The complete mitochondrial genomes of five critical phytopathogenic Bipolaris species: features, evolution, and phylogeny

Abstract

In the present study, three mitogenomes from the Bipolaris genus (Bipolaris maydis, B. zeicola, and B. oryzae) were assembled and compared with the other two reported Bipolaris mitogenomes (B. oryzae and B. sorokiniana). The five mitogenomes were all circular DNA molecules, with lengths ranging from 106,403 bp to 135,790 bp. The mitogenomes of the five Bipolaris species mainly comprised the same set of 13 core protein-coding genes (PCGs), two rRNAs, and a certain number of tRNAs and unidentified open reading frames (ORFs). The PCG length, AT skew and GC skew showed large variability among the 13 PCGs in the five mitogenomes. Across the 13 core PCGs tested, nad6 had the least genetic distance among the 16 Pleosporales species we investigated, indicating that this gene was highly conserved. In addition, the Ka/Ks values for all 12 core PCGs (excluding rps3) were < 1, suggesting that these genes were subject to purifying selection. Comparative mitogenomic analyses indicate that introns were the main factor contributing to the size variation of Bipolaris mitogenomes. The introns of the cox1 gene experienced frequent gain/loss events in Pleosporales species. The gene arrangement and collinearity in the mitogenomes of the five Bipolaris species were almost highly conserved within the genus. Phylogenetic analysis based on combined mitochondrial gene datasets showed that the five Bipolaris species formed well-supported topologies. This study is the first report on the mitogenomes of B. maydis and B. zeicola, as well as the first comparison of mitogenomes among Bipolaris species. The findings of this study will further advance investigations into the population genetics, evolution, and genomics of Bipolaris species.

Keywords: Bipolaris; Comparative analysis; Gene rearrangement; Intron; Mitogenome; Phylogenetic analysis.

Fig. 1

Circular maps of the five Bipolaris mitogenomes. Genes are represented by different colored blocks. Colored blocks outside each ring indicate that the genes are on the direct strand, while colored blocks within the ring indicates that the genes are located on the reverse strand. Genes on the direct strand are transcribed in a counterclockwise direction, while genes on the reverse strand are transcribed in a clockwise direction. The inner grayscale bar graph shows the GC content of the mitochondrial sequences. The circle inside the GC content graph marks the 50% threshold

Fig. 2

Putative secondary structures of tRNA genes identified in the mitogenomes of five Bipolaris species. The 29 tRNAs in green or red fonts represent tRNAs shared by the five Bipolaris species, while the tRNA in blue font represent tRNA only in Bipolaris maydis, B. zeicola, and B. sorokiniana. Residues conserved across the five mitogenomes are shown in green, while variable sites are shown in red

Fig. 3

Codon usage in the mitogenomes of five Bipolaris species. Frequency of codon usage is plotted on the y-axis. a: Bipolaris maydis, b: B. zeicola, c: B. oryzae, d: B. sorokiniana, e: B. cookie

Fig. 4

Position class (Pcl) information of cox1 genes in the 16 species. Introns in cox1 genes of 16 published mitogenomes were classified into different position classes (Pcls) using the cox1 gene of Bipolaris cookei as the reference. Each Pcl was constituted by introns inserted at the same position of corresponding cox1 gene and named according to its insertion site in the aligned corresponding reference sequence (nt). Phylogenetic positions of the 16 species were established using the Bayesian inference (BI) method and Maximum-Likelihood (ML) method based on combined mitochondrial data sets

Fig. 5

Genetic analysis of 12 core protein coding genes (excluding rps3 gene) in 16 Pleosporales species. The black straight and dotted lines indicate the magnitude of the median and mean values, respectively. K2P, the Kimura-2-parameter distance; Ka, the number of nonsynonymous substitutions per nonsynonymous site; Ks, the number of synonymous substitutions per synonymous site

Fig. 6

Sequence information of 13 core protein coding genes in the five Bipolaris species

Fig. 7

Mitochondrial gene arrangement analyses of the 16 Pleosporales species. The gene sequence begins with the cox1 gene and contains 13 core protein coding genes (PCGs) and two rRNA genes. The same gene were represented by same color blocks. Phylogenetic positions of the 16 species were established using the Bayesian inference (BI) method and Maximum-Likelihood (ML) method based on combined mitochondrial data sets

Fig. 8

Molecular phylogeny of 94 Ascomycota species based on Bayesian inference (BI) and Maximum likelihood (ML) analysis of 15 protein coding genes. Support values are Bayesian posterior probabilities (BPP) and bootstrap values (BS) placed before and after the slash, respectively. Asterisks indicate BPP and BS values of 1.00 and 100, respectively. Species and NCBI registry numbers of mitogenomes used for phylogenetic analyses can be provided in Additional file 1: Table S8