Subterranean morphology modulates the degree of mycoheterotrophy in a green orchid Calypso bulbosa exploiting wood-decaying fungi

1. Many vascular plants and aquatic organisms are not strictly autotrophic or heterotrophic but rather mixotrophic. Mixotrophy is a widespread nutritional strategy, merging autotrophy and heterotrophy to acquire organic carbon (C). Because all orchids are mycoheterotrophic during the early stages, many species are also predisposed to mycoheterotrophic nutrition during the mature stage. Consequently, many green orchids adopt partially mycoheterotrophy, a kind of mixotrophic strategy, obtaining carbon through autotrophy and mycoheterotrophy. However, the proportions of fungal-derived carbon reported for these mixotrophic orchids show considerable variation, even within species under similar light conditions and at similar growth stages. The factors promoting such variation remain to be fully elucidated. 2. We investigated the nutritional mode of a green orchid Calypso bulbosa to determine whether coralloid rhizomes, which are often found in fully mycoheterotrophic orchids, affect the degree of mycoheterotrophy. To this end, we performed molecular barcoding and C-13 and N-15 analyses to identify the mycorrhizal partners and fungal dependency of C. bulbosa specimens with and without coralloid rhizomes. 3. We found that C. bulbosa individuals were consistently colonized by an OTU of the wood-decaying fungal genus Protomerulius (Auriculariales), regardless of the presence of rhizomes. Furthermore, although both types of C. bulbosa specimens are partially mycoheterotrophic, as indicated by their higher C-13 and N-15 abundances, those with coralloid rhizomes exhibited a higher degree of mycoheterotrophy. Our results indicate that partial mycoheterotrophy in C. bulbosa is a flexible mechanism driven by subterranean morphology. 4. Although mixotrophy has evolved repeatedly in vascular plants and aquatic organisms, their trophic plasticity remains largely unexplored. Here we propose a novel mechanism modulating the degree of mycoheterotrophy in green orchids, providing a new perspective on the ecological plasticity of nutritional mode in mixotrophic organisms. A free Plain Language Summary can be found within the Supporting Information of this article.

Automated summary

The nutritional strategy of mixotrophy, merging autotrophy and heterotrophy, is widespread among plants and aquatic organisms. Green orchids, such as Calypso bulbosa, show a flexible mechanism of partial mycoheterotrophy driven by underground morphology. The presence of coralloid rhizomes can affect the degree of mycoheterotrophy in these orchids.