties of orchid seeds and their biological implications. New Phytologist 145: 367-421.
3. Bateman RM, James KE, Luo YB, Lauri RK, Fulcher T, Cribb PJ, Chase MW. 2009. Molecular phylogenetics and morphological reappraisal of the Platanthera clade (Orchidaceae: Orchidinae) prompts expansion of the generic limits of Galearis and Platanthera. Annals of Botany 104: 431-445.
4. Bergemann SE, Garbelotto M. 2006. High diversity of fungi recovered from the roots of mature tanoak (Lithocarpus densiflorus) in northern California. Canadian Journal of Botany 84: 1380-1394.
5. 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. Proceedings of the Royal Society B: Biological Sciences 271: 1799-1806.
6. Bougoure J, Ludwig M, Brundrett M, Grierson P. 2009. Identity and specificity of the fungi forming mycorrhizas with the rare myco-heterotrophic orchid Rhizanthella gardneri. Mycological Research 113: 1097-1106.
7. 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 Phytologist 171: 405-416.
8. Collier FA, Bidartondo MI. 2009. Waiting for fungi: the ectomycorrhizal invasions of lowland heathlands. Journal of Ecology 97: 950-963.
9. Currach RS, Smreciu EA, Hambleton S. 1990. Mycorrhizae and mycorrhizal fungi of boreal species of Platanthera and Coeloglossum (Orchidaceae). Canadian Journal of Botany 68: 1171-1181.
10. Dearnaley JDW. 2007. Further advances in orchid mycorrhizal research. Mycorrhiza 17: 475-486.
11. Dearnaley JDW, Martos F, Selosse M-A. 2012. Orchid mycorrhizas: molecular ecology, physiology, evolution and conservation aspects.In: Hock B, ed. Fungal Associations, 2nd Edition. The Mycota IX. Berlin, Heidelberg: Springer-Verlag, (in press).
12. Dixon KW, Kell SP, Barrerr RL, Cribb PJ. 2003. Orchid conservation - a global perspective. Kota Kinabalu, Sabah, M'sia: Natural History Publications.
13. Felsenstein L. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
14. Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
15. 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytologist 160: 209-223.
16. 15N natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization. New Phytologist 142: 93-101.
17. Girlanda M, Selosse MA, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F et al. 2006. Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Molecular Ecology 15: 491-504.
18. Hapeman JR, Inoue K. 1997. Plant - pollinator interactions and floral radiation in Platanthera (Orchidaceae). In: Givnish TJ, Sytsma KJ, eds. Molecular evolution and adaptive radiation. Cambridge, UK: Cambridge University Press, 433-454.
19. Hashimoto T, Kanda K, Murakawa H. 1991. Japanese indigenous orchids in color revised and enlarged (Japanese). Tokyo, Japan: Ienohikari association.
20. Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse MA. 2005. Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytologist 166: 639-653.
21. Karasawa K. 2003. Species Orchidacearum. Tokyo, Japan: Japan Broadcasting Publishing.
22. Kennedy AH, Taylor DL, Watoson LE. 2011. Mycorrhizal specificity in the fully myco-heteotrophic Hexalectris Raf. (Orchidaceae: Epidendroieae). Molecular Ecology 20: 1303-1316.
23. Kristiansen KA, Taylor DL, Kjøller R, Rasmussen HN, Rosendahl S. 2001. Identification of mycorrhizal fungi from single pelotons of Dactylorhiza majalis (Orchidaceae) using single-strand conformation polymorphism and mitochondrial ribosomal large subunit DNA sequences. Molecular Ecology 10: 2089-2093.
24. Martos F, Dulormne M, Pailler T, Bonfante P, Faccio A, Fournel J, Dubois M-P, Selosse M-A. 2009. Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytologist 184: 668-681.
25. Marx DH. 1969. Influence of ectotrophic mycorrhizal fungi on resistance or pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59: 153-163.
26. 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 Phytologist 145: 539-548.
27. Motomura H, Selosse MA, Martos F, Kagawa A, Yukawa T. 2010. Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae). Annals of Botany 106: 573-581.
28. Nylander JAA. 2004. Mr. Modeltest v2. Program distributed by the author. Uppsala, Sweden: Uppasala University, Evolutionary Biology Center.
29. O'Donnell K. 1993. Fusarium and its near relatives. In: Reynolds DR, Taylor JW, eds. The fungal holomorph: mitotic, meiotic and pleiomorphic speciation in fungal systematics. Wallingford, CT, USA: CAB International, 225-233.
