Plastome and transcriptome analysis reveals a degenerated photosynthesis-related pathway in the mycoheterotrophic vanilloid orchid Cyrtosia lindleyana.

Background: Achlorophyllous mycoheterotrophic plant species demonstrate drastic evolutionary shifts in their photosynthetic machinery as encoded in their chloroplast and nuclear genomes. We used next-generation sequencing to scrutinize these genome-level alterations linked to their distinctive life history. The plastome, a partial nuclear rDNA operon gene sequence, and the transcriptome of Cyrtosia lindleyana were assembled and characterized.

Results: The plastome, despite its reduction to 89,414 base pairs, maintained its quadripartite structure. We detected 63 potentially intact genes, of which nine protein-coding genes exhibited predicted RNA-editing sites. Relative to Vanilla pompona, three genes, rpl23, rps14, and rps19, had undergone positive selection (Ka/Ks > 1), and gene-block inversions were detected in both the large and small single-copy regions. Our plastome- and rDNA-based phylogenetic analyses strongly support a close relationship between C. lindleyana and C. septentrionalis. Transcriptome analysis indicated that the pathways for photosynthesis (KEGG ko00195), photosynthesis-antenna proteins (KEGG ko00196), carbon fixation in photosynthetic organisms (KEGG ko00710), and porphyrin metabolism (KEGG ko00860) in C. lindleyana remained intact. A BLAST analysis of the raw next-generation sequencing contigs revealed 46 contigs, presumed to originate from plastid genes, yet they remained unannotated in the plastome. Intriguingly, these putative plastid genes, absent from the plastome of C. lindleyana, also proved undetectable at the transcriptomic level, implying their non-functionality.

Conclusion: Our plastome and transcriptome analyses highlight evidence of gene degradation and loss in C. lindleyana, mirroring a process of photosynthetic capability degeneration. These genomic findings contribute to our understanding of the evolution of the Vanilloideae subfamily and mycoheterotrophy within the family Orchidaceae.