Evidence of extensive intraspecific noncoding reshuffling in a 169-kb mitochondrial genome of a basidiomycetous fungus

Abstract

12Comparative genomics of fungal mitochondrial genomes (mitogenomes) have revealed 13 a remarkable pattern of rearrangement between and within major phyla owing to 14 horizontal gene transfer (HGT) and recombination. The role of recombination was 15 exemplified at a finer evolutionary time scale in basidiomycetes group of fungi as they 16 display a diversity of mitochondrial DNA (mtDNA) inheritance patterns. Here, we 17 assembled mitogenomes of six species from the Hymenochaetales order of 18 basidiomycetes and examined 59 mitogenomes from two genetic lineages of 19Pyrrhoderma noxium. Gene order is largely colinear while intergene regions are major 20 determinants of mitogenome size variation. Substantial sequence divergence was found 21 in shared introns consistent with high HGT frequency observed in yeasts, but we also 22 identified a rare case where an intron was retained in five species since speciation. In 23 contrast to the hyperdiversity observed in nuclear genomes of P. noxium, mitogenomes' 24 intraspecific polymorphisms at protein coding sequences are extremely low. Phylogeny 25 based on introns revealed turnover as well as exchange of introns between two lineages. 26Strikingly, some strains harbor a mosaic origin of introns from both lineages. Analysis 27 of intergenic sequence indicated substantial differences between and within lineages, 28 and an expansion may be ongoing as a result of exchange between distal intergenes. 29These findings suggest that the evolution in mtDNAs is usually lineage specific but 30 chimeric mitotypes are frequently observed, thus capturing the possible evolutionary 31 processes shaping mitogenomes in a basidiomycete. The large mitogenome sizes 32 reported in various basidiomycetes appear to be a result of interspecific reshuffling of 33 intergenes. 34 62 mitochondria are typically inherited from the larger gamete (Sandor, et al. 2018). For 63 basidiomycetes, various modes of mitochondrial inheritance may have been involved 64 in generating recombinant mitochondrial genotypes (Xu and He 2015; Xu and Wang 65 2015; Sandor, et al. 2018).66 67 In fungi, tight regulation of mtDNA transmission is part of molecular mechanisms 68 responsible for sex determination (mating). For model basidiomycetes yeast 69 Cryptococcus neoformans, mtDNA is inherited uniparentally from MATa parent 70 butbecomes biparental if the sex-specific homeodomain transcription factor sxi1α and 71 sxi2a are disrupted (Xu, et al. 2000; Yan and Xu 2003). A closely related species of C. 72 neoformans, C. gattii exhibited different inheritance patterns depending on strain 73 combinations and environmental factors such as temperature (Voelz, et al. 2013; Zhu, 74 et al. 2013; Wang, et al. 2015). For U. maydis, which has a tetrapolar mating system 75 similar to the model mushroom Coprinopsis cinerea, the mtDNA inheritance is 76 controlled by lga2 and rga2 of uncertain function encoded by a2 locus (homologous to 77 C. cinerea matB locus) (Fedler, et al. 2009).78 79 Strictly selecting mtDNA from only one parent du...

The Coevolution of Fungal Mitochondrial Introns and Their Homing Endonucleases (GIY-YIG and LAGLIDADG)

“…The assembly of the mitochondrion is achieved nowadays with the participation of the nucleus, after the transfer of a-proteobacterium’s preexisting genes to the nucleus in one “big” event ( Koonin 2006 ). Thus, the ancestral introns are “living” remnants of this procedure, 5) there are “new” introns usually found in mt genes of “higher” fungi which were acquired recently and provide evidence of the mt genome expansions ( Lee et al. 2019 ) and 6) free-standing HEGs were found at the beginning of evolution but nowadays in “higher” fungi are mostly “intron homing” and structurally stable.…”

Molecular diversity maintained by long-term balancing selection in mating loci defines multiple mating types in fungi

“…Scaffolds with less than 100 PacBio reads of support and less than 10 Kbp of length were removed from the final corrected genome assembly. T. abietinum ultrascaffolding was done using a Hymenochaetales species, P. noxium KPN91 PacBio genome assembly, as reference (Accession number GCA002287475, (Lee et al 2019). We first checked chromosome correspondence using D-Genies (Cabanettes and Klopp 2018) and manually ultrascaffolded in Geneious 6.1.6 (Kearse et al 2012).…”