Irradiance governs exploitation of fungi: fine-tuning of carbon gain by two partially myco-heterotrophic orchids

Abstract

While all members of the Orchidaceae are fully dependent on mycorrhizal fungi during their achlorophyllous juvenile stages, mature plants may remain fully myco-heterotrophic, become fully autotrophic or develop a nutritional mode where the carbon gain through photosynthesis is complemented by organic carbon from fungal partners. This so-called partial myco-heterotrophy is intriguingly complex. Current knowledge indicates a large range in the proportion of fungus-derived carbon between and within partially myco-heterotrophic plant species. However, the driving factors for this variation are so far mostly unknown. Here we show for two green species of the orchid genus Cephalanthera that light availability is the major determinant of the degree of myco-heterotrophy. Using leaf stable isotope natural abundance analysis together with time-integrated microscale light climate monitoring we could demonstrate that there is a sensitive reaction to varying light availability within forests. Low light levels result in strong myco-heterotrophy while higher irradiances successively drive the orchids towards autotrophy. Our results demonstrate that partial myco-heterotrophy in these species is not a static nutritional mode but a flexible mechanism driven by light availability which allows a balanced usage of carbon resources available in nature.

Plant family identity distinguishes patterns of carbon and nitrogen stable isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi

“…(2012) and Johansson et al (2015) were kindly made available by the authors. Unpublished data on N stable isotope abundance were supplied by Preiss et al (2010). Furthermore, B. Burghardt and G. Gebauer provided unpublished C and N stable isotope abundance and N concentration data on Hypopitys monotropa and Epipactis leptochila (Godfrey) Godfrey.…”

Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ

“…The study was performed at Montferrier (Mon) near Montpellier (43839 0 N, 3851 0 E; TranchidaLombardo et al 2010), and partly replicated in another C. damasonium population at Boigneville (Boi ) near Paris (2821 0 E, 48821 0 N; Julou et al 2005). Mon is a 15-year-old poplar plantation on a former vineyard where Populus nigra is planted every 7 m, with young Quercus pubescens growing inbetween, and a very homogeneous light environment (Appendix A), limiting the physiological variations reported for MX plants when the light environment varies (Preiss et al 2010). The Mon understory is covered by grasses, Clematis vitalba, Rubia peregrina, and Hedera helix, and is sometimes flooded by the Lez, a nearby river, in spring and fall.…”

“…Cephalanthera damasonium is an orchid species with MX nutrition (Julou et al 2005, Cameron et al 2009, Preiss et al 2010, Sto¨ckel et al 2011) and autogamous mating (Scacchi et al 1991, Micheneau et al 2010) that sprouts one or more shoots per year from perennial rhizomes, also bearing the mycorrhizal roots (Rasmussen 1995). The study was performed at Montferrier (Mon) near Montpellier (43839 0 N, 3851 0 E; TranchidaLombardo et al 2010), and partly replicated in another C. damasonium population at Boigneville (Boi ) near Paris (2821 0 E, 48821 0 N; Julou et al 2005).…”

“…Thus, the observed trend reflects a ;43 increase in autotrophy. One important caveat is that this part of the study was not replicated beyond Mon, so that we do not know whether the trend would be as pronounced in other populations, especially in lower light environments where MX plants assimilate less C through photosynthesis (Preiss et al 2010). FIG.…”

“…13 C values in MX plants that are less photosynthetically active, due to leaf variegation (Sto¨ckel et al 2011) or ambient light conditions (Preiss et al 2010, Matsuda et al 2012, may result from a higher compensatory fungal C input. However, since we lack estimates of the total plant C budget, we do not know whether less photosynthetically active plants recover fungal C more efficiently, or not, in which case diluting equivalent amounts of 13 C-enriched fungal carbon in lower amounts of photosynthates also leads to increased d 13 C values.…”