Platanthera zijinensis and Platanthera guangdongensis Genome sequencing and assembly. Platanthera zijinensis and Platanthera guangdongensis

Mycoheterotrophs exist in almost every major lineage of terrestrial plants, but the majority of them are found in the family Orchidaceae. To improve our understanding of the origin and evolution of mycoheterotrophic plants, we here present the genome sequences of two sibling orchid species, estimated to have diverged approximately 22 Mya, namely the leafy, partially mycoheterotrophic Platanthera zijinensi with roots, and the leafless, fully mycoheterotrophic P. guangdongensis without roots. For both species we obtained chromosome-scale assemblies and found that their large genome sizes are mainly due to the expansion of retrotransposons Gypsy and Copia. Comparative analysis with other, previously sequenced orchids shows that mycoheterotrophy in Orchidaceae is associated with increased substitution rates and gene loss. Specifically, the fully mycoheterotrophic orchids P. guangdongensis and Gastrodia elata have lost many, if not most genes involved in photosynthesis. Also, deletion of most photoreceptor genes and auxin transporter genes might be linked to the unique leafless and rootless 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 the fully mycoheterotrophic P. guangdongensis, different from photosynthetic orchids, keep 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.