Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids.
Mycoheterotrophic orchids have adapted to shaded forest understory by shifting to achlorophylly and receiving carbon from their mycorrhizal fungi. In temperate forests, they associate in a highly specific way with fungi forming ectomycorrhizas on nearby trees, and exploiting tree photosynthates. However, many rainforests lack ectomycorrhizal fungi, and there is evidence that some tropical Asiatic species associate with saprotrophic fungi. To investigate this in different geographic and phylogenetic contexts, we identified the mycorrhizal fungi supporting two tropical mycoheterotrophic orchids from Mascarene (Indian Ocean) and Caribbean islands. We tested their possible carbon sources by measuring natural nitrogen ((15)N) and carbon ((13)C) abundances. Saprotrophic basidiomycetes were found: Gastrodia similis associates with a wood-decaying Resinicium (Hymenochaetales); Wullschlaegelia aphylla associates with both litter-decaying Gymnopus and Mycena species, whose rhizomorphs link orchid roots to leaf litter. The (15)N and (13)C abundances make plausible food chains from dead wood to G. similis and from dead leaves to W. aphylla. We propose that temperature and moisture in rainforests, but not in most temperate forests, may favour sufficient saprotrophic activity to support development of mycoheterotrophs. By enlarging the spectrum of mycorrhizal fungi and the level of specificity in mycoheterotrophic orchids, this study provides new insights on orchid and mycorrhizal biology in the tropics.
Martos
Florent
F
Centre d'Ecologie Fonctionnelle et Evolutive (CNRS, UMR 5175), Equipe Interactions Biotiques, 1919 Route de Mende, F-34293 Montpellier cedex 5, France.|UMR C53 Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Université de La Réunion, 15 Avenue René Cassin, BP 7151, F-97715 Saint-Denis cedex 9, France.
Dulormne
Maguy
M
Conservatoire Botanique des Antilles Françaises, F-97100 Basse Terre, Guadeloupe, France.|EA 926 DYNECAR, Université des Antilles et de la Guyane, BP 592, F-97159 Pointe-à-Pitre, Guadeloupe, France.
Pailler
Thierry
T
UMR C53 Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Université de La Réunion, 15 Avenue René Cassin, BP 7151, F-97715 Saint-Denis cedex 9, France.
Bonfante
Paola
P
Dipartimento di Biologia Vegetale dell'Università, Istituto per la Protezione delle Piante - CNR, Viale Mattioli 25, I-10125 Torino, Italy.
Faccio
Antonella
A
Dipartimento di Biologia Vegetale dell'Università, Istituto per la Protezione delle Piante - CNR, Viale Mattioli 25, I-10125 Torino, Italy.
Fournel
Jacques
J
UMR C53 Peuplements Végétaux et Bioagresseurs en Milieu Tropical, Université de La Réunion, 15 Avenue René Cassin, BP 7151, F-97715 Saint-Denis cedex 9, France.
Dubois
Marie-Pierre
MP
Centre d'Ecologie Fonctionnelle et Evolutive (CNRS, UMR 5175), Equipe Interactions Biotiques, 1919 Route de Mende, F-34293 Montpellier cedex 5, France.
Selosse
Marc-André
MA
Centre d'Ecologie Fonctionnelle et Evolutive (CNRS, UMR 5175), Equipe Interactions Biotiques, 1919 Route de Mende, F-34293 Montpellier cedex 5, France.
D001487:Basidiomycota / Q000145:classification / Q000235:genetics / Q000502:physiology; D002247:Carbon Isotopes; D002980:Climate; D020387:Food Chain; D038821:Mycorrhizae / Q000145:classification / Q000235:genetics / Q000502:physiology*; D009587:Nitrogen Isotopes; D029595:Orchidaceae / Q000382:microbiology*; D010802:Phylogeny; D013559:Symbiosis / Q000235:genetics / Q000502:physiology; D014329:Tropical Climate
D002247:Carbon Isotopes; D009587:Nitrogen Isotopes
Alexander IJ, Lee SS. 2005. Mycorrhizas and ecosystem processes in tropical rain forest: implications for diversity. In: Burslem DFRP, Pinard MA, Hartley SE, eds. Biotic interactions in the tropics: their role in the maintenance of species. Cambridge, UK: Cambridge University Press, 165-203.
Alexander IJ, Selosse M-A. 2009. Mycorrhizas in tropical forest: a neglected research imperative. New Phytologist 182: 14-16.
Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541-549.
Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences, USA 100: 15649-15654.
Beaver RA. 1979. Host specificity of temperate and tropical animals. Nature 281: 139-141.
Bidartondo MI. 2005. The evolutionary ecology of mycoheterotrophy. New Phytologist 167: 335-352.
Bosser J. 2006. Contribution à l’étude des Orchidaceae de Madagascar, des Comores et des Mascareignes. XXXV. Description d’un Oeceoclades nouveau de Madagascar, et notes sur trois genres nouveaux pour les Mascareignes. Adansonia 28: 45-54.
Burgeff H. 1932. Saprophytismus und symbiose. Studien an tropischen Orchideen. Jena, Germany: Gustav Fisher.
Butler RA, Laurance WF. 2008. New strategies for conserving tropical forests. Trends in Ecology and Evolution 23: 469-472.
Cameron DD, Leake JR, Read DJ. 2006. Mutualistic mycorrhiza in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist 171: 405-416.
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP. 2002. Stable isotopes in plant ecology. Annual Review of Ecology Evolution and Systematics 33: 507-559.
Dearnaley JDW. 2007. Further advances in orchid mycorrhizal research. Mycorrhiza 17: 475-486.
Fan L, Guo SX, Cao WQ, Xiao PG, Xu JT. 1996. Isolation, culture, identification and biological activity of Mycena orchidicola sp. Nov. in Cymbidium sinense (Orchidaceae). Acta Mycologica Sinica 15: 251-255.
Feldmann P, Barré N. 2001. Atlas des orchidées sauvages de la Guadeloupe. Patrimoines Naturels 48. Paris, France: SPN/IEGB/MNHN/CIRAD.
Franke T, Beenken L, Döring M, Kocyan A, Agerer R. 2006. Arbuscular mycorrhizal fungi of the Glomus-group A lineage (Glomerales; Glomeromycota) detected in myco-heterotrophic plants from tropical Africa. Mycological Progress 5: 24-31.
Ghosh A, Frankland JC, Thurston CF, Robinson CH. 2003. Enzyme production by Mycena galopus mycelium in artificial media and in Picea sitchensis F1 horizon needle litter. Mycological Research 107: 996-1008.
Hillebrand H. 2004. On the generality of the latitudinal gradient. American Naturalist 163: 192-211.
Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
Imhof S. 2007. Specialized mycorrhizal colonization pattern in achlorophyllous Epirixanthes spp. (Polygalaceae). Plant Biology 9: 786-792.
Isagi Y, Kawahara T, Kamo K. 1993. Biomass and net production in a bamboo Phyllostachys bambusoides stand. Ecological Research 8: 123-133.
Jansson PE, Berg B. 1985. Temporal variation of litter decomposition in relation to simulated soil climate. Long term decomposition in a Scots pine forest. Canadian Journal of Botany 63: 1008-1016.
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.
Kikuchi G, Higuchi M, Morota T, Nagasawa E, Suzuki A. 2008. Fungal symbiont and cultivation test of Gastrodia elata Blume (Orchidaceae). Journal of Japanese Botany 83: 88-95.
Kusano S. 1911. Gastrodia elata and its symbiotic association with Armillaria mellea. Journal of the College of Agriculture Imperial University of Tokyo 4: 1-65.
Lavelle P, Blanchard E, Martin A, Martin S. 1993. A hierarchical model for decomposition in terrestrial ecosystems: application to soils of the humid tropics. Biotropica 25: 130-150.
Leake JR. 1994. The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytologist 127: 171-216.
Leake JR. 2004. Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Current Opinion in Plant Biology 7: 422-428.
Martin F, Selosse MA. 2008. The Laccaria genome: a symbiont blueprint decoded. New Phytologist 188: 296-310.
Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo J-M, Ge Z-W, Yang Z-L, Slot JC, Ammirati JF, Baroni TJ et al . 2007. Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Molecular Phylogenetics and Evolution 43: 430-451.
Merckx V, Bidartondo MI. 2008. Breakdown and delayed cospeciation in the arbuscular mycorrhizal mutualism. Proceedings of the Royal Society London Series B 275: 1029-1035.
Molvray M, Kores PJ, Chase MW. 2000. Polyphyly of mycoheterotrophic orchids and functional influence on floral and molecular characters. In: Wilson KL, Morrison DA, eds. Monocots: systematics and evolution. Melbourne, Australia: CSIRO, 441-447.
