Assembling the puzzle: Complete chloroplast genome sequences of Discocactus bahiensis Britton & Rose and Melocactus ernestii Vaupel (Cactaceae) and their evolutionary significance

Abstract

Discocactus and Melocactus are representatives of Core Cactoideae II BCT clade (Browningieae, Cereeae and Trichocereeae clade) and consist of 14 and 50 species, respectively. Both genera occur in South America, but Melocactus distribution extends through Central America and the West Indies. Although the Cactaceae family stands out for having highly rearranged plastomes, with particular gene organization, small or divergent inverted repeats (IRs) and IR loss, the plastome variation in the BCT clade is unknown. In this study, we assembled plastomes of Discocactus bahiensis and Melocactus ernestii and compared them with other available plastomes of Cactoideae (Carnegiea gigantea, and species of the genera Mammillaria and Rhipsalis) as well as with canonical plastomes of members of the order Caryophyllales (Portulaca oleracea and Spinacea oleracea). The plastomes of D. bahiensis (128,733-bp) and M. ernestii (130,703-bp) showed a quadripartite structure with 17 rearrangements when compared to those of P. oleracea and S. oleracea. Thus, twenty-eight genes were transferred from the LSC (large single copy) region to the IRs and 12 genes from the IRs to the LSC or SSC (small single copy) regions. Twenty-seven syntenic blocks were identified, evidencing a large number of rearrangements within the subfamily Cactoideae. These rearrangements could not be explained by the absence of IR regions nor the number of repeats. By comparing plastomes of D. bahiensis and M. ernestii, we propose new regions for phylogenetic inferences for the subfamily Cactoideae, for Discocactus and Melocactus, and for related groups.

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

“…Further, independent losses of the inverted repeat and the ndh gene suite have been reported in unrelated lineages (e.g., the saguaro cactus, Carnegiea gigantea, the cardo-ananá, Cereus fernambucensis, and the Chacoan-leafy-cactus, Quiabentia verticilata, Sanderson et al, 2015;Köhler et al, 2020;Amaral et al, 2021). Additionally, nearly all studied species have shown distinct features involving expansion or contractions of the IR region, rearrangements, and gene losses or pseudogenization (Solórzano et al, 2019;Oulo et al 2020;Amaral et al 2021;Silva et al, 2021;Almeida et al, 2021;Dalla Costa et al 2022;Qin et al 2022). Nonetheless, just a small fraction of cactus diversity (< 5%) has had their plastome analyzed in a comparative framework.…”

“…Nonetheless, beyond their morphological, physiological, and ecological aspects, molecular components also may reveal intriguing traits of cacti. The study of entire cactus plastomes was initiated recently (Sanderson et al, 2015), and since then, it has been revealed that plastomes across cacti have undergone significant changes in gene content, order, and structure compared to canonical angiosperm references (Majure et al, 2019;Solórzano et al, 2019;Köhler et al, 2020;Oulo et al 2020;Amaral et al, 2021;Silva et al, 2021;Almeida et al, 2021;Dalla Costa et al 2022;Qin et al 2022;Yu et al, 2023). Cactaceae seem to have the smallest plastome for an obligately photosynthetic angiosperm (~104-113 kb, Sanderson et al, 2015;Solórzano et al, 2019;Amaral et al, 2021).…”

“…The study of entire cactus plastomes was initiated recently (Sanderson et al ., 2015), and since then, it has been revealed that plastomes across cacti have undergone significant changes in gene content, order, and structure compared to canonical angiosperm references (Majure et al ., 2019; Solórzano et al ., 2019; Köhler et al ., 2020; Oulo et al . 2020; Amaral et al ., 2021; Silva et al ., 2021; Almeida et al ., 2021; Dalla Costa et al . 2022; Qin et al .…”

“…2020; Amaral et al . 2021; Silva et al ., 2021; Almeida et al ., 2021; Dalla Costa et al . 2022; Qin et al .…”

Extreme Reconfiguration of Plastid Genomes in Papaveraceae: Rearrangements, Gene Loss, Pseudogenization, IR Expansion, and Repeats

“…Although some atypical forms such as the extreme contraction of IRs, entire IR loss, and direct repeats (DRs) have been detected, the typical plastome architecture, including genome size, gene content, and gene order, is generally highly conserved, with two configurations usually coexisting and interchanging via IRs [5]. Nevertheless, an increasing number of studies have revealed a structural variation, including large-scale rearrangements in Fabaceae [6][7][8][9][10], Geraniaceae [11][12][13][14], Cactaceae [15,16], Campanulaceae [17,18], and Passifloraceae [19][20][21][22], as well as large IR contractions in Schisandraceae [23] and Lauraceae [24], and even loss of one IR region in Leguminosae [7,25], Geraniaceae [12], and Passifloraceae [20].…”