Evidence for mycorrhizal cheating in Apostasia nipponica, an early-diverging member of the Orchidaceae

Most land plants, from liverworts to angiosperms, form mutualistic mycorrhizal symbioses with fungal partners. However, several plants known as mycoheterotrophs exploit fungal partners by reversing the polarity of carbon movement, which usually moves from plant to fungus. We investigated the physiological ecology of a photosynthetic orchid, Apostasia nipponica, which belongs to the first branching group within the Orchidaceae, to improve our understanding of mycoheterotrophic evolution in orchids. The fungal symbionts and nutrition modes of A. nipponica were investigated using molecular barcoding and carbon-13 (C-13) and nitrogen-15 (N-15) measurements, respectively. Community profiling based on a metabarcoding technique revealed that A. nipponica associates with specific Ceratobasidium spp. within ectomycorrhizas-forming clades, whereas isotope analysis revealed that A. nipponica was similar to fully mycoheterotrophic orchids in its C-13 signature and was even more enriched in N-15 than most of the fully mycoheterotrophic orchids that exploit ectomycorrhizal fungi. Our molecular and mass-spectrometric approaches demonstrated, for the first time, that a member of the Apostasioideae, the earliest-diverging lineage of the Orchidaceae, gains carbon through both photosynthesis and fungal cheating (i.e. partial mycoheterotrophy) during the adult stage.

Automated summary

Most land plants form mutualistic mycorrhizal symbioses with fungal partners, but mycoheterotrophs exploit fungal partners by reversing carbon movement. This study focused on a photosynthetic orchid, Apostasia nipponica, and found that it gains carbon through both photosynthesis and fungal cheating (partial mycoheterotrophy), shedding light on the evolution of mycoheterotrophy in orchids.