Plastid phylogenomics reveals evolutionary relationships in the mycoheterotrophic orchid genusDipodiumand provides insights into plastid gene degeneration

Abstract

The orchid genusDipodiumR.Br. (Epidendroideae) comprises leafy autotrophic and leafless mycoheterotrophic species, the latter confined to sect.Dipodium. This study examined plastome degeneration inDipodiumin a phylogenomic and temporal context. Whole plastomes were reconstructed and annotated for 24Dipodiumsamples representing 14 species and two putatively new species, encompassing over 80% of species diversity in sect.Dipodium. Phylogenomic analysis based on 68 plastid loci including a broad outgroup sampling across Orchidaceae found sect.Leopardanthusas sister lineage to sect.Dipodium.Dipodium ensifolium, the only leafy autotrophic species in sect.Dipodiumwas found sister to all leafless, mycoheterotrophic species, supporting a single evolutionary origin of mycoheterotrophy in the genus. Divergence time estimations found thatDipodiumarose ca. 33.3 Ma near the lower boundary of the Oligocene and crown diversification commenced in the late Miocene, ca. 11.3 Ma. Mycoheterotrophy in the genus was estimated to have evolved in the late Miocene, ca. 7.3 Ma, in sect.Dipodium. The comparative assessment of plastome structure and gene degradation inDipodiumrevealed that plastidndhgenes were pseudogenised or physically lost in all Dipodium species, including in leafy autotrophic species of bothDipodiumsections. Levels of plastidndhgene degradation were found to vary among species as well as within species, providing evidence of relaxed selection for retention of the NADH dehydrogenase complex within the genus.Dipodiumexhibits an early stage of plastid genome degradation as all species were found to have retained a full set of functional photosynthesis-related genes and housekeeping genes. This study provides important insights into plastid genome degradation along the transition from autotrophy to mycoheterotrophy in a phylogenomic and temporal context.

Plastid phylogenomics reveals evolutionary relationships in the mycoheterotrophic orchid genus Dipodium and provides insights into plastid gene degeneration

“…for collection of plant material used in this study. A preprint of the manuscript was released online ( Goedderz et al., 2024 ; DOI: doi.org/10.1101/2024.02.05.578113).…”