Partial mycoheterotrophy in orchids
Final Report Abstract
In the mycorrhizal symbiosis, plants exchange carbohydrates from photosynthesis for mineral nutrients acquired by fungi from the soil. This mutualistic arrangement has been subverted by a few hundreds of mycorrhizal plant species that lack the ability to photosynthesize. The most numerous examples of this mycoheterotrophic nutrition are found among the orchid family. Although achlorophyllous orchid species are known since long as mycoheterotrophic, green orchids were thought until recently as being fully autotrophic. However, carbon and nitrogen stable isotope abundances together with molecular ecological identification of fungi in orchid roots, provided evidence that some green orchids (i) gain carbon and nitrogen at least partially at the cost of fungi and (ii) switch the fungal partner towards mycorrhizas with ectomycorrhizal fungi of forest trees. This project aimed to deepen our knowledge (i) on the environmental conditions (light climate, nitrogen availability as limiting factors) and ecophysiological properties (leaf chlorophyll concentrations, switch from initial mycoheterotrophy in the seedling phase towards putative autotrophy in the adult phase, unusual high plant N concentrations) under which this hitherto unknown plant nutritional mode occurs and (ii) on the relationships between type of nutrition, fungal partners and habitats of selected taxonomic groups and - as a consequence - their distribution constraints. Light availability and leaf chlorophyll concentration turned out as major determinants of the degree of mycoheterotrophy for forest-ground orchids associated with ectomycorrhizal fungi. Low light levels and low leaf chlorophyll concentrations resulted in strong mycoheterotrophy while higher irradiance and rising leaf chlorophyll concentrations successively drove these orchids towards autotrophy. A similar light or chlorophyll-driven successive switch of carbon gain from photosynthesis and fungal source could not be confirmed or was only weakly pronounced in orchids mycorrhizal with saprotrophic fungi of the rhizoctonia group. Thus, a switch of the fungal partner from rhizoctonia fungi towards ectomycorrhizal fungi is probably an essential prerequisite for orchids thriving successfully in the deepest shade of forest grounds. Ectomycorrhiza-associated partially and fully mycoheterotrophic orchids are constrained to forest habitats composed of ectomycorrhizal trees. Therefore, ectomycorrhiza-associated orchids turned out as missing on the islands of Macaronesia poor in ectomycorrhizal tree diversity and simultaneously having a vast distribution in the Mediterranean region rich in ectomycorrhizal tree diversity. Changes in soil nitrogen availability affected orchids irrespective whether green or achlorophyllous and irrespective whether associated with rhizoctonia fungi or ectomycorrhizal fungi much less than neighbouring autotrophic non-orchids. We conclude from this finding and from identical nitrogen isotope compositions found for green orchids in the initially mycoheterotrophic seedling phase and in the photosynthetic adult phase that orchids cover their nitrogen demand preferentially or exclusively through the fungal route. This conclusion explains also the unusually high total nitrogen concentrations of orchid tissues, which are closer to fungal tissues than to tissues of the majority of autotrophic plants. High nitrogen concentrations set fully and partially mycoheterotrophic Orchidaceae apart from fully and partially mycoheterotrophic Ericaceae. We postulate a different physiology of fungus-to-plants matter exchange in these taxonomically different, but simultaneously habitat-sharing plant groups. The high nitrogen concentrations in orchids are preferentially stored as proteins with currently unknown function. The nitrogen isotope composition of orchids turned out as heavily driven by the nitrogen isotope composition of their respective fungal hosts. For representatives of the orchid genus Epipactis we identified the following sequence: 15N enrichment in Epipactis spp. associated with rhizoctonias < 15N enrichment in Epipactis spp. with ectomycorrhizal basidiomycetes < 15N enrichment in Epipactis spp. with ectomycorrhizal ascomycetes + basidiomycetes < 15N enrichment in Epipactis spp. associated with ectomycorrhizal ascomycetes. While carbon and nitrogen stable isotope natural abundance was an ideally suited tool to identify partially mycoheterotrophic species among ectomycorrhiza-associated chlorophyllous orchids and to elucidate effects of environmental conditions, habitats and sources, the isotope abundance of these two elements alone turned out as not suited to unequivocally identify partially mycoheterotrophic species among rhizoctonia-mycorrhizal orchids. Additional analysis of hydrogen and oxygen stable isotope natural abundance was identified as a tool to circumvent this limitation. Using a multi-element stable isotope natural abundance approach further partially mycoheterotrophic species among rhizoctonia-mycorrhizal orchids were identified. Thus, partial mycoheterotrophy is more widespread among orchids than previously assumed and requires further investigation.
