Comparative mitochondrial genomics of Terniopsis yongtaiensis in Malpighiales: structural, sequential, and phylogenetic perspectives

Abstract

Background: Terniopsis yongtaiensis, a member of the Podostemaceae family, is an aquatic flowering plant displaying remarkable adaptive traits that enable survival in submerged, turbulent habitats. Despite the progressive expansion of chloroplast genomic information within this family, mitochondrial genome sequences have yet to be reported.

Results: In current study, the mitochondrial genome of the T. yongtaiensis was characterized by a circular genome of 426,928 bp encoding 31 protein-coding genes (PCGs), 18 tRNAs, and 3 rRNA genes. Our comprehensive analysis focused on gene content, repeat sequences, RNA editing processes, intracellular gene transfer, phylogeny, and codon usage bias. Numerous repeat sequences were identified, including 130 simple sequence repeats, 22 tandem repeats, and 220 dispersed repeats. Phylogenetic analysis positioned T. yongtaiensis (Podostemaceae) within the Malpighiales order, showing a close relationship with the Calophyllaceae family, which was consistent with the APG IV classification. A comparative analysis with nine other Malpighiales species revealed both variable and conserved regions, providing insights into the genomic evolution within this order. Notably, the GC content of T. yongtaiensis was distinctively lower compared to other Malpighilales, primarily due to variations in non-coding regions and specific protein-coding genes, particularly the nad genes. Remarkably, the number of RNA editing sites was low (276), distributed unevenly across 27 PCGs. The dN/dS analysis showed only the ccmB gene of T. yongtaiensis was positively selected, which plays a crucial role in cytochrome c biosynthesis. Additionally, there were 13 gene-containing homologous regions between the mitochondrial and chloroplast genomes of T. yongtaiensis, suggesting the gene transfer events between these organellar genomes.

Conclusions: This study assembled and annotated the first mitochondrial genome of the Podostemaceae family. The comparison results of mitochondrial gene composition, GC content, and RNA editing sites provided novel insights into the adaptive traits and genetic reprogramming of this aquatic eudicot group and offered a foundation for future research on the genomic evolution and adaptive mechanisms of Podostemaceae and related plant families in the Malpighiales order.

Keywords: Terniopsis yongtaiensis; Evolution; Genome size variation; Mitochondrial genome; Phylogenetic.

Fig. 1

The circular map of the mitochondrial genome of Terniopsis yongtaiensis. Genes are color-coded based on their functional groups. GC content is represented on the inner circle by the dark gray plot

Fig. 2

Gene content in the Malpighiales plant mitochondrial genomes. Dark green boxes indicate the presence of an intact reading frame or folding structure while light gray boxes indicate the absence of an intact reading frame or folding structure. The numbers at the bottom of each gene group indicate the total number of intact genes for that species

Fig. 3

The repeat analysis of the Terniopsis yongtaiensis organelle genomes. (A) The repeat sequences identified in the chloroplast genome. (B) The repeat sequences identified in the mitochondrial genome. The innermost circle shows the dispersed repeats connected with green (chloroplast genome) and blue (mitochondrial genome) arcs from the center going outward. The center circle shows the tandem repeats as short bars. The outermost circle shows the microsatellite sequences identified using MISA. The scale is shown on the outermost circle, with intervals of 10 kb for chloroplast genome and 20 kb for mitochondrial genome

Fig. 4

The distribution of RNA editing sites across different genes of organelle genomes of Terniopsis yongtaiensis. The X axis shows the name of protein-coding genes, and the Y axis shows the number of predicted RNA editing sites

Fig. 5

Total number of editing sites in protein-coding genes across the 10 Malpighiales plants, involving 5 families (from top to bottom: Euphorbiaceae, Calophyllaceae, Podostemaceae, Passifloraceae, Salicaceae). Stacked bars showing numbers of editing sites at the first position (light green), second position (light blue), and the simultaneous occurrence in the first and second positions (dark blue) of codons, respectively

Fig. 6

Analysis of codon usage bias in Terniopsis yongtaiensis mitochondrial genomes. X-axis, codon families; Y-axis, the relative synonymous codon usage (RSCU) value. RSCU measures the likelihood of a specific codon being used among synonymous codons that encode the same amino acid and values greater than 1 indicate a higher frequency of usage for the codon

Fig. 7

Comparison of the chloroplast genome and mitochondrial genome of Terniopsis yongtaiensis. The blue and green outer arcs represent the mitochondrial genome (mtDNA) and chloroplast genome (cpDNA), respectively, and the inner green arcs show the homologous DNA fragments. The scale is shown on the outer arcs, with intervals of 20 kb

Fig. 8

The boxplots of dN/dS values of each mitochondrial gene in the 10 Malphighiales plants. The X axis shows the names of protein-coding genes, and the Y axis shows the dN/dS values

Fig. 9

Phylogenetic tree constructed using the data from 38 taxa based on 31 mitochondrial protein-coding genes. Different phyla and classes are highlighted in different colors, with the name of each phylum or class marked at the right of each highlight. Numbers above and below branches indicate RAxML (left) bootstrap probabilities (BP) and Bayesian (right) posterior probabilities (PP), respectively. Where * means BP = 100 or PP = 1.00

Fig. 10

Sizes and GC contents of mitochondrial genomes of 38 plants