Comparative and phylogenetic analyses using mitogenomes revealed gene re-arrangement of Boletaceae (Boletales)

Abstract

Boletaceae, the largest family in the Boletales order, is an ecologically and economically important group and the phylogenetic studies of this group need to be further developed. The mitogenome is an effective molecular marker for analysing phylogenetic relationships; however, Boletaceae mitochondrial genome (mitogenome) has been studied to a lesser extent. Thus, a comparative analysis of the mitogenomic features of seven Boletaceae species, representing seven distinct genera, was conducted. Phylogenetic relationships amongst these species within Boletales were reconstructed, based on the mitogenomic data. Highly consistent phylogenetic results within 34 Boletales species and two outgroups from Polyporales, based on mitogenomic datasets, were obtained using Maximum Likelihood and Bayesian Inference methods. Results of phylogenetic analyses revealed that Boletus, Retiboletus and Neoboletus were polyphyletic. Interestingly, species of Neoboletus with different bruising discolouration patterns were found in separate clades, suggesting this trait may reflect underlying genetic divergence. Furthermore, comparative and phylogenetic analyses revealed gene re-arrangements in mitogenomes of Boletaceae. This study is the first to report on complete mitogenomes of four genera (Amoenoboletus, Hourangia, Leccinum and Strobilomyces) and will help better understand the phylogenetic relationships of Boletales. Furthermore, addition of more new taxa is necessary to reconstruct a high-resolution tree.

Keywords: Boletaceae; conserved gene clusters; evolutionary rates; injury discolouration.

Figure 1.

Circular maps of mitogenomes of seven newly-sequenced Boletaceae species. Genes are represented with different colour blocks. Strand orientation is indicated by block position: genes on the direct strand are represented by colour blocks outside the ring, while genes on the reverse strand are denoted by colour blocks inside the ring.

Figure 2.

Relative synonymous codon usage analysis of 15 protein-coding genes of the seven Boletaceae mitogenomes. Codon families are provided on the x-axis.

Figure 3.

Genetic analysis of 15 core protein-coding genes amongst 26 Boletaceae mitogenomes. Ka, the number of non-synonymous substitutions per non-synonymous site; Ks, the number of synonymous substitutions per synonymous site.

Figure 4.

Heterogeneity of the sequence composition of mitogenomes in different datasets. The pairwise Aliscore values are indicated by coloured squares. Darker colours indicate full random similarity and lighter colours indicate the opposite. Arrows represent the order in which the species are arranged.

Figure 5.

Phylogenetic relationships of 34 Boletales, based on AA using MrBayes. The asterisk indicates BPP = 1. The polyphyletic genus is represented by the same colour. The seven newly-sequenced mitogenomes are highlighted in pink. Four colours show the four subfamilies.

Figure 6.

Synteny analysis of the 26 Boletaceae mitogenomes. Homologous regions between different Boletaceae species are represented by the same colour blocks and connected by the same colour lines. The asterisk indicates BPP = 1. The seven newly-sequenced mitogenomes are highlighted in pink. The polyphyletic genus is represented by the same colour.

Figure 7.

Gene order of 26 Boletaceae mitogenomes. The 15 core PCGs and 2 rRNA genes are included in the gene arrangement, starting from the cox1 gene. The coloured blocks indicate different categories of genes. The asterisk indicates BPP = 1. The seven newly-sequenced mitogenomes are highlighted in pink. The polyphyletic genus is represented by the same colour. The triangles represent the duplication of this gene in the mitogenome.