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Recent Developments in the Study of Orchid Mycorrhiza

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Recent Developments in the Study of Orchid Mycorrhiza Plant and Soil 244: 149–163, 2002. 149 © 2002 Kluwer Academic Publishers. Printed in the Netherlands. Recent developments in the study of orchid mycorrhiza Hanne N. Rasmussen Danish Forest & Landscape Research Institute, 11 Hoersholm Kongevej, DK 2970 Hoersholm, Denmark∗ Received 21 August 2001. Accepted in revised form 12 December 2001 Key words: basidiomycetes, mycoheterotrophy, Orchidaceae, plant-fungal relationships, specificity, symbiosis Abstract Orchids are mycoheterotrophic during their seedling stage and in many species the dependency on fungi as a carbohydrate source is prolonged into adulthood. The mycobionts in orchid mycorrhiza belong in at least 5 major taxonomic groups of basidiomycetes. Traditional records have mainly focused on saprotrophic mycobionts but the participation of both ectomycorrhizal and parasitic fungi in orchid mycorrhiza has been corroborated. There is an increasing evidence of specific relationships between orchids and fungi, though usually not on a species-to-species level. Physiological compatibility demonstrated under artificial conditions, as in vitro, may be much broader, however. Recent development of field sowing techniques has improved the possibilities of evaluating orchid- fungal relations in an ecological context. Although the general nutrient flow in orchid mycorrhiza is well known, some questions remain regarding breakdown processes of fungi within orchid tissues, especially the ptyophagic syndrome that has recently been illustrated at the ultrastructural level for the first time. Energy sources for orchid mycorrhiza in the field sociate with species of Cymbidium and Gastrodia (Fan et al., 1996; Lan et al., 1996), are acknowledged sapro- Fungi associated with orchid mycorrhiza (OM) have trophs. Lentinus edodes Berk., the shiitake mushroom, traditionally been mostly regarded as saprotrophs, that is a white-rot saprotroph, can support the devel- dead organic material thus being the energy source opment of a chlorophyll-deficient orchid, Erythrorchis for the symbiosis. This is supported by well docu- ochobiensis (Hayata) Garay, as can a range of other mented cases where orchids have developed with fungi wood rotting fungi (Umata, 1998a). The natural sym- cultured on organic additives in vitro,oronorganic biont of E. ochobiensis,aswellasGaleola altissima debris. A water agar with the addition of ground wood- (Bl.) Bl., another chlorophyll-deficient liana, is Eryth- chips can sustain some orchid-fungus symbioses from romyces crocicreas (Berk.&Br.) Hjortst. & Ryv., the seed to small plant (Whigham et al., MS). Many of the causal agent for white pocket rot in wood (Hjortstam orchid endophytes that are referred to Rhizoctonia DC and Tellería, 1990; Umata, 1995). (sensu lato) are saprophytes (Roberts, 1999). Thanate- Some anastomosis groups of Rhizoctonia solani phorus ochraceus (Massee)P.Roberts (Table 1) for ex- Kühn, a well known plant pathogen, are found in con- ample, grows on decaying wood and dead fern fronds stant association with orchids (Carling et al., 1999; (Roberts, 1998). Rhizoctonias associated with orchids Perkins and McGee, 1995); similar associations have produce a range of carbohydrate-degrading and other been described previously but usually as unstable re- enzymes enabling the breakdown of plant debris (a lationships (survey in Rasmussen, 1995). The patho- summary in Rasmussen, 1995). Rhizoctonia strains genic rhizoctonias are generally necrotrophic para- referred to Ceratorhiza R.T. Moore produce poly- sites, first killing their host and subsequently living phenoloxidases, which are active in the breakdown of =saprotrophically from it (Roberts, 1999). This life lignin (Zelmer et al., 1996). Species of Mycena that as- form thus requires a considerable saprotrophic ca- pacity (Garrett, 1962). Hypovirulent strains of R. ∗ FAX No: 45-763233. E-mail: [email protected] solani exist and it is not known whether the energy Table 1. The diversity of fungi in mycorrhizal relationship with orchids involve saprotrophs, ectomyccorhizal and parasitic fungi and 5 major basidiomycete groups: Heterobasidiomycetes: 150 Ceratobasidium, Oliveonia, Thanatephorus, Tulasnella, Sebacina, ‘Hericianae’: Russula , ‘Hymenocaetanae’: Erythromyces, ‘Thelephoranae’: Thelephora-Tomentella,and‘Agaricanae’: Armillaria, Mycena (higher basidiomycete; systematics according to informal system by Henrik Petersen, http://www.mycokey.com/aau/systematics/systematicsbasifuturistic.htm1.). Species combinations from well documented symbioses are listed, but this is not meant to imply that these species are exclusive to other symbionts. The list is not intended to be exhaustive but mainly comprises recent developments. ∗ Source not