To improve our understanding of the origin and evolution of mycoheterotrophic plants, we here present the chromosome-scale genome assemblies of two sibling orchid species: partially mycoheterotrophic Platanthera zijinensis and holomycoheterotrophic Platanthera guangdongensis. Comparative analysis shows that mycoheterotrophy is associated with increased substitution rates and gene loss, and the deletion of most photoreceptor genes and auxin transporter genes might be linked to the unique phenotypes of fully mycoheterotrophic orchids. Conversely, trehalase genes that catalyse the conversion of trehalose into glucose have expanded in most sequenced orchids, in line with the fact that the germination of orchid non-endosperm seeds needs carbohydrates from fungi during the protocorm stage. We further show that the mature plant of P. guangdongensis, different from photosynthetic orchids, keeps expressing trehalase genes to hijack trehalose from fungi. Therefore, we propose that mycoheterotrophy in mature orchids is a continuation of the protocorm stage by sustaining the expression of trehalase genes. Our results shed light on the molecular mechanism underlying initial, partial and full mycoheterotrophy.

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Calanthe s.l. is the most diverse group in the tribe Collabieae (Orchidaceae), which are pantropical in distribution. Illumina sequencing followed by de novo assembly was used in this study, and the plastid genetic information of Calanthe s.l. was used to investigate the adaptive evolution of this taxon. Herein, the complete plastome of five Calanthe s.l. species (Calanthe davidii, Styloglossum lyroglossa, Preptanthe rubens, Cephalantheropsis obcordata, and Phaius tankervilliae) were determined, and the two other published plastome sequences of Calanthe s.l. were added for comparative analyses to examine the evolutionary pattern of the plastome in the alliance. The seven plastomes ranged from 150,181 bp (C. delavayi) to 159,014 bp (C. davidii) in length and were all mapped as circular structures. Except for the three ndh genes (ndhC, ndhF, and ndhK) lost in C. delavayi, the remaining six species contain identical gene orders and numbers (115 gene). Nucleotide diversity was detected across the plastomes, and we screened 14 mutational hotspot regions, including 12 non-coding regions and two gene regions. For the adaptive evolution investigation, three species showed positive selected genes compared with others, C. obcordata (cemA), S. lyroglossa (infA, ycf1 and ycf2) and C. delavayi (nad6 and ndhB). Six genes were under site-specific positive selection in Calanthe s.l., namely, accD, ndhB, ndhD, rpoC2, ycf1, and ycf2, most of which are involved in photosynthesis. These results, including the new plastomes, provide resources for the comparative plastome, breeding, and plastid genetic engineering of orchids and flowering plants.