Integrated Metabolomics, Transcriptomics, and Ultrastructural Assessment of the Myco‐Heterotrophic Plant, Monotropa uniflora

ABSTRACT A systems biology approach was used to characterize Monotropa uniflora, a nonhotosynthetic, myco‐heterotrophic plant. In contrast to autotrophic plants, myco‐heterotrophic plants obtain carbon and other nutrients by connecting roots to fungi, which establish the physical connection to a photosynthetic host, and thereby source required nutrients. Although a large proportion of plants form mycorrhizal associations, heterotrophic plants that are completely dependent on the mycorrhizal association for nutrients are rare and less well studied. The potential of developing M. uniflora as a model for myco‐heterotrophic plants is demonstrated by datasets collected within this study, which include cellular ultrastructural morphologies, metabolomes and transcriptomes from tissue‐types that are at different stages of growth or development. The morphological comparisons indicate that cells of the lower stem are older than those of the upper stem. The molecular ‐omics datasets reveal greater differences as the result of development rather than growth. Despite the obvious absence of photosynthetic functions in M. uniflora, as in photosynthetic plants the most abundant metabolites are sugars and organic acids that are used to translocate carbon in the latter. KEGG pathway enrichment analysis of the transcriptomes indicates that catabolic processes are highly active, which is consistent with the hypothesis that these processes generate intermediary energy metabolites (i.e., ATP and NAD(P)H) that can support anabolic processes associated with growth or development. Correlative analyses of the abundance of cutin monomers or cuticular waxes relative to the expressed transcriptomes identified co‐expressing genes, revealing coordinated lipid metabolism network(s) that support cuticle formation in the absence of photosynthetic energy production. This model systems biology study of a myco‐heterotrophic plant offers baseline insights into the functioning and resilience of ecological niches that are increasingly threatened by anthropogenic pressures.