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

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Abstract

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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Most cited references 63

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Mitochondrial evolution.

M W Gray, G. Burger, B F Lang (1999)

The serial endosymbiosis theory is a favored model for explaining the origin of mitochondria, a defining event in the evolution of eukaryotic cells. As usually described, this theory posits that mitochondria are the direct descendants of a bacterial endosymbiont that became established at an early stage in a nucleus-containing (but amitochondriate) host cell. Gene sequence data strongly support a monophyletic origin of the mitochondrion from a eubacterial ancestor shared with a subgroup of the alpha-Proteobacteria. However, recent studies of unicellular eukaryotes (protists), some of them little known, have provided insights that challenge the traditional serial endosymbiosis-based view of how the eukaryotic cell and its mitochondrion came to be. These data indicate that the mitochondrion arose in a common ancestor of all extant eukaryotes and raise the possibility that this organelle originated at essentially the same time as the nuclear component of the eukaryotic cell rather than in a separate, subsequent event.

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The genome sequence of Rickettsia prowazekii and the origin of mitochondria.

S. G. Andersson, A Zomorodipour, J O Andersson … (1998)

We describe here the complete genome sequence (1,111,523 base pairs) of the obligate intracellular parasite Rickettsia prowazekii, the causative agent of epidemic typhus. This genome contains 834 protein-coding genes. The functional profiles of these genes show similarities to those of mitochondrial genes: no genes required for anaerobic glycolysis are found in either R. prowazekii or mitochondrial genomes, but a complete set of genes encoding components of the tricarboxylic acid cycle and the respiratory-chain complex is found in R. prowazekii. In effect, ATP production in Rickettsia is the same as that in mitochondria. Many genes involved in the biosynthesis and regulation of biosynthesis of amino acids and nucleosides in free-living bacteria are absent from R. prowazekii and mitochondria. Such genes seem to have been replaced by homologues in the nuclear (host) genome. The R. prowazekii genome contains the highest proportion of non-coding DNA (24%) detected so far in a microbial genome. Such non-coding sequences may be degraded remnants of 'neutralized' genes that await elimination from the genome. Phylogenetic analyses indicate that R. prowazekii is more closely related to mitochondria than is any other microbe studied so far.

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Evolution of mitochondrial gene content: gene loss and transfer to the nucleus.

Keith L Adams, Jeffrey Palmer (2003)

Mitochondrial gene content is highly variable across extant eukaryotes. The number of mitochondrial protein genes varies from 3 to 67, while tRNA gene content varies from 0 to 27. Moreover, these numbers exclude the many diverse lineages of non-respiring eukaryotes that lack a mitochondrial genome yet still contain a mitochondrion, albeit one often highly derived in ultrastructure and metabolic function, such as the hydrogenosome. Diversity in tRNA gene content primarily reflects differential usage of imported tRNAs of nuclear origin. In the case of protein genes, most of this diversity reflects differential degrees of functional gene transfer to the nucleus, with more minor contributions resulting from gene loss from the cell as a consequence of either substitution via a functional nuclear homolog or the cell's dispensation of the function of the gene product. The tempo and pattern of mitochondrial gene loss is highly episodic, both across the broad sweep of eukaryotes and within such well-studied groups as angiosperms. All animals, some plants, and certain other groups of eukaryotes are mired in profound stases in mitochondrial gene content, whereas other lineages have experienced relatively frequent gene loss. Loss and transfer to the nucleus of ribosomal protein and succinate dehydrogenase genes has been especially frequent, sporadic, and episodic during angiosperm evolution. Potential mechanisms for activation of transferred genes have been inferred, and intermediate stages in the process have been identified by comparative studies. Several hypotheses have been proposed for why mitochondrial genes are transferred to the nucleus, why mitochondria retain genomes, and why functional gene transfer is almost exclusively unidirectional.