seen. ∗2Not evident from reference; found repeatedly in tissues of C.s. but germination test failed; yet germination test succeeded with Gastrodia elata and Dendrobium spp. ∗3According to Henrik Petersen Oliveonia belongs in Ceratobasidiales. ∗4 Source not seen. Teleomorph fungus Anamorph fungus Species of orchid Synomyms of fungus Fungal group Orchid lifeform Fungal lifeform Source to fungalSource to identity and relationship synonymy Armillaria jezoensis Cha Galeola septentrionalis Reichb.f. Tricholomatales terrestrial, chloro- parasite Cha and Igarishi, and Igarashi phyll deficient 1996 Armillaria mellea Gastrodia elata Bl. Tricholomatales terrestrial, chlorophyll parasite Lan et al., (Vahl.Fr.) Karst. deficient, climber 1994 Ceratobasidium bicorne J. Prasophyllum macrostachyum Ypsilonidium Ceratobasidiales terrestrial geophyte saprotroph, Roberts, 1999 Warcup and Erikss. and Ryvarden R. Br. anomalum Warcup and parasite Talbot, 1980 Talbot =Thanatephorus anomala Ceratobasidium cornigerum Acianthus reniformis C. obscurum Aut. Ceratobasidiales terrestrial geophyte saprotroph, Roberts, 1999 Warcup and (Bourdot) Rogers (R.Br.) Schltr. parasite Talbot, 1971 Ceratobasidium cornigerum Canadian orchids C. obscurum Aut. Ceratobasidiales saprotroph, Roberts, 1999 Currah et al, (Bourdot) Rogers parasite 1987 Ceratobasidium cornigerum Goodyera repens (L.) R.Br. Ceratobasidiales terrestrial rhizoma- saprotroph, Roberts,1999 (Bourdot) Rogers tous evergreen parasite Ceratobasidium cornigerum Ceratorhiza goodyerae Platanthera obtusata (Banks ex Ceratobasidiales terrestrial geophyte saprotroph Roberts, 1999 Currah et al., (Bourdot) Rogers -repentis (Costantin Pursh) Lindl. 1990 & Dufour) Moore Ceratobasidium cornigerum Pterostylis sp., Prasophyllum sp. Ceratobasidiales terrestrial geophyte saprotroph, Roberts, 1999 (Bourdot) Rogers parasite Ceratobasidium cornigerum Sarcochilus sp. C. papillatum Warcup Ceratobasidiales epiphytic, saprotroph, Roberts, 1999 (Bourdot) Rogers & Talbot monopodial parasite Ceratobasidium cornigerum Thrixspermum congestum (F. C. papillatum Warcup Ceratobasidiales epiphytic, saprotroph, Roberts, 1999 (Bourdot) Rogers M. Bail) Dockr. & Talbot monopodial parasite Ceratobasidium globisporum Calanthe triplicata (Willem.) Ames Ceratobasidiales terrestrial, only known as Roberts, 1999 Warcup & Talbot pseudobulbous orchid symbiont Ceratobasidium globisporum Trichoglottis australiensis Ceratobasidiales epiphytic, monopodial only known as Roberts, 1999 Warcup & Talbot Dockr. orchid symbiont Ceratobasidium pseudocor- Pterostylis mutica R.Br. C. angustisporum Ceratobasidiales terrestrial geophyte saprotroph Roberts, 1999 Warcup & Talbot, nigerum M.P.Christ. Warcup & Talbot 1980 ∗ Ceratobasidium sp. Taeniophyllum obtusum Bl. Ceratobasidiales epiphytic, leafless, saprotroph Irawati, 1993 photosynthetic roots Ceratobasidium sphaerosporum members of Sarcanthinae Ceratobasidiales epiphytic, monopodial only known as Roberts, 2000 Warcup & Talbot orchid symbiont Ceratobasidium sphaerosporum Pomatocalpa macphersonii (F. Ceratobasidiales epiphytic, monopodial only known as Roberts, 1999 Warcup & Warcup & Talbot Muell.) Hunt orchid symbiont Talbot, 1971 Ceratobasidium sphaerosporum Robiquetia wassellii Dockrill Ceratobasidiales epiphytic, monopodial only known as Roberts, 1999 Warcup & Warcup & Talbot orchid symbiont Talbot, 1971 Table 1. Continued Erythromyces crocicreas Galeola altissima (Bl.) Bl. Hymenochaete Aphyllophorales terrestrial, chlorophyll saprotroph Umata, 1995 (Berk. & Br.) Hjortst.&Ryv. crocicreas Berk. & Br. deficient, climber Erythromyces crocicreas Erythrorchis ochobiense Hymenochaete Hymenochaetalesterrestrial, chlorophyll saprotroph Umata, 1998 (Berk. & Br.) Hjortst.& Ryv. (Hayata) Garay crocicreas Berk. & Br. deficient, climber Moniliopsis anomala Currah Coeloglossum viride Ceratobasidiales terrestrial geophyte only known as Currah et al., 1990 (L.) Hartm. orchid symbiont Moniliopsis anomala Currah Platanthera hyperborea Ceratobasidiales terrestrial geophyte only known as Currah et al., 1990 (L.) Lindl. orchid symbiont 2 Mycena orchidicola Fan et Guo Cymbidium sinense (Andr.) Willd. Tricholomatales terrestrial rhizomatous saprotroph Fan et al., 1996∗ Mycena osmundicola Lange Gastrodia elata Bl. Tricholomatales terrestrial, chlorophyll saprotroph Lan et al., 1996 deficient, climber 3 Oliveonia pauxilla ? Exidiales∗ saprotroph Roberts, 1999 Warcup, 1975 FK(H.S.Jacks.) Donk Russulaceae spp. Corallorhiza maculata "Gloecystidiales"terrestrial, chlorophyll ectomycorrhizal Taylor and Bruns, 1999 (Rafin.) Rafin. deficient Russulaceae spp. Corallorhiza mertensiana "Gloecystidiales"terrestrial, chlorophyll ectomycorrhizal Taylor and Bruns, 1999 Bongard deficient Serendipita vermifera Acianthus spp. Sebacina vermifera Exidiales terrestrial geophyte saprotroph, Roberts, 1999 (Oberw.) P. Roberts Oberw.
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