Publications
- (2008): A methodological approach to improve estimates of nutrient gains by partially myco-heterotrophic plants. Isotopes in Environmental and Health Studies 44: 393-401
Preiss K., Gebauer G.
(See online at https://dx.doi.org/10.1080/10256010802507458) - (2008): The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytologist 178: 395-400
Zimmer K., Meyer C., Gebauer G.
(See online at https://dx.doi.org/10.1111/j.1469-8137.2007.02362.x) - (2009): The chlorophyll containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist 183: 358-364
Cameron D.D., Preiss K., Gebauer G., Read D.J.
(See online at https://dx.doi.org/10.1111/j.1469-8137.2009.02853.x) - (2010): C and N isotope signatures reveal constraints to nutritional modes in orchids of the Mediterranean and Macaronesia. American Journal of Botany 97: 903-912
Liebel H.T., Bidartondo M.I., Preiss K., Segreto R., Stöckel M., Rodda M., Gebauer G.
(See online at https://dx.doi.org/10.3732/ajb.0900354) - (2010): Irradiance governs exploitation of fungi: Finetuning of carbon gain by partially myco-heterotrophic orchids. Proceedings of the Royal Society London B 277: 1333-1336
Preiss K., Adam I.K.U., Gebauer G.
(See online at https://dx.doi.org/10.1098/rspb.2009.1966) - (2011): Stable isotope signatures confirm carbon and nitrogen gain through ectomycorrhizas in the ghost orchid Epipogium aphyllum Swartz. Plant Biology 13: 270-275
Liebel H.T., Gebauer G.
(See online at https://dx.doi.org/10.1111/j.1438-8677.2010.00369.x) - (2011): The degree of mycoheterotrophic C gain in green, variegated and vegetative albino individuals of Cephalanthera damasonium is related to leaf chlorophyll concentrations. New Phytologist 189: 790-796
Stöckel M., Meyer C., Gebauer G.
(See online at https://dx.doi.org/10.1111/j.1469-8137.2010.03510.x) - (2013): The Physiological Ecology of Mycoheterotrophy. In: V.S.F.T. Merckx (ed.) Mycoheterotrophy: The Biology of Plants Living on Fungi. Springer-Verlag, Heidelberg, Germany, pp 297-342
Hynson N.A., Madsen T.P., Selosse M.-A., Adam I.K.U., Ogura-Tsujita Y., Roy M., Gebauer G.
(See online at https://dx.doi.org/10.1007/978-1-4614-5209-6_8) - (2014): Carbon and nitrogen gain during the growth of orchid seedlings in nature. New Phytologist 202: 606-615
Stöckel M., Těšitelová T., Jersáková J., Bidartondo M.I., Gebauer G.
(See online at https://doi.org/10.1111/nph.12688) - (2015): Are carbon and nitrogen exchange between fungi and the orchid Goodyera repens affected by irradiance? Annals of Botany 115: 251-261
Liebel H.T., Bidartondo M.I., Gebauer G.
(See online at https://doi.org/10.1093/aob/mcu240) - (2016): Partial mycoheterotrophy is more widespread among orchids than previously assumed. New Phytologist 211: 11-15
Gebauer G., Preiss K., Gebauer A.C.
(See online at https://doi.org/10.1111/nph.13865) - (2016): Plant family identity distinguishes patterns of carbon and nitrogen stable isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi. Annals of Botany
Hynson N.A., Schiebold J.M.I., Gebauer G.
(See online at https://doi.org/10.1093/aob/mcw119)
