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Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species

BACKGROUND: Species in the genus Armillaria (fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despi...

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Autores principales: Kolesnikova, Anna I., Putintseva, Yuliya A., Simonov, Evgeniy P., Biriukov, Vladislav V., Oreshkova, Natalya V., Pavlov, Igor N., Sharov, Vadim V., Kuzmin, Dmitry A., Anderson, James B., Krutovsky, Konstantin V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6506933/
https://www.ncbi.nlm.nih.gov/pubmed/31068137
http://dx.doi.org/10.1186/s12864-019-5732-z
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author Kolesnikova, Anna I.
Putintseva, Yuliya A.
Simonov, Evgeniy P.
Biriukov, Vladislav V.
Oreshkova, Natalya V.
Pavlov, Igor N.
Sharov, Vadim V.
Kuzmin, Dmitry A.
Anderson, James B.
Krutovsky, Konstantin V.
author_facet Kolesnikova, Anna I.
Putintseva, Yuliya A.
Simonov, Evgeniy P.
Biriukov, Vladislav V.
Oreshkova, Natalya V.
Pavlov, Igor N.
Sharov, Vadim V.
Kuzmin, Dmitry A.
Anderson, James B.
Krutovsky, Konstantin V.
author_sort Kolesnikova, Anna I.
collection PubMed
description BACKGROUND: Species in the genus Armillaria (fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despite the importance and wide distribution of Armillaria, the complete mitogenomes have not previously been reported for this genus. Meanwhile, the well-supported phylogeny of Armillaria species provides an excellent framework in which to study variation in mitogenomes and how they have evolved over time. RESULTS: Here we completely sequenced, assembled, and annotated the circular mitogenomes of four species: A. borealis, A. gallica, A. sinapina, and A. solidipes (116,443, 98,896, 103,563, and 122,167 bp, respectively). The variation in mitogenome size can be explained by variable numbers of mobile genetic elements, introns, and plasmid-related sequences. Most Armillaria introns contained open reading frames (ORFs) that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Insertions of mobile elements were also evident as fragments of plasmid-related sequences in Armillaria mitogenomes. We also found several truncated gene duplications in all four mitogenomes. CONCLUSIONS: Our study showed that fungal mitogenomes have a high degree of variation in size, gene content, and genomic organization even among closely related species of Armillara. We suggest that mobile genetic elements invading introns and intergenic sequences in the Armillaria mitogenomes have played a significant role in shaping their genome structure. The mitogenome changes we describe here are consistent with widely accepted phylogenetic relationships among the four species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5732-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-65069332019-05-13 Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species Kolesnikova, Anna I. Putintseva, Yuliya A. Simonov, Evgeniy P. Biriukov, Vladislav V. Oreshkova, Natalya V. Pavlov, Igor N. Sharov, Vadim V. Kuzmin, Dmitry A. Anderson, James B. Krutovsky, Konstantin V. BMC Genomics Research Article BACKGROUND: Species in the genus Armillaria (fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despite the importance and wide distribution of Armillaria, the complete mitogenomes have not previously been reported for this genus. Meanwhile, the well-supported phylogeny of Armillaria species provides an excellent framework in which to study variation in mitogenomes and how they have evolved over time. RESULTS: Here we completely sequenced, assembled, and annotated the circular mitogenomes of four species: A. borealis, A. gallica, A. sinapina, and A. solidipes (116,443, 98,896, 103,563, and 122,167 bp, respectively). The variation in mitogenome size can be explained by variable numbers of mobile genetic elements, introns, and plasmid-related sequences. Most Armillaria introns contained open reading frames (ORFs) that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Insertions of mobile elements were also evident as fragments of plasmid-related sequences in Armillaria mitogenomes. We also found several truncated gene duplications in all four mitogenomes. CONCLUSIONS: Our study showed that fungal mitogenomes have a high degree of variation in size, gene content, and genomic organization even among closely related species of Armillara. We suggest that mobile genetic elements invading introns and intergenic sequences in the Armillaria mitogenomes have played a significant role in shaping their genome structure. The mitogenome changes we describe here are consistent with widely accepted phylogenetic relationships among the four species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5732-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-08 /pmc/articles/PMC6506933/ /pubmed/31068137 http://dx.doi.org/10.1186/s12864-019-5732-z Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Kolesnikova, Anna I.
Putintseva, Yuliya A.
Simonov, Evgeniy P.
Biriukov, Vladislav V.
Oreshkova, Natalya V.
Pavlov, Igor N.
Sharov, Vadim V.
Kuzmin, Dmitry A.
Anderson, James B.
Krutovsky, Konstantin V.
Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title_full Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title_fullStr Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title_full_unstemmed Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title_short Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species
title_sort mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related armillaria species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6506933/
https://www.ncbi.nlm.nih.gov/pubmed/31068137
http://dx.doi.org/10.1186/s12864-019-5732-z
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