Mixotrophy in orchids: facts, questions, and perspectives.

Julita Minasiewicz, Etienne Delannoy, Florent Martos, Marc-André Selosse, Pierre-Louis Alaux, Lara Deloche, Spyros Tsiftsis, Tomas Figura

Journal: The New phytologist 2025;246(5):1912-1921

PMID: 40195594

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Abstract

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 H, C, and N. 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 H, C, and N. 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 H and N. 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.

Address: Institut Systématique Évolution Biodiversité, Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France.; Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308, Gdansk, Poland.; Institut Universitaire de France, Paris, France.; Institut Systématique Évolution Biodiversité, Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France.; Institut Systématique Évolution Biodiversité, Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France.; Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Université Evry, Gif sur Yvette, 91190, France.; Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris Cité, CNRS, INRAE, Gif sur Yvette, 91190, France.; Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Université Evry, Gif sur Yvette, 91190, France.; Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris Cité, CNRS, INRAE, Gif sur Yvette, 91190, France.; Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308, Gdansk, Poland.; Department of Forest and Natural Environment Sciences, Democritus University of Thrace, GR-66132, Drama, Greece.; Institut Systématique Évolution Biodiversité, Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, Paris, France.; Department of Mycorrhizal Symbioses, Institute of Botany, Czech Academy of Sciences, Lesní 322, 25243, Průhonice, Czech Republic.

DOI: 10.1111/nph.70106

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MeSH Terms: Orchidaceae, Mycorrhizae, Symbiosis, Carbon, Basidiomycota, Phylogeny, Heterotrophic Processes