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Global Characterization of Fungal Mitogenomes: New Insights on Genomic Diversity and Dynamism of Coding Genes and Accessory Elements.

ABSTRACT: Fungi comprise a great diversity of species with distinct ecological functions and lifestyles. Similar to other eukaryotes, fungi rely on interactions with prokaryotes and one of the most important symbiotic events was the acquisition of mitochondria. Mitochondria are organelles found in eukaryotic cells whose main function is to generate energy through aerobic respiration. Mitogenomes (mtDNAs) are double-stranded circular or linear DNA from mitochondria that may contain core genes and accessory elements that can be replicated, transcribed, and independently translated from the nuclear genome. Despite their importance, investigative studies on the diversity of fungal mitogenomes are scarce. Herein, we have evaluated 788 curated fungal mitogenomes available at NCBI database to assess discrepancies and similarities among them and to better understand the mechanisms involved in fungal mtDNAs variability. From a total of 12 fungal phyla, four do not have any representative with available mitogenomes, which highlights the underrepresentation of some groups in the current available data. We selected representative and non-redundant mitogenomes based on the threshold of 90% similarity, eliminating 81 mtDNAs. Comparative analyses revealed considerable size variability of mtDNAs with a difference of up to 260 kb in length. Furthermore, variation in mitogenome length and genomic composition are generally related to the number and length of accessory elements (introns, HEGs, and uORFs). We identified an overall average of 8.0 (0-39) introns, 8.0 (0-100) HEGs, and 8.2 (0-102) uORFs per genome, with high variation among phyla. Even though the length of the core protein-coding genes is considerably conserved, approximately 36.3% of the mitogenomes evaluated have at least one of the 14 core coding genes absent. Also, our results revealed that there is not even a single gene shared among all mitogenomes. Other unusual genes in mitogenomes were also detected in many mitogenomes, such as dpo and rpo, and displayed diverse evolutionary histories. Altogether, the results presented in this study suggest that fungal mitogenomes are diverse, contain accessory elements and are absent of a conserved gene that can be used for the taxonomic classification of the Kingdom Fungi.

SUBMITTER: Fonseca PLC

PROVIDER: S-EPMC8672057 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Monilinia fructicola and Monilinia laxa species are the most destructive and economically devastating fungal plant pathogens causing brown rot disease on stone and pome fruits worldwide. Mitochondrial genomes (mitogenomes) play critical roles influencing the mechanisms and directions of the evolution of fungal pathogens. The pan-mitogenomics approach predicts core and accessory regions of the mitochondrial genomes and explains the gain or loss of variation within and between species. The present study is a fungal pan-mitogenome of M. fructicola (N = 8) and M. laxa (N = 8) species. The completely sequenced and annotated mitogenomes showed high variability in size within and between the species. The mitogenomes of M. laxa were larger, ranging from 178,351 to 179,780bp, than the mitogenomes of M. fructicola, ranging from 158,607 to 167,838bp. However, size variation within the species showed that M. fructicola isolates were more variable in the size range than M. laxa isolates. All the mitogenomes included conserved mitochondrial genes, as well as variable regions including different mobile introns encoding homing endonucleases or maturase, non-coding introns, and repetitive elements. The linear model analysis supported the hypothesis that the mitogenome size expansion is due to presence of variable (accessory) regions. Gene synteny was mostly conserved among all samples, with the exception for order of the rps3 in the mitogenome of one isolate. The mitogenomes presented AT richness; however, A/T and G/C skew varied among the mitochondrial genes. The purifying selection was detected in almost all the protein-coding genes (PCGs) between the species. However, cytochrome b was the only gene showing a positive selection signal among the total samples. Combined datasets of amino acid sequences of 14 core mitochondrial PCGs and rps3 obtained from this study together with published mitochondrial genome sequences from some other species from Heliotales were used to infer a maximum likelihood (ML) phylogenetic tree. ML tree indicated that both Monilinia species highly diverged from each other as well as some other fungal species from the same order. Mitogenomes harbor much information about the evolution of fungal plant pathogens, which could be useful to predict pathogenic life strategies.

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Global Characterization of Fungal Mitogenomes: New Insights on Genomic Diversity and Dynamism of Coding Genes and Accessory Elements.

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