RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of holo-mycoheterotrophic plants

Summary • While photosynthesis is the most notable trait of plants, several lineages of plants (so-called holo-heterotrophs) have adapted to obtain organic compounds from other sources. The switch to heterotrophy leads to profound changes at the morphological, physiological and genomic levels. • Here, we characterize the transcriptomes of three species representing two lineages of mycoheterotrophic plants: orchids ( Epipogium aphyllum and Epipogium roseum ) and Ericaceae ( Hypopitys monotropa ). Comparative analysis is used to highlight the parallelism between distantly related holo-heterotrophic plants. • In both lineages, we observed genome-wide elimination of nuclear genes that encode proteins related to photosynthesis, while systems associated with protein import to plastids as well as plastid transcription and translation remain active. Genes encoding components of plastid ribosomes that have been lost from the plastid genomes have not been transferred to the nuclear genomes; instead, some of the encoded proteins have been substituted by homologs. The nuclear genes of both Epipogium species accumulated mutations twice as rapidly as their photosynthetic relatives; in contrast, no increase in the substitution rate was observed in H.monotropa . • Holo-heterotrophy leads to profound changes in nuclear gene content. The observed increase in the rate of nucleotide substitutions is lineage specific, rather than a universal phenomenon among non-photosynthetic plants.