Exploring Mitochondrial Heterogeneity and Evolutionary Dynamics in Thelephora ganbajun through Population Genomics

Abstract

Limited exploration in fungal mitochondrial genetics has uncovered diverse inheritance modes. The mitochondrial genomes are inherited uniparentally in the majority of sexual eukaryotes, our discovery of persistent mitochondrial heterogeneity within the natural population of the basidiomycete fungus Thelephora ganbajun represents a significant advance in understanding mitochondrial inheritance and evolution in eukaryotes. Here, we present a comprehensive analysis by sequencing and assembling the complete mitogenomes of 40 samples exhibiting diverse cox1 heterogeneity patterns from various geographical origins. Additionally, we identified heterogeneous variants in the nad5 gene, which, similar to cox1, displayed variability across multiple copies. Notably, our study reveals a distinct prevalence of introns and homing endonucleases in these heterogeneous genes. Furthermore, we detected potential instances of horizontal gene transfer involving homing endonucleases. Population genomic analyses underscore regional variations in mitochondrial genome composition among natural samples exhibiting heterogeneity. Thus, polymorphisms in heterogeneous genes, introns, and homing endonucleases significantly influence mitochondrial structure, structural variation, and evolutionary dynamics in this species. This study contributes valuable insights into mitochondrial genome architecture, population dynamics, and the evolutionary implications of mitochondrial heterogeneity in sexual eukaryotes.

Keywords: comparative population genomics; mitogenome; persistent heteroplasmy; wild edible fungi.

Figure 1

Structure of standard protein-encoding gene (PCG) and distribution of the numbers of introns and multicopy genes on a Bayesian inference (BI) tree constructed from 13 conserved PCGs and rps3. Note: Different colors indicate different genes, different lengths indicate the size of genes, and arrows indicate the direction of genes.

Figure 2

Relative copy number of mitochondrial multicopy genes. Notes: Names in the x-axis are the names of tested HTs by RT-PCR, fragments starting with C are the multicopy genes of cox1, and those starting with N are from nad5. The distributions of these multi-copy genes are listed in Table S2.

Figure 3

Maximum Likelihood (ML) phylogenetic analysis of all intron types (Nucleic acid sequences) from 40 T. ganbajun samples in this study. Notes: Due to the large number (707), the introns of the sequence duplicates are kept, and the excess sequences are deleted. The different colors of the inner ring indicate different types of introns, and the dark blue bar graph of the outer ring indicates the corresponding number of introns.

Figure 4

Correlation analysis of mitochondrial genome structure, composition, size of homing endonuclease genes and introns, and the existence of multicopy heterogeneous types in cox1 and nad5. The sizes of the circle suggest R² value. Red and blue colors indicate the correlation. The blue color represents the trend of positive correlation, red represents a negative correlation.

Figure 5

Phylogenetic analysis of horizontal gene transfer (HGT) of homing endonucleases. Note: Different colors in the inner circle indicate different types of homing endonucleases, and different colors in the outer circle indicate species in different families.

Figure 6

Genetic clusters and their distributions among four geographic regions obtained from the PCoA (a–d) and STRUCTURE (e–h) analyses of different datasets of mitochondrial genomes. Different colors represent different genetic clusters.