Skip to main content
Log in

The complete mitochondrial genome of the vascular wilt fungus Verticillium dahliae: a novel gene order for Verticillium and a diagnostic tool for species identification

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

The complete sequence (27,184 bp) of the mitochondrial (mt) genome of the phytopathogenic fungus Verticillium dahliae has been determined. It contains 14 protein-coding genes related to oxidative phosphorylation, two rRNA genes and a set of 25 tRNA genes. A single intron, that harbors an intronic ORF coding for a putative ribosomal protein (rps), is located within the large rRNA gene (rnl). Gene order comparisons of V. dahliae mtDNA and complete mt genomes of Pezizomycotina revealed four units of synteny for Sordariomycetes, namely rnl-trn (11–12)-nad2-nad3, nad4L-nad5-cob-cox1, nad1-nad4-atp8-atp6 and rns-trn (1–5)-cox3-trn (1–5)-nad6-trn (2–5). These four units, in different combinations, merged to single continuous unit in the orders of Hypocreales and Sordariales. V. dahliae (Phyllachorales) and all members of the genus showed a unique feature which is the translocation of the nad1-nad4-atp8-atp6-rns-cox3-nad6 region in between genes nad3 and atp9 of the Hypocreales mtDNA gene order. Analysis of mt intergenic sequences of Verticillium species permitted the design of a species-specific primer allowing the discrimination of V. longisporum against V. dahliae and V. albo-atrum. By considering the protein-coding gene sequences as one unit, a phylogenetic comparison with representatives of Ascomycota complete mtDNA was performed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Barbara DJ, Clewes E (2003) Plant pathogenic Verticillium species: how many of them are there? Mol Plant Pathol 4:297–305

    Article  CAS  Google Scholar 

  • Berbee ML, Taylor JW (2001) Fungal molecular evolution: gene trees and geologic time. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota VII part B: systematics and evolution. Springer, Berlin Heidelberg New York, pp 229–245

    Google Scholar 

  • Berbee ML, Carmean DA, Winka K (2000) Ribosomal DNA and resolution of branching order among the Ascomycota: how many nucleotides are enough? Mol Phylogenet Evol 17:337–344

    Article  PubMed  CAS  Google Scholar 

  • Bok J-W, Griffiths AJF (1999) Transfer of Neurospora kalilo plasmids between species and strains by introgression. Curr Genet 36:275–281

    Article  PubMed  CAS  Google Scholar 

  • Bruns TD, White TJ, Taylor JW (1991) Fungal molecular systematics. Annu Rev Ecol Syst 22:525–564

    Article  Google Scholar 

  • Bullerwell CE, Burger G, Lang F (2000) A novel motif for identifying Rps3 homologs in fungal mitochondrial genomes. Trends Biochem Sci 25:363–365

    Article  PubMed  CAS  Google Scholar 

  • Bullerwell CE, Forget L, Lang BF (2003) Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences. Nucleic Acids Res 31:1614–1623

    Article  PubMed  CAS  Google Scholar 

  • Burger G, Helmer CM, Nelson MA, Werner S, Macino G (1985) RNA processing in Neurospora crassa mitochondria: transfer RNAs punctuate a large precursor transcript. EMBO J 4:197–204

    PubMed  CAS  Google Scholar 

  • Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716

    Article  PubMed  CAS  Google Scholar 

  • Christianson T, Rabinowitz M (1983) Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase. J Biol Chem 258:14025–14033

    PubMed  CAS  Google Scholar 

  • Collins A, Okoli CAN, Morton A, Parry D, Edwards SG, Barbara DJ (2003) Isolates of Verticillium dahliae pathogenic to crucifers are of at least three distinct molecular types. Phytopathology 93:364–376

    Article  Google Scholar 

  • Cummings DJ, McNally KL, Domenico JM, Matsuura ET (1990) The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr Genet 17:375–402

    Article  PubMed  CAS  Google Scholar 

  • Dobinson KF, Patterson NA, White GJ (1998) DNA fingerprinting and vegetative compatibility analysis indicate multiple origins for Verticillium dahliae race 2 tomato isolates from Ontario, Canada. Mycol Res 102:1089–1095

    Article  CAS  Google Scholar 

  • Dyson NJ, Brown TA, Ray JA, Waring RB, Scazzocchio C, Davies RW (1989) Processing of mitochondrial RNA in Aspergillus nidulans. J Mol Biol 208:587–599

