Search

Simple Summary: Plastids are semi-autonomous plant organelles which play critical roles in photosynthesis, stress response, and storage. The plastid genomes (plastomes) in angiosperms are relatively conserved in quadripartite structure, but variable in size, gene content, and evolutionary rates of genes. The genus Crassula L. is the second-largest genus in the family Crassulaceae J.St.-Hil, that significantly contributes to the diversity of Crassulaceae. However, few studies have focused on the evolution of plastomes within Crassula. In the present study, we sequenced ten plastomes of Crassula: C. alstonii Marloth, C. columella Marloth & Schönland, C. dejecta Jacq., C. deltoidei Thunb., C. expansa subsp. fragilis (Baker) Toelken, C. mesembrianthemopsis Dinter, C. mesembryanthoides (Haw.) D.Dietr., C. socialis Schönland, C. tecta Thunb., and C. volkensii Engl. Through comparative studies, we found Crassula plastomes have unique codon usage and aversion patterns within Crassulaceae. In addition, genomic features, evolutionary rates, and phylogenetic implications were analyzed using plastome data. Our findings will not only reveal new insights into the plastome evolution of Crassulaceae, but also provide potential molecular markers for DNA barcoding. The genus Crassula is the second-largest genus in the family Crassulaceae, with about 200 species. As an acknowledged super-barcode, plastomes have been extensively utilized for plant evolutionary studies. Here, we first report 10 new plastomes of Crassula. We further focused on the structural characterizations, codon usage, aversion patterns, and evolutionary rates of plastomes. The IR junction patterns—IRb had 110 bp expansion to rps19—were conservative among Crassula species. Interestingly, we found the codon usage patterns of matK gene in Crassula species are unique among Crassulaceae species with elevated ENC values. Furthermore, subgenus Crassula species have specific GC-biases in the matK gene. In addition, the codon aversion motifs from matK, pafI, and rpl22 contained phylogenetic implications within Crassula. The evolutionary rates analyses indicated all plastid genes of Crassulaceae were under the purifying selection. Among plastid genes, ycf1 and ycf2 were the most rapidly evolving genes, whereas psaC was the most conserved gene. Additionally, our phylogenetic analyses strongly supported that Crassula is sister to all other Crassulaceae species. Our findings will be useful for further evolutionary studies within the Crassula and Crassulaceae. [ABSTRACT FROM AUTHOR]

• This study assembled and annotated four new plastomes from the Telephium clade. • Monophyletic Telephium clade further formed Hylotelephium and Rhodiola subclade. • No positive selection gene was observed but 19 genes had positive selection sites. • Codon usage was biased, shaped by natural selection, mutations and other factors. • 34 taxon-specific codon aversion motifs were identified from 49 plastid genes. The Telephium clade of the Crassulaceae family contains many medicinal, ornamental, and ecologically restorative plants. However, the phylogenetic relationships within the clade remain debated, and comprehensive analyses of codon usage and selection pressure in Telephium plastomes are limited. In this study, we assembled and annotated four plastomes and performed extensive analyses. The plastomes exhibited a typical quadripartite structure and high conservation. The lengths ranged from 151,357 bp to 151,641 bp with 134 genes identified. The GC content was the highest within IR, followed by LSC, and lowest in the SSC region. Meanwhile, a unique inversion was observed within the LSC region of Meterostachys sikokianus. Polymorphisms analysis revealed minimum nucleotide diversity in the IR regions, with over ten highly polymorphic regions identified. Phylogenetically, two subclades formed within the monophyletic Telephium clade, with Umbilicus as the sister group to the remaining Hylotelephium subclade members. Notably, no significant positive selection was found among the 79 plastid genes, which showed varying evolutionary patterns. However, 19 genes contained codons under positive selection. The specific functions of these sites require further investigation. Synonymous codon usage was biased and conserved across the tested plastomes, shaped by natural selection, mutations and other factors of varying influence. We also identified 34 taxon-specific codon aversion motifs from 49 plastid genes. Our plastomic analyses elucidate phylogenetic relationships and evolutionary patterns in this medicinal clade, providing a foundation for further research on these ecologically and pharmaceutically important plants. [ABSTRACT FROM AUTHOR]