Moore RT. 1996. The dolipore/parenthosome septum in modern taxonomy. In: Sneh B, Jabaji-Hare S, Neate S, Dijst G, eds. Rhizoctonia species: taxonomy, molecular biology, ecology, pathology and disease control. Dordrecht, the Netherlands: Kluwer Academic Publishers, 13-35.
Nakasone KK. 2007. Morphological and molecular studies on Resinicium s. str. Canadian Journal of Botany 85: 420-436.
Ogura-Tsujita Y, Yukawa T. 2008. High mycorrhizal specificity in a widespread mycoheterotrophic plant, Eulophia zollingeri (Orchidaceae). American Journal of Botany 95: 93-97.
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. Proceedings of the Royal Society London Series B 276: 761-767.
Ohlsson KEA, Wallmark PH. 1999. Novel calibration with correction for drift and non-linear response for continuous flow isotope ratio mass spectrometry applied to the determination of δ15N, total nitrogen, δ13C and total carbon in biological material. Analyst 124: 571-577.
Öpik M, Moora M, Liira J, Zobel M. 2006. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. Journal of Ecology 94: 778-790.
Osono T, Takeda H. 2006. Fungal decomposition of Abies needle and Betula leaf litter. Mycologia 98: 172-179.
Rasmussen HN. 1995. Terrestrial orchids - from seed to mycotrophic plant. Cambridge, UK: Cambridge University Press.
Rasmussen HN. 2002. Recent developments in the study of orchid mycorrhiza. Plant and Soil 244: 149-163.
Roy M, Whatthana S, Richard F, Vessabutr S, Selosse M-A. (in press). Mycoheterotrophic orchids from Thailand tropical dipterocarpacean forests associate with a broad diversity of ectomycorrhizal fungi. BMC Biology.
Roy M, Yagame T, Yamato M, Iwase K, Heinz C, Faccio A, Bonfante P, Selosse M-A. 2009. Ectomycorrhizal Inocybe species associate with the mycoheterotrophic orchid Epipogium aphyllum Sw., but not with its asexual propagules, throughout its Eurasiatic range. Annals of Botany 104 : 595-610.
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.
Selosse M-A, Faccio A, Scappaticci P, Bonfante P. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47: 416-426.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Cambridge, UK: Academic Press.
Taylor AFS, Fransson PMA. 2007. Natural abundance of 15N and 13C in saprotrophic fungi: what can they tell us? In: Gadd GM, Watkinson SC, Dyer PS, eds. Fungi in the environment. Cambridge, UK: University Press, 141-157.
Taylor DL, Bruns TD, Leake JR, Read D. 2002. Mycorrhizal specificity and function in myco-heterotrophic plants. In: Van der Heijden MGA, Sanders I, eds. Mycorrhizal ecology. Berlin, Germany: Springer-Verlag, 375-413.
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 Phytologist 160: 391-401.
Umata H. 1995. Seed germination of Galeola altissima, an achlorophyllous orchid, with aphyllophorales fungi. Mycoscience 36: 369-372.
Valaskova V, Snajdr J, Bittner B, Cajthaml T, Merhautova V, Hofrichter M, Baldrian P. 2007. Production of lignocellulose-degrading enzymes and degradation of leaf litter by saprotrophic basidiomycetes isolated from a Quercus petraea forest. Soil Biology and Biochemistry 39: 2651-2660.
Vasiliauskas R, Mankis A, Finlay RD, Stenlid J. 2007. Wood-decay fungi in fine living roots of conifer seedlings. New Phytologist 174: 441-446.
Wang H, Wang Z, Zhang F, Liu J, He X. 1997. A cytological study on the nutrient-uptake mechanism of a saprophytic orchid Gastrodia elata. Acta Botanica Sinica 39: 500-504.
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304: 1629-1633.
Xu J, Guo S. 2000. Retrospective on the research of the cultivation of Gastrodia elata BI, a rare traditional Chinese medicine. Chinese Medical Journal 113: 686-692.
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.
Zeller B, Brechet C, Maurice JP, Le Tacon F. 2007. 13C and 15N isotopic fractionation in trees, soils and fungi in a natural forest stand and a Norway spruce plantation. Annals of Science 64: 419-429.
Zimmer K, Hynson NA, Gebauer G, Allen EB, Allen MF, Read DJ. 2008. Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytologist 175: 166-175.