In the mycorrhizal symbiosis, plants exchange photosynthates for mineral nutrients acquired by fungi from the soil. This mutualistic arrangement has been subverted by hundreds of mycorrhizal plant species that lack the ability to photosynthesize. The most numerous examples of this behaviour are found in the largest plant family, the Orchidaceae. Although non-photosynthetic orchid species are known to be highly specialized exploiters of the ectomycorrhizal symbiosis, photosynthetic orchids are thought to use free-living saprophytic or pathogenic fungal lineages. However, we present evidence that putatively photosynthetic orchids from five species that grow in the understorey of forests (i) form mycorrhizas with ectomycorrhizal fungi of forest trees and (ii) have stable-isotope signatures indicating distinctive pathways for nitrogen and carbon acquisition approaching those of non-photosynthetic orchids that associate with ectomycorrhizal fungi of forest trees. These findings represent a major shift in our understanding of both orchid ecology and evolution because they explain how orchids can thrive in low-irradiance niches and they show that a shift to exploiting ectomycorrhizal fungi precedes viable losses of photosynthetic ability in orchid lineages.

Explaining the large-scale diversity of soil organisms that drive biogeochemical processes-and their responses to environmental change-is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is-to our knowledge-unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.

Contents  Summary 1 Introduction 1 Monotropa: over 180 years of controversy 3 Do all epiparasites evolve from photosynthetic mycorrhizal ancestors?  5 What is unique about the monotrope radiation? 8 Potential sources of exceptional myco‐heterotrophy 10 What form of carbon moves from fungus to plant? 10 Mycorrhizas vs reproduction? 11 What fungal signal triggers symbiotic seed germination? 12 Conclusions 14  Acknowledgements 14  References 14 Summary Nonphotosynthetic mycorrhizal plants have long attracted the curiosity of botanists and mycologists, and they have been a target for unabated controversy and speculation. In fact, these puzzling plants dominated the very beginnings of the field of mycorrhizal biology. However, only recently has the mycorrhizal biology of this diverse group of plants begun to be systematically unravelled, largely following a landmark Tansley review a decade ago and crucial developments in the field of molecular ecology. Here I explore our knowledge of these evolutionarily and ecologically diverse plant–fungal symbioses, highlighting areas where there has been significant progress. The focus is on what is arguably the best understood example, the monotropoid mycorrhizal symbiosis, and the overarching goal is to lay out the questions that remain to be answered about the biology of myco‐heterotrophy and epiparasitism.