While orchids germinate thanks to carbon from their symbiotic fungi, variable carbon exchanges exist between adult orchids and their mycorrhizal fungi. Although some truly autotrophic orchids reward their fungi with carbon at adulthood, some species remain achlorophyllous and fully dependent on fungal carbon (mycoheterotrophy). Others are photosynthetic but also import fungal carbon: The so-called mixotrophic (MX) orchids rely on fungi of diverse taxonomy and ecology. Here, we classify MX nutrition of orchids into three types. Type I mixotrophy associates with diverse Asco- and Basidiomycota that are either saprotrophic or ectomycorrhizal, entailing enrichment of the orchids in 2H, 13C, and 15N. The two other types associate with rhizoctonias, a polyphyletic assemblage of Basidiomycotas that is ancestrally mycorrhizal in orchids. Type II mixotrophy associates with rhizoctonias that secondarily evolved into saprotrophic or ectomycorrhizal ecology, and thus enrich the orchid in 2H, 13C, and 15N. Type III mixotrophy, which remains debated, associates with rhizoctonias that have retained their ancestral lifestyle, that is saprotrophic and/or endophytic in nonorchids, and only entail orchid enrichment in 2H and 15N. Based on a case study of achlorophyllous variants in Mediterranean Ophrys and on published data, we discuss the distinct nature and research perspectives of type III mixotrophy.

Department of Forest and Natural Environment Sciences Democritus University of Thrace GR 66132 Drama Greece

Department of Mycorrhizal Symbioses Institute of Botany Czech Academy of Sciences Lesní 322 25243 Průhonice Czech Republic

Department of Plant Taxonomy and Nature Conservation University of Gdansk Wita Stwosza 59 80 308 Gdansk Poland

Institut Systématique Évolution Biodiversité Muséum National d'Histoire Naturelle CNRS Sorbonne Université Paris France

Institut Universitaire de France Paris France

Institute of Plant Sciences Paris Saclay Université Paris Cité CNRS INRAE Gif sur Yvette 91190 France

Institute of Plant Sciences Paris Saclay Université Paris Saclay CNRS INRAE Université Evry Gif sur Yvette 91190 France

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