Mobile elements and mitochondrial genome expansion in the soil fungus and potato pathogen<i>Rhizoctonia solani</i>AG-3

Losada, Liliana; Pakala, Suman B.; Fedorova, Natalie D.; Joardar, Vinita; Shabalina, Svetlana A.; Hostetler, Jessica B.; Pakala, Suchitra; Zafar, Nikhat; Thomas, Elizabeth; Rodriguez-Carres, Marianela; Dean, Ralph A.; Vilgalys, Rytas; Nierman, William C.; Cubeta, Marc A.

doi:10.1111/1574-6968.12387

Cited by 88 publications

(93 citation statements)

References 56 publications

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“…Some fungal mitochondrial genomes contain a high fraction of repeat sequences which could account for an increase in the genome size, as observed for the mt genomes of Agaricus bisporus [35] and R. solani [7]. Dot plot analysis shows the lack of long duplicated regions in the S. borealis mt genome (Figure S1), and a BLASTN similarity search reveals that repeated sequences account for only about 6.6% of S. borealis mtDNA.…”

Section: Resultsmentioning

confidence: 78%

“…Our comparative analysis indicates that the 203,051 bp long S. borealis mt genome is the second largest fungal mt genome sequenced to date, after the 235,849 bp long mtDNA of the basidiomycete R. solani Rhs1AP [7]. The next largest mitochondrial genomes are the R. solani AG1-IB (162,751 bp) [50] and A. bisporus (135,005 bp) [35].…”

Section: Resultsmentioning

confidence: 87%

“…The next largest mitochondrial genomes are the R. solani AG1-IB (162,751 bp) [50] and A. bisporus (135,005 bp) [35]. Expansion of the mitochondrial genome size in R. solani Rhs1AP was driven by accumulation of introns, HEG-like genes and hypothetical genes, but the most peculiar feature was the presence of various interspersed repeats, which occupy about one third of the genome [7].…”

Section: Resultsmentioning

confidence: 99%

“…Fungal mt genomes range in size from about 19 kbp ( Hanseniaspora uvarum ) to 235,849 bp for Rhizoctonia solani AG-3 strain Rhs1AP [7], and usually contain 14 genes that encode oxidative phosphorylation system proteins, the large ( rnl ) and small ( rns ) ribosomal RNA subunits, and a fairly constant set of tRNAs genes [8], [9]. Besides this core set of genes, a varying number of introns, often including GIY-YIG or LAGLIDADG endonuclease genes, have been reported [10], [11], [12], [13].…”

Section: Introductionmentioning

confidence: 99%

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The 203 kbp Mitochondrial Genome of the Phytopathogenic Fungus Sclerotinia borealis Reveals Multiple Invasions of Introns and Genomic Duplications

et al. 2014

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Here we report the complete sequence of the mitochondrial (mt) genome of the necrotrophic phytopathogenic fungus Sclerotinia borealis, a member of the order Helotiales of Ascomycetes. The 203,051 bp long mtDNA of S. borealis represents one of the largest sequenced fungal mt genomes. The large size is mostly determined by the presence of mobile genetic elements, which include 61 introns. Introns contain a total of 125,394 bp, are scattered throughout the genome, and are found in 12 protein-coding genes and in the ribosomal RNA genes. Most introns contain complete or truncated ORFs that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Integrations of mobile elements are also evidenced by the presence of two regions similar to fragments of inverton-like plasmids. Although duplications of some short genome regions, resulting in the appearance of truncated extra copies of genes, did occur, we found no evidences of extensive accumulation of repeat sequences accounting for mitochondrial genome size expansion in some other fungi. Comparisons of mtDNA of S. borealis with other members of the order Helotiales reveal considerable gene order conservation and a dynamic pattern of intron acquisition and loss during evolution. Our data are consistent with the hypothesis that horizontal DNA transfer has played a significant role in the evolution and size expansion of the S. borealis mt genome.

