Characterization and Analysis of the Mitochondrial Genome of Common Bean (Phaseolus vulgaris) by Comparative Genomic Approaches

Abstract

The common bean (Phaseolus vulgaris) is a major source of protein and essential nutrients for humans. To explore the genetic diversity and phylogenetic relationships of P. vulgaris, its complete mitochondrial genome (mitogenome) was sequenced and assembled. The mitogenome is 395,516 bp in length, including 31 unique protein-coding genes (PCGs), 15 transfer RNA (tRNA) genes, and 3 ribosomal RNA (rRNA) genes. Among the 31 PCGs, four genes (mttB, nad1, nad4L, and rps10) use ACG as initiation codons, which are altered to standard initiation codons by RNA editing. In addition, the termination codon CGA in the ccmF_C gene is converted to UGA. Selective pressure analysis indicates that the ccmB, ccmF_C, rps1, rps10, and rps14 genes were under evolutionary positive selection. The proportions of five amino acids (Phe, Leu, Pro, Arg, and Ser) in the whole amino acid profile of the proteins in each mitogenome can be used to distinguish angiosperms from gymnosperms. Phylogenetic analyses show that P. vulgaris is evolutionarily closer to the Glycininae than other leguminous plants. The results of the present study not only provide an important opportunity to conduct further genomic breeding studies in the common bean, they also provide valuable information for future evolutionary and molecular studies of leguminous plants.

Keywords: Phaseolus vulgaris; common bean; comparative genomics; mitochondrial genome; phylogeny.

Figure 1

The master genome and two isomeric genomes observed from P. vulgaris mitogenome mediated by two pairs of large repeats (Contig15 and Contig40). The mt contigs were generated and selected from Newbler assembly software. MC and ISO mean the master and isomeric conformations, respectively. Arrows denote the sequence orientation of assembled contigs.

Figure 2

Circular map of the P. vulgaris mitogenome. Genes shown on the outside of the circle are transcribed clockwise, whereas genes on the inside are transcribed counterclockwise. GC content is represented on the inner circle by the dark gray plot. The asterisks besides genes denote intron-containing genes.

Figure 3

Codon usage pattern of P. vulgaris mitogenome compared with nine other higher plants. The proportion of each amino acid residues to the whole mitochondrial proteins is shown on the Y-axis. Ginkgo biloba and Cycas taitungensis are gymnosperms, while others are angiosperms.

Figure 4

Relative synonymous codon usage (RSCU) of P. vulgaris mitogenome. Codon families are on the X-axis. RSCU values are the number of times of a particular codon, relative to the number of times that the codon would be observed for a uniform synonymous codon usage.

Figure 5

K_a/K_s ratios for 31 protein coding genes of P. vulgaris, C. lanatus, V. vinifera, and A. thaliana. The blue, orange, and gray boxes indicate K_a/K_s ratios of P. vulgaris vs. C. lanatus, P. vulgaris vs. V. vinifera, and P. vulgaris vs. A. thaliana.

Figure 6

Predicted RNA editing sites of the P. vulgaris mitogenome compared with four other leguminous plants. RNA-editing sites are predicted on PREP-Mt sites (http://prep.unl.edu/) with the cut-off value of 0.2.

Figure 7

Frequency distribution of dispersed repeat in the P. vulgaris mitogenome compared with five other leguminous plants. The number of dispersed repeats in Phaseolus vulgaris, Glycine max Vicia faba, Vigna faba, Vigna angularis, Lotus japonicus, and Millettia pinnata mitogenomes are shown by blue, orange, gray, yellow, blue, and green, respectively.

Figure 8

Maximum likelihood phylogenies of P. vulgaris within Fabaceae. Relationships were inferred employing 26 conserved PCGs of 23 plant mitogenomes. Numbers on each node are bootstrap support values. NCBI accession numbers are listed in Table S2. Scale indicates number of nucleotide substitutions per site.

Figure 9

Distribution of PCGs in plant mitogenomes. White boxes indicate that the gene is not present in the mitogenome. The colors of genes indicate their corresponding categories. The colors of species represent the classes of rosids (orange), asterids (pink), monocotyledons (gold), gymnosperms (light blue), and liverworts (green).