Evolutionary histories and mycorrhizal associations of mycoheterotrophic plants dependent on saprotrophic fungi

Abstract

Mycoheterotrophic plants (MHPs) are leafless, achlorophyllous, and completely dependent on mycorrhizal fungi for their carbon supply. Mycorrhizal symbiosis is a mutualistic association with fungi that is undertaken by the majority of land plants, but mycoheterotrophy represents a breakdown of this mutualism in that plants parasitize fungi. Most MHPs are associated with fungi that are mycorrhizal with autotrophic plants, such as arbuscular mycorrhizal (AM) or ectomycorrhizal (ECM) fungi. Although these MHPs gain carbon via the common mycorrhizal network that links the surrounding autotrophic plants, some mycoheterotrophic lineages are associated with saprotrophic (SAP) fungi, which are free-living and decompose leaf litter and wood materials. Such MHPs are dependent on the forest carbon cycle, which involves the decomposition of wood debris and leaf litter, and have a unique biology and evolutionary history. MHPs associated with SAP fungi (SAP-MHPs) have to date been found only in the Orchidaceae and likely evolved independently at least nine times within that family. Phylogenetically divergent SAP Basidiomycota, mostly Agaricales but also Hymenochaetales, Polyporales, and others, are involved in mycoheterotrophy. The fungal specificity of SAP-MHPs varies from a highly specific association with a single fungal species to a broad range of interactions with multiple fungal orders. Establishment of symbiotic culture systems is indispensable for understanding the mechanisms underlying plant-fungus interactions and the conservation of MHPs. Symbiotic culture systems have been established for many SAP-MHP species as a pure culture of free-living SAP fungi is easier than that of biotrophic AM or ECM fungi. Culturable SAP-MHPs are useful research materials and will contribute to the advancement of plant science.

Keywords: In vitro culture; Litter decay fungi; Orchid; Stable isotopes; Wood decay fungi.

Fig. 1

Mycoheterotrophic species associated with saprotrophic (SAP) fungi. a Cremastra aphylla, b Gastrodia confusa, c Cyrtosia septentrionalis, d Erythrorchis altissima, e Yoania flava, f Gastrodia nipponica, and g a tuber of Gastrodia elata. Black rhizomorphs are attached to the surface of the tuber. h In vitro symbiotic culture of E. altissima (photo by H Umata), and i in vitro symbiotic germination of G. nipponica seeds

Fig. 2

Occurrence of mycoheterotrophy within Orchidaceae. Evolutionary tracks of mycoheterotrophy are traced on a phylogenetic tree covering all major clades of the family (Chase et al. 2015). Tribes or subtribes that include saprophytic fungi-associated mycoheterotrophic plants (SAP-MHPs) are colored yellow. Genera that include SAP or ectomycorrhizal (ECM) fungi-associated MHPs (ECM-MHPs) are colored red and blue, respectively. The genus Epipogium comprises both SAP- and ECM-associated species. Genera of unknown mycorrhizal status are not colored. Asterisks indicate genera that include both leafy and leafless species