30. Paduano C, Rodda M, Ercole E, Girlanda M, Perotto S. 2011. Pectin localization in the Mediterranean orchid Limodorum abortivum reveals modulation of the plant interface in response to different mycorrhizal fungi. Mycorrhiza 21: 97-104.
31. Page RDM. 1996. An application to display phylogenetic tree personal computers. Bioinformatics 12: 357-358.
32. Rasmussen HN. 1995. Terrestrial orchids - from seed to mycotrophic plant. Cambridge, UK: Cambridge University Press.
33. Rasmussen HN. 2002. Recent developments in the study of orchid mycorrhiza. Plant and Soil 244: 149-163.
34. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
35. Rosling A, Landeweert R, Lindahl BD, Larsson K-H, Kuyper TW, Taylor AFS, Finlay RD. 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytologist 159: 775-783.
36. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
37. Selosse MA, Faccio A, Scappaticci G, Bonfante P. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47: 416-426.
38. Selosse M-A, Weiss M, Jany JL, Tillier A. 2002. Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis and neighbouring tree ectomycorrhizae. Molecular Ecology 11: 1831-1844.
39. Selosse MA, Roy M. 2009. Green plants that feed on fungi: facts and question about mixotrophy. Trends in Plant Science 14: 64-70.
40. Sharma J, Zettler LW, van Sambeek JW. 2003. A survey of mycobionts of federally threatened Platanthera praeclara (Orchidaceae). Symbiosis 34: 145-155.
41. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. San Diego, CA, USA: Academic Press.
42. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
43. Swofford DL. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Massachusetts, USA: Sinauer Associates.
44. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
45. Taylor DL, McCormick MK. 2008. Internal transcribed spacer primers and sequences for improved characterization of basidiomycetous orchid mycorrhizas. New Phytologist 177: 1020-1033.
46. Tedersoo L, Pellet P, Koljalg U, Selosse MA. 2007. Parallel evolutionary paths to myco-heterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151: 206-217.
47. Tedersoo L, May TW, Smith ME. 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-263.
48. Thompson JD, Higgins DG, Gibson TJ. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequencing weighting, position sequence gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680.
49. Trudell SA, Rygiewicz PT, Edmonds RL. 2004. Patterns of nitrogen and carbon stable isotope ratios in macrofungi, plants and soils in two old-growth conifer forests. New Phytologist 164: 317-335.
50. Warcup JH. 1985. Rhizanthella gardneri (Orchidaceae), its Rhizoctonia endophyte and close association with Melaleuca uncinata (Myrtaceae) in Western Australia. New Phytologist 99: 273-280.
51. Waterman RJ, Bidartondo MI, Stofberg J, Combs JK, Gebauer G, Savolainen V, Barraclough TG, Pauw A. 2011. The effects of above- and belowground mutualisms on orchid speciation and coexistence. American Naturalist 177: 54-68.
52. Wood JJ, Cribb PJ. 1994. A check-list of the orchids of Borneo. Kew, UK: Royal BotanicGardens.
53. Wright SHA, Lim S, Berbee ML. 2009. The effect of fertilization on the below-ground diversity and community composition of ectomycorrhizal fungi associated with western hemlock (Tsuga heterophylla). Mycorrhiza 19: 267-276.
54. Yagame T, Yamato M, Suzuki A, Iwase K. 2008. Ceratobasidiaceae mycorrhizal fungi isolated from nonphotosynthetic orchid Chamaegastrodia sikokiana. Mycorrhiza 18: 97-101.
55. Yukawa T, Ogura-Tsujita Y, Shefferson RP, Yokoyama J. 2009. Mycorrhizal diversity in Apostasia (Orchidaceae) indicates the origin and evolution of orchid mycorrhiza. American Journal of Botany 96: 1997-2000.
56. Zelmer CD, Currah RS. 1995. Ceratorhiza pernacetene and Epulorhiza calendulina spp. nov.: mycorrhizal fungi of terrestrial orchids. Canadian Journal of Botany 73: 1981-1985.
57. Zelmer CD, Cuthbertson L, Currah RS. 1996. Fungi associated with terrestrial orchid mycorrhizas, seeds and protocorms. Mycoscience 37: 439-448.
58. Zettler LW. 2005. Protocorm mycobionts of the federally threatened eastern prairie fringed orchid, Platanthera leucophaea (Nutt.) Lindley, and a technique to prompt leaf elongation in seedlings. Studies in Mycology 53: 163-171.