Intronic and plasmid-derived regions contribute to the large mitochondrial genome sizes of Agaricomycetes

Abstract

Sizes of mitochondrial genomes vary extensively between fungal species although they typically contain a conserved set of core genes. We have characterised the mitochondrial genome of the conifer root rot pathogen Heterobasidion irregulare and compared the size, gene content and structure of 20 Basidiomycete mitochondrial genomes. The mitochondrial genome of H. irregulare was 114, 193 bp and contained a core set of 15 protein coding genes, two rRNA genes and 26 tRNA genes. In addition, we found six non-conserved open reading frames (ORFs) and four putative plasmid genes clustered in three separate regions together with 24 introns and 14 intronic homing endonuclease genes, unequally spread across seven of the core genes. The size differences among the 20 Basidiomycetes can largely be explained by length variation of intergenic regions and introns. The Agaricomycetes contained the nine largest mitochondrial genomes in the Basidiomycete group and Agaricomycete genomes are significantly (p < 0.001) larger than the other Basidiomycetes. A feature of the Agaricomycete mitochondrial genomes in this study was the simultaneous occurrence of putative plasmid genes and non-conserved ORFs, with Cantharellus cibarius as only exception, where no non-conserved ORF was identified. This indicates a mitochondrial plasmid origin of the non-conserved ORFs or increased mitochondrial genome dynamics of species harbouring mitochondrial plasmids. We hypothesise that two independent factors are the driving forces for large mitochondrial genomes: the homing endonuclease genes in introns and integration of plasmid DNA.

Mitogenomes of Two Phallus Mushroom Species Reveal Gene Rearrangement, Intron Dynamics, and Basidiomycete Phylogeny

“…Variation in introns, intergenic regions, and free-standing ORFs were the three most important factors and had a major influence on the mitogenome size of these species. The influence of these factors on mitogenome length has been confirmed by other research on fungal mitogenomes (Himmelstrand et al, 2014;Chen et al, 2019). Introns accounted for 58.7% of the length of the P. indusiatus mitogenome, and this was greater than any of the other 43 species.…”

Complete mitochondrial genome of the Verticillium-wilt causing plant pathogen Verticillium nonalfalfae

“…Another more frequent way of comparing mitochondrial genomes is inter-species, rather than an intra-species approach [ 13 , 26 , 27 , 56 , 60 ]. An analysis of two related soybean rust pathogens based on their mitochondrial genomes is such an example [ 14 ].…”

“…For example, [ 25 ] reports that intronic regions in mitochondrial genomes can be present in different numbers and lengths, from a few bp up to 5 kb. Despite these size differences, mitochondrial genomes still predominantly contain the conserved set of protein-coding genes [ 26 ]. Other sources of fungal mitochondrial genome variation are variability in the mitochondrial gene order, presence of repeats and variable numbers of ORFs with an unknown function.…”

Intron Derived Size Polymorphism in the Mitochondrial Genomes of Closely Related Chrysoporthe Species

“…The diversity of mt genomes is evident among Ascomycetes, where the smallest mt genome is 18,512 bp for Hanseniaspora uvarum [ 32 ] and the largest is 203,051 bp for Sclerotinia borealis [ 33 ]. These size differences appear to be directly correlated to the numbers and sizes of introns, the presence of dispersed repetitive regions, and new genes introduced through horizontal transfer [ 25 , 34 – 36 ]. The divergence of these mt genomes is also associated with rearrangements in gene order [ 15 , 22 ] and the presence or absence of auto-replicating plasmids [ 30 ].…”