Comparative analysis of the mitogenomes of multiple species of Fagaceae, with special focus on Quercus gilva

Abstract

Background: Quercus, as the most abundant and widely distributed genus within the family Fagaceae, has been extensively studied at nuclear genome and plastome. However, mitogenome studies in Quercus remain scarce. In this study, we assemble and annotate the mitogenome of Quercus gilva based on Illumina and Nanopore data. Additionally, we explore the structural features of its mitogenome and provide comprehensive analyses of the phylogeny and evolution of Fagaceae.

Results: The Q. gilva mitogenome consists of four molecules (three circular molecules and one linear molecule) with 490,015 bp in total length and 45.68% in guanine-cytosine (GC) content. The mitogenome encodes 59 genes, including 37 protein-coding genes (PCGs), 19 transfer RNA genes (tRNAs), and three ribosomal RNA genes (rRNAs). We also examine the repeat sequences, codon usage bias, RNA editing sites, and endosymbiotic gene transfer in the mitogenome. The wide distribution of repeat sequences is a key factor in mitogenome rearrangement. These is widespread gene transfer among the mitogenome, plastome, and nuclear genome of Q. gilva. Comparative genomic analyses of the 11 Fagaceae mitogenomes reveal significant structural variations in size and gene loss. Synteny analysis further indicates extensive genome rearrangements and inversions within the 11 mitogenomes. However, analyses of nucleotide diversity (Pi) and nonsynonymous and synonymous substitution ratio (Ka/Ks) values reveal a low rate of evolution in the mitogenomes of Fagaceae. Finally, phylogenetic analysis based on 12 conserved mitochondrial PCGs of 40 taxa strongly supports the classification of Fabids.

Conclusions: In this study, the mitogenome of Q. gilva is newly assembled, providing important genomic resources for the phylogeny, resource conservation and development of Quercus. At the same time, the study of structural variation among the mitogenomes of Fagaceae species also help to elucidate the formation mechanism of mitogenome structural diversity.

Keywords: Quercus; Endosymbiotic gene transfer; Mitogenome; RNA editing site.

Fig. 1

Genome map of the Quercus gilva mitogenome. Genes outside the circle and on the line are transcribed in the clockwise direction, while genes inside the circle and below the line are transcribed in the counterclockwise direction. The genes belonging to different functional groups are identified by different colors

Fig. 2

The repeats of the Q. gilva mitogenome. (A) Total number of repeats across various types; (B) Distribution of dispersed repeat sequences by length categories (30–39 bp, 40–49 bp, 50–59 bp, and > 60 bp); (C) Circos plot showing the distribution of all repeats. The outermost circle represents the Q. gilva mitogenome, while the layers from the outside to the inside illustrate the distribution of SSRs, TRSs, and DRSs, respectively; (D) Proportion of all repeats located in different genomic regions. SSRs, simple sequence repeats; TRSs, tandem repeat sequences; DRSs, dispersed repeat sequences; IGS, intergenic spacer regions

Fig. 3

Characteristics of RNA editing sites predicted in the 36 PCGs of the Q. gilva mitogenome. (A) The number of RNA editing sites predicted in the PCGs. (B) The distribution of amino acid changes resulting from RNA editing events

Fig. 4

Schematic representations of MTPTs and NUMTs of Q. gilva. (A) Endosymbiotic gene transfer between the mitogenome and plastome. (B) Endosymbiotic gene transfer between the mitogenome and nuclear genome. The green, blue, and orange arcs represent the plastome, mitogenome, and nuclear genome, respectively. And the inner colored lines connecting the arcs indicate MTPTs and NUMTs, with different colors representing the level of the sequence identity. MTPT, mitochondrial plastid transferred fragments; NUMT, nuclear mitochondrial transferred fragments

Fig. 5

Collinearity analysis of the mitogenomes of 11 Fagaceae species. The red arc area implies inversion, whereas the gray area represents high homology

Fig. 6

The Pi values (A) and Ka/Ks ratio (B) of 30 common mitogenome PCGs among Fagaceae. The box plot represents the distribution of Ka/Ks values for all pairwise comparison in the data. Pi, nucleotide diversity; Ka/Ks, nonsynonymous and synonymous substitution ratio

Fig. 7

Phylogenetic tree of 40 angiosperms based on 12 conserved mitochondrial PCGs. The number at each node is the bootstrap support values