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Section: Resultsmentioning

confidence: 78%

Section: Resultsmentioning

confidence: 87%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The 203 kbp Mitochondrial Genome of the Phytopathogenic Fungus Sclerotinia borealis Reveals Multiple Invasions of Introns and Genomic Duplications

et al. 2014

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“…Very few mitochondrial genomes are available for members of the Ustiloginales ( U. maydis , DQ157700.1; Melanopsichium pennsylvanicum , HG529787; and S. reilianum ) and sizes range from 5,814 bp to 90,496 bp. Despite the size variation, the gene content among these genomes are very similar and size variability is mostly due to spacers and the presence or absence of introns and intron encoded ORFs [57–59]. …”

Section: Discussionmentioning

confidence: 99%

Complete Genome Sequence of Sporisorium scitamineum and Biotrophic Interaction Transcriptome with Sugarcane

et al. 2015

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Sporisorium scitamineum is a biotrophic fungus responsible for the sugarcane smut, a worldwide spread disease. This study provides the complete sequence of individual chromosomes of S. scitamineum from telomere to telomere achieved by a combination of PacBio long reads and Illumina short reads sequence data, as well as a draft sequence of a second fungal strain. Comparative analysis to previous available sequences of another strain detected few polymorphisms among the three genomes. The novel complete sequence described herein allowed us to identify and annotate extended subtelomeric regions, repetitive elements and the mitochondrial DNA sequence. The genome comprises 19,979,571 bases, 6,677 genes encoding proteins, 111 tRNAs and 3 assembled copies of rDNA, out of our estimated number of copies as 130. Chromosomal reorganizations were detected when comparing to sequences of S. reilianum, the closest smut relative, potentially influenced by repeats of transposable elements. Repetitive elements may have also directed the linkage of the two mating-type loci. The fungal transcriptome profiling from in vitro and from interaction with sugarcane at two time points (early infection and whip emergence) revealed that 13.5% of the genes were differentially expressed in planta and particular to each developmental stage. Among them are plant cell wall degrading enzymes, proteases, lipases, chitin modification and lignin degradation enzymes, sugar transporters and transcriptional factors. The fungus also modulates transcription of genes related to surviving against reactive oxygen species and other toxic metabolites produced by the plant. Previously described effectors in smut/plant interactions were detected but some new candidates are proposed. Ten genomic islands harboring some of the candidate genes unique to S. scitamineum were expressed only in planta. RNAseq data was also used to reassure gene predictions.

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Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Pogoda

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Nadiadi

et al. 2019

Ecology and Evolution

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Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial genomes. Here, we examine patterns of mitochondrial evolution specifically looking at intron size, number, and position across 58 species from 21 genera of lichenized Ascomycete fungi, representing a broad range of fungal diversity and niches. Our results show that the cox1 gene always contained the highest number of introns out of all the mitochondrial protein‐coding genes, that high intron sequence similarity (>90%) can be maintained between different genera, and that lichens have undergone at least two instances of complete, genome‐wide intron loss consistent with evidence for genome streamlining via loss of parasitic, noncoding DNA, in Phlyctis boliviensis and Graphis lineola . Notably, however, lichenized fungi have not only undergone intron loss but in some instances have expanded considerably in size due to intron proliferation (e.g., Alectoria fallacina and Parmotrema neotropicum ), even between closely related sister species (e.g., Cladonia ). These results shed light on the highly dynamic mitochondrial evolution that is occurring in lichens and suggest that these obligate symbiotic organisms are in some cases undergoing recent, broad‐scale genome streamlining via loss of protein‐coding genes as well as noncoding, parasitic DNA elements.

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Mobile elements and mitochondrial genome expansion in the soil fungus and potato pathogenRhizoctonia solaniAG-3

Cited by 88 publications

References 56 publications

The 203 kbp Mitochondrial Genome of the Phytopathogenic Fungus Sclerotinia borealis Reveals Multiple Invasions of Introns and Genomic Duplications

The 203 kbp Mitochondrial Genome of the Phytopathogenic Fungus Sclerotinia borealis Reveals Multiple Invasions of Introns and Genomic Duplications

Complete Genome Sequence of Sporisorium scitamineum and Biotrophic Interaction Transcriptome with Sugarcane

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

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