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Group I and II introns are large catalytic RNAs (ribozymes) that are frequently encountered in fungal mitochondrial genomes. The discovery of respiratory mutants linked to intron splicing defects demonstrated that for the efficient removal of organellar introns there appears to be a requirement of protein splicing factors. These splicing factors can be intron-encoded proteins with maturase activities that usually promote the splicing of the introns that encode them (cis-acting) and/or nuclear-encoded factors that can promote the splicing of a range of different introns (trans-acting). Compared to plants organellar introns, fungal mitochondrial intron splicing is still poorly explored, especially in terms of the synergy of nuclear factors with intron-encoded maturases that has direct impact on splicing through their association with intron RNA. In addition, nuclear-encoded accessory factors might drive the splicing impetus through translational activation, mitoribosome assembly, and phosphorylation-mediated RNA turnover. This review explores protein-assisted splicing of introns by nuclear and mitochondrial-encoded maturases as a means of mitonuclear interplay that could respond to environmental and developmental factors promoting phenotypic adaptation and potentially speciation. It also highlights key evolutionary events that have led to changes in structure and ATP-dependence to accommodate the dual functionality of nuclear and organellar splicing factors.

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Introduction: Many members of the Ophiostomatales are of economic importance as they are bark-beetle associates and causative agents for blue stain on timber and in some instances contribute towards tree mortality. The taxonomy of these fungi has been challenging due to the convergent evolution of many traits associated with insect dispersal and a limited number of morphological characters that happen to be highly pleomorphic. This study examines the mitochondrial genomes for three members of Leptographium sensu lato [Leptographium aureum (also known as Grosmannia aurea), Grosmannia fruticeta (also known as Leptographium fruticetum), and Leptographium sp. WIN(M)1376)]. Methods: Illumina sequencing combined with gene and intron annotations and phylogenetic analysis were performed. Results: Sequence analysis showed that gene content and gene synteny are conserved but mitochondrial genome sizes were variable: G. fruticeta at 63,821 bp, Leptographium sp. WIN(M)1376 at 81,823 bp and L. aureum at 104,547 bp. The variation in size is due to the number of introns and intron-associated open reading frames. Phylogenetic analysis of currently available mitochondrial genomes for members of the Ophiostomatales supports currently accepted generic arrangements within this order and specifically supports the separation of members with Leptographium-like conidiophores into two genera, with L. aureum grouping with Leptographium and G. fruticeta aligning with Grosmannia. Discussion: Mitochondrial genomes are promising sequences for resolving evolutionary relationships within the Ophiostomatales.

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Urnula craterium (Schwein.) Fr. (1851) has been reported from North America, Europe, and Asia, and can be a pathogen on various hardwood species. In this study, we investigated the mitochondrial genome of U. craterium. The biology and taxonomy of this fungus is poorly studied and there are no mitogenomes currently available for any member of the Sarcosomataceae (Order Pezizales). The complete mitogenome of U. craterium comprises 43 967 bps and encodes 14 protein-coding genes, a complete set of tRNAs and rRNA genes. A novel feature of the mitogenome is the presence of a single subunit DNA polymerase-coding region that is typically associated with linear invertron-type plasmids. The mitogenome may offer insights into the evolution of mitogenomes among members of the Pezizales with regards to gene content and order, mobile elements, and genome sizes.

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RESUMEN

Introns are ubiquitous in eukaryotic genomes and have long been considered as 'junk RNA' but the huge energy expenditure in their transcription, removal, and degradation indicate that they may have functional significance and can offer evolutionary advantages. In fungi, plants and algae introns make a significant contribution to the size of the organellar genomes. Organellar introns are classified as catalytic self-splicing introns that can be categorized as either Group I or Group II introns. There are some biases, with Group I introns being more frequently encountered in fungal mitochondrial genomes, whereas among plants Group II introns dominate within the mitochondrial and chloroplast genomes. Organellar introns can encode a variety of proteins, such as maturases, homing endonucleases, reverse transcriptases, and, in some cases, ribosomal proteins, along with other novel open reading frames. Although organellar introns are viewed to be ribozymes, they do interact with various intron- or nuclear genome-encoded protein factors that assist in the intron RNA to fold into competent splicing structures, or facilitate the turn-over of intron RNAs to prevent reverse splicing. Organellar introns are also known to be involved in non-canonical splicing, such as backsplicing and trans-splicing which can result in novel splicing products or, in some instances, compensate for the fragmentation of genes by recombination events. In organellar genomes, Group I and II introns may exist in nested intronic arrangements, such as introns within introns, referred to as twintrons, where splicing of the external intron may be dependent on splicing of the internal intron. These nested or complex introns, with two or three-component intron modules, are being explored as platforms for alternative splicing and their possible function as molecular switches for modulating gene expression which could be potentially applied towards heterologous gene expression. This review explores recent findings on organellar Group I and II introns, focusing on splicing and mobility mechanisms aided by associated intron/nuclear encoded proteins and their potential roles in organellar gene expression and cross talk between nuclear and organellar genomes. Potential application for these types of elements in biotechnology are also discussed.

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