Insights into chloroplast genome variation across Opuntioideae (Cactaceae)

Abstract

Chloroplast genomes (plastomes) are frequently treated as highly conserved among land plants. However, many lineages of vascular plants have experienced extensive structural rearrangements, including inversions and modifications to the size and content of genes. Cacti are one of these lineages, containing the smallest plastome known for an obligately photosynthetic angiosperm, including the loss of one copy of the inverted repeat (~25 kb) and the ndh genes suite, but only a few cacti from the subfamily Cactoideae have been sufficiently characterized. Here, we investigated the variation of plastome sequences across the second-major lineage of the Cactaceae, the subfamily Opuntioideae, to address 1) how variable is the content and arrangement of chloroplast genome sequences across the subfamily, and 2) how phylogenetically informative are the plastome sequences for resolving major relationships among the clades of Opuntioideae. Our de novo assembly of the Opuntia quimilo plastome recovered an organelle of 150,347 bp in length with both copies of the inverted repeats and the presence of all the ndh genes suite. An expansion of the large single copy unit and a reduction of the small single copy was observed, including translocations and inversion of genes as well as the putative pseudogenization of numerous loci. Comparative analyses among all clades within Opuntioideae suggested that plastome structure and content vary across taxa of this subfamily, with putative independent losses of the ndh gene suite and pseudogenization of genes across disparate lineages, further demonstrating the dynamic nature of plastomes in Cactaceae. Our plastome dataset was robust in determining relationships among major clades and subclades within Opuntioideae, resolving three tribes with high support: Cylindropuntieae, Tephrocacteae and Opuntieae. A plastome-wide survey for highly informative phylogenetic markers revealed previously unused regions for future use in Sanger-based studies, presenting a valuable dataset with primers designed for continued evolutionary studies across Cactaceae. These results bring new insights into the evolution of plastomes in cacti, suggesting that further analyses should be carried out to address how ecological drivers, physiological constraints and morphological traits of cacti may be related with the common rearrangements in plastomes that have been reported across the family.

Complete Chloroplast Genome of Rhipsalis baccifera, the only Cactus with Natural Distribution in the Old World: Genome Rearrangement, Intron Gain and Loss, and Implications for Phylogenetic Studies

“…Moreover, we observed another inversion of the SSC region of R. baccifera chloroplast genome in comparison to the structure of most angiosperms' cp genomes. This was also observed in the cp genome of C. gigantea and M. solisioides but was not the case in Opuntia as in a recent study of O. quimilo [46]. We suggest that this might be a unique feature of subfamily Cactoideae.…”

“…The loss of both clpP gene and rps12 gene in the same chloroplast genome was first observed in, Cicer arietinum [38] and was described as unique. The petB gene in R. baccifera cp genome has an intron as is the case in P. oleracea and T. paniculatum, whereas this gene lacks introns in most cp genome of members of Cactaceae family so far studied, but was observed in a recent study to be present in Opuntia quimilo [46]. Assuming R. baccifera has gained the petB gene intron, then R. baccifera might have gained this intron during its evolution to enhance the expression level of this petB gene.…”

Phylogenetics of Leptocereus (Cactaceae) on Hispaniola: clarifying species limits in the L. weingartianus complex and a new species from the Sierra de Bahoruco

“…Whole genomic DNAs of all taxa were extracted using a standard CTAB protocol with silica column cleaning (see Majure et al 2019 ; Köhler et al 2020 ). DNAs were resuspended in 300 ul of TE (Tris-EDTA) buffer (pH 8.0), and DNA quantity was analyzed on a Qubit 2.0 Fluorometer.…”

Complete chloroplast genome sequence and phylogenetic analysis of dragon fruit (Selenicereus undatus (Haw.) D.R.Hunt)

“… 2019 ; Kohler et al. 2020 ), including Carnegiea gigantea (113,064 bp), Cylindropuntia bigelovii (125,158 bp), Opuntia quimilo (150,374 bp), Mammillaria albiflora (110,789 bp), Mammillaria albiflora (108,561 bp), Mammillaria crucigera (115,505 bp), Mammillaria huitzilopochtli (115,886 bp), Mammillaria solisioides (115,356 bp), Mammillaria supertexta (116,175 bp), and Mammillaria zephyranthoides (107,343 bp). Compared with these species, the chloroplast genome of S. undatus is only smaller than that of Opuntia quimilo , which has a very long LSC region (104,475 bp) accounting for 67.48% of its entire chloroplast genome.…”