A phoenix in the greenhouse: characterization and phylogenomics of complete chloroplast genomes sheds light on the putatively extinct-in-the-wild Solanum ensifolium (Solanaceae).

Abstract

Background: The genus Solanum is a diverse group of flowering plants with significant economic importance. Within this genus, the subgenus Leptostemonum, comprising spiny solanums, is particularly noteworthy due to its high species diversity and endemism. Solanum ensifolium, a member of this subgenus, is a critically endangered species endemic to Puerto Rico and known locally as erubia. The species survives in greenhouses and botanical gardens and is thought to be extinct in the wild, but with reintroduction efforts in progress. Despite its conservation status, genomic data for S. ensifolium remains scarce, limiting our understanding of its evolutionary history and potential adaptations.

Results: The S. ensifolium chloroplast genome (155,295 bp) exhibits a typical quadripartite structure and encodes 151 genes, including 95 protein-coding genes involved in photosynthesis, transcription, translation, and other essential cellular functions. Gene content and genome organization are similar to those observed in closely related Solanum species. Comparative genomic analysis of the annotated genome with that of closely related Solanum species revealed differences in nucleotide diversity between the large single-copy (LSC) and small single-copy regions (SSC), and the inverted repeat (IR) regions. Additionally, phylogenetic analyses confirmed placement of S. ensifolium within the Leptostemonum subgenus, affirming its suspected close relationship with S. crotonoides and S. aturense. Furthermore, of the three individuals of S. ensifolium for which chloroplast genomes were obtained, no genetic variation was observed.

Conclusions: The availability of the S. ensifolium chloroplast genome provides insights into its evolutionary history and conservation needs. Comparative genomics uncovered evolutionary differences in Solanum chloroplast genomes, including nucleotide diversity and structural variations. Phylogenetic analyses confirmed the close relationship between S. ensifolium and other Leptostemonum species. These findings enhance our understanding of this critically endangered species' evolution, guiding effective conservation strategies like using chloroplast variation to assess genetic diversity for ex situ conservation and reintroduction programs. The uniformity of the chloroplast genome in S. ensifolium may reveal that this species has undergone a genetic bottleneck. To prevent inbreeding depression and maintain evolutionary adaptability, efforts should be made to generate and preserve as much genetic diversity as possible.