More than a prickly morphology: plastome variation in the prickly pear cacti (Opuntieae)

Abstract

Plastid genomes (plastomes) have long been recognized as highly conserved in their overall structure, size, gene arrangement and content among land plants. However, recent studies have shown that some lineages present unusual variations in some of these features. Members of the cactus family are one of these lineages, with distinct plastome structures reported across disparate lineages including gene losses, inversions, boundary movements, or loss of the canonical inverted repeat (IR) region. Here, we further investigated plastome features of the tribe Opuntieae, the remarkable prickly pear cacti, which represent a diverse and important lineage of Cactaceae. We assembled the plastome of 43 species, representing a comprehensive sampling of the tribe including all seven genera. Plastomes varied considerably in length from 121 kbp to 162 kbp, with striking differences in the content and size of the IR region (contraction and expansion events), including the lack of the canonical IR in some lineages, and the pseudogenization or loss of some genes. Overall, nine different types of plastomes were reported deviating in the presence of the IR region or the genes contained in the IR. Plastomes sequences resolved phylogenetic relationships within major clades of Opuntieae but presented some contentious nodes depending on the data set analyzed (e.g., whole plastome vs. genes only). Incongruence analyses revealed that few plastome regions are supporting the most likely topology, while disputing topologies are driven by a handful of plastome markers, which may be the result of hard recalcitrant nodes in the phylogeny or by the lack of phylogenetic signal in certain markers. Our study reveals a dynamic nature of plastome evolution across closely related lineages, shedding light on peculiar features of cactus plastomes. Variation of plastome types across Opuntieae is remarkable in size, structure, and content, and can be important for the recognition of species in some major clades. Unraveling connections between the causes of plastome variation and the consequences on species biology, ecology, diversification, and adaptation, is a promising endeavor.