Selective regime shifts and intracellular gene transfer in the organellar genomes of the mycoheterotrophic orchid Galeola nudifolia Lour. (Orchidaceae)

Abstract

The transition to mycoheterotrophy has occurred repeatedly in Orchidaceae and is expected to impose contrasting evolutionary signatures on the plastome and mitogenome. However, quantitative comparisons between these two organellar compartments remain scarce, particularly within the Vanilloideae. Here, we report the first paired plastome and mitogenome of Galeola nudifolia Lour., a fully mycoheterotrophic orchid in the tribe Vanilleae (Vanilloideae), and integrate these data with published organellar genomes across photosynthetic and mycoheterotrophic Orchidaceae. The 852,490 bp mitogenome (24 linear contigs) encodes 38 protein-coding genes, eight tRNA genes, and three rRNA genes; the loss of rpl 2 was confirmed by targeted re-assembly. The 101,856 bp plastome retained a typical quadripartite structure but exhibited extensive gene loss in photosynthesis-related genes. Forty-two plastome-derived regions, corresponding to 20 plastid protein-coding genes, were detected in the mitogenome; none retained intact open reading frames, indicating that physical transfer was extensive but functional transfer was absent. Branch-model (codeml) and RELAX analyses indicated a contrasting selective regime between the two genomes: relaxation of purifying selection in plastome genes was concentrated in the photosynthesis- and ATP synthesis-related loci (with atp I significant after multiple-testing correction, p adj  = 0.033, and further ATP synthase genes supported by RELAX), whereas the mitogenome largely retained purifying selection. Predicted RNA-editing density showed no substantial differences between trophic groups, though this analysis is exploratory. In the plastome-based phylogeny, Cyrtosia was recovered as paraphyletic with respect to G. nudifolia ; however, given the limited sampling and weak support, this arrangement is preliminary and requires confirmation with denser sampling and nuclear data.