Abstract
Mycoheterotrophic plants (MHP) are divided into non-photosynthesizing full MHP and green-leaved partial or initial MHP. We investigated 13C and 15N isotope enrichment in five putatively partial MHP species in the tribe Pyroleae (Ericaceae): Chimaphila umbellata, Moneses uniflora, Orthilia secunda, Pyrola chlorantha and Pyrola minor, sampled from forest sites on Öland, Sweden. For M. uniflora and P. chlorantha, we investigated isotope signatures of subterranean seedlings (which are mycoheterotrophic), to examine how the use of seedlings instead of full MHP species (Hypopitys monotropa) as reference species affects the assessment of partial mycoheterotrophy. Our main findings were as follows: (1) All investigated Pyroleae species were enriched in 15N compared to autotrophic reference plants. (2) significant fungal-derived C among the Pyroleae species was found for O. secunda and P. chlorantha. For the remaining species of C. umbellata, M. uniflora and P. minor, isotope signatures suggested adult autotrophy. (3) C and N gains, calculated using seedlings as a full MHP reference, yielded qualitatively similar results as when using H. monotropa as a reference. However, the estimated differences in C and N gains became larger when using seedlings as an MHP reference. (4) A previously unknown interspecific variation in isotope signature occurs during early ontogeny, from seed production to developing seedlings. Our findings suggest that there is a variation among Pyroleae species concerning partial mycoheterotrophy in adults. Adult autotrophy may be most common in Pyroleae species, and these species may not be as dependent on fungal-derived nutrients as some green orchids.
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References
Berry SC, Varney GT (1997) Leaf δ13C in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradients. Oecologia 109:499–506. doi:10.1007/s004420050110
Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352. doi:10.1111/j.1469-8137.2005.01429.x
Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392. doi:10.1038/nature01054
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. Proc R Soc Lond Ser B 271:1799–1806. doi:10.1098/rspb.2004.2807
Björkman E (1960) Monotropa hypopitys L.—an epiparasite on tree roots. Physiol Plant 13:308–327. doi:10.1111/j.1399-3054.1960.tb08034.x
Bol R, Ostle NJ, Chenu CC, Petzke K-J, Werner RA, Balesdent J (2004) Long term changes in the distribution and δ15N values of individual soil amino acids in the absence of plant and fertiliser inputs. Isotopes Environ Health Stud 40:243–256. doi:10.1080/10256010412331305607
Cameron DD, Johnson I, Read DJ, Leake JR (2008) Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid Goodyera repens. New Phytol 180:176–184. doi:10.1111/j.1469-8137.2008.02533.x
Cullings KW, Szaro TM, Bruns TD (1996) Evolution of extreme specialization within a lineage of ectomycorrhizal epiparasites. Nature 379:63–66. doi:10.1038/379063a0
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559. doi:10.1146/annurev.ecolsys.33.020602.095451
Eriksson O, Kainulainen K (2011) The evolutionary ecology of dust seeds. Perspect Plant Ecol Evol Syst 13:73–87. doi:10.1016/j.ppees.2011.02.002
Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126. doi:10.1016/S1360-1385(01)01889-1
Fry B (2006) Stable isotope ecology. Springer, New York
Gebauer G, Meyer M (2003) N-15 and C-13 natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytol 160:209–223. doi:10.1046/j.1469-8137.2003.0087
Gonneau C, Jersáková J, de Tredern E, Till-Bottraud I, Saarinen K, Sauve M, Roy M, Hájek T, Selosse M-A (2014) Photosynthesis in perennial mixotrophic Epipactis spp. (Orchidaceae) contributes more to shoot and fruit biomass than to hypogeous survival. J Ecol 102:1183–1194. doi:10.1111/1365-2745.12274
Hashimoto Y, Fukukawa S, Kunushi A, Suga H, Richard F, Sauve M, Selosse M-A (2012) Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids. New Phytol 195:620–630. doi:10.1111/j.1469-8137.2012.04174.x
Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382. doi:10.1111/j.1469-8137.2012.04300.x
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70. doi:10.2307/4615733
Hynson NA, Preiss K, Gebauer G, Bruns TD (2009a) Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytol 182:719–726. doi:10.1111/j.1469-8137.2009.02781.x
Hynson NA, Preiss K, Gebauer G (2009b) Is it better to give than to receive? a stable isotope perspective on orchid-fungal carbon transport in the green orchid species Goodyera repens and Goodyera oblongifolia. New Phytol 182:8–11. doi:10.1111/j.1469-8137.2009.02778.x