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Author and article information

Contributors

Anna I. Kolesnikova: annakolesnikova69@gmail.com

Yuliya A. Putintseva: yaputintseva@mail.ru

Evgeniy P. Simonov: ev.simonov@gmail.com

Vladislav V. Biriukov: vladbir2010@gmail.com

Natalya V. Oreshkova: oreshkova@ksc.krasn.ru

Igor N. Pavlov: forester24@mail.ru

Vadim V. Sharov: vsharov@sfu-kras.ru

Dmitry A. Kuzmin: dm.kuzmin@gmail.com

James B. Anderson: jb.anderson@utoronto.ca

Konstantin V. Krutovsky:

ORCID: http://orcid.org/0000-0002-8819-7084

konstantin.krutovsky@forst.uni-goettingen.de

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 8 May 2019

Publication date PMC-release: 8 May 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 351

Affiliations

[1 ]ISNI 0000 0001 0940 9855, GRID grid.412592.9, Laboratory of Forest Genomics, Genome Research and Education Center, Institute of Fundamental Biology and Biotechnology, , Siberian Federal University, ; Krasnoyarsk, 660036 Russia

[2 ]Laboratory of Genomic Research and Biotechnology, Federal Research Center “Krasnoyarsk Science Center of the Siberian Branch of the Russian Academy of Sciences”, Krasnoyarsk, 660036 Russia

[3 ]ISNI 0000 0001 2254 1834, GRID grid.415877.8, Institute of Animal Systematics and Ecology, , Siberian Branch of Russian Academy of Sciences, ; 630091 Novosibirsk, Russia

[4 ]ISNI 0000 0001 2254 1834, GRID grid.415877.8, Laboratory of Forest Genetics and Selection, V. N. Sukachev Institute of Forest, , Siberian Branch of Russian Academy of Sciences, ; Krasnoyarsk, 660036 Russia

[5 ]ISNI 0000 0001 2254 1834, GRID grid.415877.8, Laboratory of Reforestation, Mycology and Plant Pathology, V. N. Sukachev Institute of Forest, , Siberian Branch of Russian Academy of Sciences, ; Krasnoyarsk, 660036 Russia

[6 ]ISNI 0000 0001 0940 9855, GRID grid.412592.9, Department of High Performance Computing, Institute of Space and Information Technologies, , Siberian Federal University, ; Krasnoyarsk, 660074 Russia

[7 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Department of Biology, , University of Toronto, ; Mississauga, ON l5L 1C6 Canada

[8 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Department of Forest Genetics and Forest Tree Breeding, , Georg-August University of Göttingen, ; 37077 Göttingen, Germany

[9 ]ISNI 0000 0001 2192 9124, GRID grid.4886.2, Laboratory of Population Genetics, N. I. Vavilov Institute of General Genetics, , Russian Academy of Sciences, ; Moscow, 119333 Russia

[10 ]ISNI 0000 0004 4687 2082, GRID grid.264756.4, Department of Ecosystem Science and Management, , Texas A&M University, ; College Station, TX 77843-2138 USA

Author information

Konstantin V. Krutovsky http://orcid.org/0000-0002-8819-7084

Article

Publisher ID: 5732

DOI: 10.1186/s12864-019-5732-z

PMC ID: 6506933

PubMed ID: 31068137

SO-VID: 55845693-1e49-4c44-8bf4-79805ed69b8d

License:

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.

History

Date received : 6 November 2018

Date accepted : 24 April 2019

Funding

Funded by: Government of the Russian Federation

Award ID: 14.Y26.31.0004

Award Recipient : Konstantin V. Krutovsky

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: armillaria,duplications,evolution,giy-yig,homing endonucleases,introns,laglidadg,mitochondrial genome,mtdna,mobile genetic elements

Data availability:

ScienceOpen disciplines: Genetics

Keywords: armillaria, duplications, evolution, giy-yig, homing endonucleases, introns, laglidadg, mitochondrial genome, mtdna, mobile genetic elements

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

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Abstract

Background

Results

Conclusions

Electronic supplementary material

Related collections

Genomic Prediction

Most cited references 63

Mitochondrial evolution.

The genome sequence of Rickettsia prowazekii and the origin of mitochondria.

Evolution of mitochondrial gene content: gene loss and transfer to the nucleus.

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