Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex

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Abstract

Background

The Fusarium oxysporum species complex (FOSC) contains several phylogenetic lineages. Phylogenetic studies identified two to three major clades within the FOSC. The mitochondrial sequences are highly informative phylogenetic markers, but have been mostly neglected due to technical difficulties.

Results

A total of 61 complete mitogenomes of FOSC strains were de novo assembled and annotated. Length variations and intron patterns support the separation of three phylogenetic species. The variable region of the mitogenome that is typical for the genus Fusarium shows two new variants in the FOSC. The variant typical for Fusarium is found in members of all three clades, while variant 2 is found in clades 2 and 3 and variant 3 only in clade 2. The extended set of loci analyzed using a new implementation of the genealogical concordance species recognition method support the identification of three phylogenetic species within the FOSC. Comparative analysis of the mitogenomes in the FOSC revealed ongoing mitochondrial recombination within, but not between phylogenetic species.

Conclusions

The recombination indicates the presence of a parasexual cycle in F. oxysporum. The obstacles hindering the usage of the mitogenomes are resolved by using next generation sequencing and selective genome assemblers, such as GRAbB. Complete mitogenome sequences offer a stable basis and reference point for phylogenetic and population genetic studies.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-017-4116-5) contains supplementary material, which is available to authorized users.

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Most cited references 27

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Phylogenetic species recognition and species concepts in fungi.

John Taylor, David J Jacobson, Scott Kroken … (2000)

The operational species concept, i.e., the one used to recognize species, is contrasted to the theoretical species concept. A phylogenetic approach to recognize fungal species based on concordance of multiple gene genealogies is compared to those based on morphology and reproductive behavior. Examples where Phylogenetic Species Recognition has been applied to fungi are reviewed and concerns regarding Phylogenetic Species Recognition are discussed.

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Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies.

K. O'Donnell, H C Kistler, E Cigelnik … (1998)

Panama disease of banana, caused by the fungus Fusarium oxysporum f. sp. cubense, is a serious constraint both to the commercial production of banana and cultivation for subsistence agriculture. Previous work has indicated that F. oxysporum f. sp. cubense consists of several clonal lineages that may be genetically distant. In this study we tested whether lineages of the Panama disease pathogen have a monophyletic origin by comparing DNA sequences of nuclear and mitochondrial genes. DNA sequences were obtained for translation elongation factor 1alpha and the mitochondrial small subunit ribosomal RNA genes for F. oxysporum strains from banana, pathogenic strains from other hosts and putatively nonpathogenic isolates of F. oxysporum. Cladograms for the two genes were highly concordant and a partition-homogeneity test indicated the two datasets could be combined. The tree inferred from the combined dataset resolved five lineages corresponding to "F. oxysporum f. sp. cubense" with a large dichotomy between two taxa represented by strains most commonly isolated from bananas with Panama disease. The results also demonstrate that the latter two taxa have significantly different chromosome numbers. F. oxysporum isolates collected as nonpathogenic or pathogenic to other hosts that have very similar or identical elongation factor 1alpha and mitochondrial small subunit genotypes as banana pathogens were shown to cause little or no disease on banana. Taken together, these results indicate Panama disease of banana is caused by fungi with independent evolutionary origins.

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Is Open Access

One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes

J.B. Stielow, C.A. Lévesque, K.A. Seifert … (2015)

The aim of this study was to assess potential candidate gene regions and corresponding universal primer pairs as secondary DNA barcodes for the fungal kingdom, additional to ITS rDNA as primary barcode. Amplification efficiencies of 14 (partially) universal primer pairs targeting eight genetic markers were tested across > 1 500 species (1 931 strains or specimens) and the outcomes of almost twenty thousand (19 577) polymerase chain reactions were evaluated. We tested several well-known primer pairs that amplify: i) sections of the nuclear ribosomal RNA gene large subunit (D1–D2 domains of 26/28S); ii) the complete internal transcribed spacer region (ITS1/2); iii) partial β -tubulin II (TUB2); iv) γ-actin (ACT); v) translation elongation factor 1-α (TEF1α); and vi) the second largest subunit of RNA-polymerase II (partial RPB2, section 5–6). Their PCR efficiencies were compared with novel candidate primers corresponding to: i) the fungal-specific translation elongation factor 3 (TEF3); ii) a small ribosomal protein necessary for t-RNA docking; iii) the 60S L10 (L1) RP; iv) DNA topoisomerase I (TOPI); v) phosphoglycerate kinase (PGK); vi) hypothetical protein LNS2; and vii) alternative sections of TEF1α. Results showed that several gene sections are accessible to universal primers (or primers universal for phyla) yielding a single PCR-product. Barcode gap and multi-dimensional scaling analyses revealed that some of the tested candidate markers have universal properties providing adequate infra- and inter-specific variation that make them attractive barcodes for species identification. Among these gene sections, a novel high fidelity primer pair for TEF1α, already widely used as a phylogenetic marker in mycology, has potential as a supplementary DNA barcode with superior resolution to ITS. Both TOPI and PGK show promise for the Ascomycota, while TOPI and LNS2 are attractive for the Pucciniomycotina, for which universal primers for ribosomal subunits often fail.

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Author and article information

Contributors

Balázs Brankovics:

ORCID: http://orcid.org/0000-0003-0536-7787

b.brankovics@westerdijkinstitute.nl

Peter van Dam: p.vandam@uva.nl

Martijn Rep: m.rep@uva.nl

G. Sybren de Hoog: s.hoog@westerdijkinstitute.nl

Theo A. J. van der Lee: theo.vanderlee@wur.nl

Cees Waalwijk: cees.waalwijk@wur.nl

Anne D. van Diepeningen: anne.vandiepeningen@wur.nl

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): 18 September 2017

Publication date PMC-release: 18 September 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 735

Affiliations

[1 ]Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, Utrecht, 3584CT The Netherlands

[2 ]ISNI 0000000084992262, GRID grid.7177.6, Institute of Biodiversity and Ecosystem Dynamics, , University of Amsterdam, ; Science Park 904, Amsterdam, 1098 XH The Netherlands

[3 ]ISNI 0000000084992262, GRID grid.7177.6, Swammerdam Institute for Life Sciences, , University of Amsterdam, ; Science Park 904, Amsterdam, 1098 XH The Netherlands

[4 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Wageningen University and Research Centre, ; Droevendaalsesteeg 4, Wageningen, 6708 PB The Netherlands

Author information

Balázs Brankovics http://orcid.org/0000-0003-0536-7787

Article

Publisher ID: 4116

DOI: 10.1186/s12864-017-4116-5

PMC ID: 5604515

PubMed ID: 28923029

SO-VID: 19658555-14a2-4c77-a7c1-02f7c55d1463

License:

Open Access This 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 : 22 December 2016

Date accepted : 5 September 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek;

Award ID: 833.13.006.

Award Recipient : Anne D. van Diepeningen

Funded by: Netherlands Genomics Initiative

Award ID: 93512007

Award Recipient : Martijn Rep

Funded by: FundRef http://dx.doi.org/10.13039/501100007601, Horizon 2020;

Award ID: 678781

Award Recipient : Cees Waalwijk

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ScienceOpen disciplines: Genetics

Keywords: comparative genomics,mitochondrial genome,mitochondrial recombination,phylogenomics

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ScienceOpen disciplines: Genetics

Keywords: comparative genomics, mitochondrial genome, mitochondrial recombination, phylogenomics

Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex

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Arabidopsis genomics

Most cited references 27

Phylogenetic species recognition and species concepts in fungi.

Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies.

One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes

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