Hynson NA, Mambelli S, Amend AS, Dawson TE (2012) Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): a field manipulation and stable isotope approach. Oecologia 169:307–317. doi:10.1007/s00442-011-2198-3
Hynson NA, Madsen TP, Selosse M-A, Adam IKU, Ogura-Tsujita Y, Roy M, Gebauer G (2013a) The physiological ecology of mycoheterotrophy. In: Merckx VSFT (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, Berlin, pp 297–342
Hynson NA, Weiss M, Preiss K, Gebauer G, Treseder KK (2013b) Fungal host specificity is not a bottleneck for the germination of Pyroleae species (Ericaceae) in a Bavarian forest. Mol Ecol 22:1473–1481. doi:10.1111/mec.12180
Johansson VA, Eriksson O (2013) Recruitment limitation, germination of dust seeds, and early development of underground seedlings in six Pyroleae species. Botany 91:17–24. doi:10.1139/cjb-2012-0153
Johansson VA, Müller G, Eriksson O (2014) Dust seed production and dispersal in Swedish Pyroleae species. Nord J Bot 32:209–214. doi:10.1111/j.1756-1051.2013.00307.x
Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse M-A (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytol 166:639–653. doi:10.1111/j.1469-8137.2005.01364.x
Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68:335–423. doi:10.1663/0006-8101(2002)068[0335:PCOEMA]2.0.CO;2
Leake JR (1994) The biology of myco-heterotrophic (Saprophytic) plants. New Phytol 127:171–216. doi:10.1111/j.1469-8137.1994.tb04272.x
Matsuda Y, Shimizu S, Mori M, Ito S-I, Selosse M-A (2012) Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica (Ericaceae) growing under different light environments. Am J Bot 99:1177–1188. doi:10.3732/ajb.1100546
Merckx VSFT (2013) Mycoheterotrophy: an introduction. In: Merckx VSFT (ed) Mycoheterotrophy: the biology of plants living on fungi. Springer, Berlin, pp 1–17
Mikusinska A, Persson T, Taylor AFS, Ekblad A (2013) Effects of ingrowth bag-size and presence of soil animals on ectomycorrhizal extraradical mycelia production and isotopic composition in a Norway spruce forest. Soil Biol Biochem 66:154–162. doi:10.1016/j.soilbio.2013.07.009
Preiss K, Gebauer G (2008) A methodological approach to improve estimates of nutrient gains by partially myco-heterotrophic plants. Isotropes Environ Health Stud 44:393–401. doi:10.1080/10256010802507458
Preiss K, Adam IKU, Gebauer G (2010) Irradiance governs exploitation of fungi: fine-tuning of carbon gain by two partially mycoheterotrophic orchids. Proc R Soc Lond Ser B 277:1333–1336. doi:10.1098/rspb.2009.1966
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45
Selosse M-A, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70. doi:10.1016/j.tplants.2008.11.004
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, San Diego
Stöckel M, Tĕšitelová T, Jersáková J, Bidartondo MI, Gebauer G (2014) Carbon and nitrogen gain during the growth of orchid seedlings in nature. New Phytol 202:606–615. doi:10.1111/nph.12688
Taylor DL, Bruns TD (1997) Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proc Natl Acad Sci USA 94:4510–4515. doi:10.1073/pnas.94.9.4510
Tedersoo L, Pellet P, Kõljalg U, Selosse M-A (2007) Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151:206–217. doi:10.1007/s00442-006-0581-2
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 Phytol 160:391–401. doi:10.1046/j.1469-8137.2003.00876.x
Wallander H, Nilsson LO, Hagberg D, Bååth E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–760. doi:10.1046/j.0028-646x.2001.00199.x
Zimmer K, Hynson NA, Gebauer G, Allen EB, Allen MF, Read DJ (2007) Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytol 175:166–175. doi:10.1111/j.1469-8137.2007.02065.x
Acknowledgments
We are grateful to D. Hadden, and to two anonymous reviewers for comments on the manuscript. This study was financially supported by a grant to OE from the Swedish Research Council.
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Communicated by Rowan Sage.
We dedicate this paper to the memory of our friend and colleague Ania Mikusinska, who tragically passed away during the preparation of the manuscript.
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Johansson, V.A., Mikusinska, A., Ekblad, A. et al. Partial mycoheterotrophy in Pyroleae: nitrogen and carbon stable isotope signatures during development from seedling to adult. Oecologia 177, 203–211 (2015). https://doi.org/10.1007/s00442-014-3137-x
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DOI: https://doi.org/10.1007/s00442-014-3137-x