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Abstract Heterotrophic plants are among the most recalcitrant from a systematics perspective because of reduced morphological and genomic features, and often extreme substitution rate heterogeneity. The orchid subtribe Calypsoinae exemplifies this, containing several lineages that have lost leaves and photosynthesis. In particular, relationships of the leafy Asian Oreorchis and the leafless American Corallorhiza have been contentious. Here we used nuclear sequence capture to resolve relationships within Calypsoinae and addressed the monophyly of Corallorhiza and Oreorchis, for which previous studies have highlighted conflicting patterns of monophyly or paraphyly, depending on the data analysed. Nuclear analyses provided strong support for a monophyletic Corallorhiza and paraphyletic Oreorchis, the latter with two strongly supported clades. As in previous studies, plastid analyses recovered strongly supported paraphyletic assemblages for both genera. Topology tests using plastid and nuclear relationships and data rejected the constrained topologies, further revealing strong cytonuclear conflict. Network-based analyses revealed a lack of evidence for hybridization, suggesting incomplete lineage sorting associated with biological and historical factors have driven intergenomic conflict. Additionally, we found that loci identified as putatively lost in holomycotrophic Corallorhiza species are functionally enriched for organellar functions. The study provides a strong case for the resurrection of Kitigorchis as the sister of Corallorhiza, with two species, Kitigorchis erythrochrysea and Kitigorchis indica, and highlights the challenges associated with phylogenetics of lineages containing mycoheterotrophs. 

Abstract Mycoheterotrophy is an alternative nutritional strategy whereby plants obtain sugars and other nutrients from soil fungi. Mycoheterotrophy and associated loss of photosynthesis have evolved repeatedly in plants, particularly in monocots. Although reductive evolution of plastomes in mycoheterotrophs is well documented, the dynamics of nuclear genome evolution remains largely unknown. Transcriptome datasets were generated from four mycoheterotrophs in three families (Orchidaceae, Burmanniaceae, Triuridaceae) and related green plants and used for phylogenomic analyses to resolve relationships among the mycoheterotrophs, their relatives, and representatives across the monocots. Phylogenetic trees based on 602 genes were mostly congruent with plastome phylogenies, except for an Asparagales + Liliales clade inferred in the nuclear trees. Reduction and loss of chlorophyll synthesis and photosynthetic gene expression and relaxation of purifying selection on retained genes were progressive, with greater loss in older nonphotosynthetic lineages. One hundred seventy-four of 1375 plant benchmark universally conserved orthologous genes were undetected in any mycoheterotroph transcriptome or the genome of the mycoheterotrophic orchid Gastrodia but were expressed in green relatives, providing evidence for massively convergent gene loss in nonphotosynthetic lineages. We designate this set of deleted or undetected genes Missing in Mycoheterotrophs (MIM). MIM genes encode not only mainly photosynthetic or plastid membrane proteins but also a diverse set of plastid processes, genes of unknown function, mitochondrial, and cellular processes. Transcription of a photosystem II gene (psb29) in all lineages implies a nonphotosynthetic function for this and other genes retained in mycoheterotrophs. Nonphotosynthetic plants enable novel insights into gene function as well as gene expression shifts, gene loss, and convergence in nuclear genomes.