    Article  PubMed  CAS  Google Scholar 

  • Fahleson J, Lagercrantz U, Hu Q, Steventon LA, Dixelius C (2003) Estimation of genetic variation among Verticillium isolates using AFLP analysis. Eur J Plant Pathol 109:361–371

    Article  CAS  Google Scholar 

  • Fahleson J, Hu Q, Dixelius C (2004) Phylogenetic analysis of Verticillium species based on nuclear and mitochondrial sequences. Arch Microbiol 181:435–442

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (2002) PHYLIP (Phylogeny Inference Package) version 3.6a3. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Forget L, Ustinova J, Wang Z, Huss AR, Lang FB (2002) Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 19:310–319

    PubMed  CAS  Google Scholar 

  • Fox TD (1987) Natural variation in the genetic code. Annu Rev Genet 21:67–91

    PubMed  CAS  Google Scholar 

  • Gams W, Zare R (2001) A revision of Verticillium sect. Prostrata. III. Generic classification. Nova Hedwigia 72:329–337

    Google Scholar 

  • Ghikas DV, Kouvelis VN, Typas MA (2006) The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes. Arch Microbiol DOI 10.1007/s00203-006-0104-x

  • Huelsenbeck JP (2000) MrBayes: Bayesian inference of phylogeny (software). University of Rochester, New York

  • Karapapa VK, Typas MA (2001) Molecular characterization of the host-adapted pathogen Verticillium longisporum on the basis of a group-I intron in the nuclear SSU-rRNA gene. Curr Microbiol 42:217–224

    PubMed  CAS  Google Scholar 

  • Karapapa VK, Bainbridge BW, Heale JB (1997) Morphological and molecular characterization of Verticillium longisporum comb. nov., pathogenic to oilseed rape. Mycol Res 101:1281–1294

    Article  Google Scholar 

  • Kennell JC, Lambowitz AM (1989) Development of an in vitro transcription system for Neurospora crassa mitochondrial DNA and identification of transcription initiation sites. Mol Cell Biol 9:3603–3613

    PubMed  CAS  Google Scholar 

  • Kleidon J, Plesofsky N, Brambl R (2003) Transcripts and transcript-binding proteins in mitochondria of Neurospora crassa. Mitochondrion 2:345–360

    Article  PubMed  CAS  Google Scholar 

  • Koll F, Boulay J, Belcour L, Dȁ9Aubenton-Carafa Y (1996) Contribution of ultra-short invasive elements to the evolution of the mitochondrial genome in the genus Podospora. Nucleic Acids Res 24:1734–1741

    Article  PubMed  CAS  Google Scholar 

  • Kouvelis VN, Ghikas DV, Typas MA (2004) The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of Sordariomycetes: phylogenetic implications. Fungal Genet Biol 41:930–940

    Article  PubMed  CAS  Google Scholar 

  • Kubelik AR, Kenell JC, Akins RA, Lambowitz AM (1990) Identification of Neurospora mitochondrial promoters and analysis of synthesis of the mitochondrial small rRNA in wild-type and the promoter mutant [poky]. J Biol Chem 265:4515–4526

    PubMed  CAS  Google Scholar 

  • Laforest M-J, Roewer I, Lang F (1997) Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG ȁ8stopȁ9 codons recognized as leucine. Nucleic Acids Res 25:626–632

    Article  PubMed  CAS  Google Scholar 

  • Lagerkvist U (1978) “Two out of three”: an alternative method for codon reading. Proc Natl Acad Sci USA 75:1759–1762

    Article  PubMed  CAS  Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221

    PubMed  CAS  Google Scholar 

  • Macey JR, Schulte JA, Larson A, Papenfuss TJ (1998) Tandem duplication via light-strand synthesis may provide a precursor for mitochondrial genomic rearrangement. Mol Biol Evol 15:71–75

    PubMed  CAS  Google Scholar 

  • Neumann MJ, Dobinson KF (2003) Sequence tag analysis of gene expression during pathogenic growth and microsclerotia development in the vascular wilt pathogen Verticillium dahliae. Fungal Genet Biol 38:54–62

    Article  PubMed  CAS  Google Scholar 

  • Pantou MP, Typas MA (2005) Electrophoretic karyotype and gene mapping of the vascular wilt fungus Verticillium dahliae. FEMS Microbiol Lett 254:213–220

    Article  Google Scholar 

  • Pantou MP, Mavridou A, Typas MA (2003) IGS sequence variation, group-I introns and the complete nuclear ribosomal DNA of the entomopathogenic fungus Metarhizium: excellent tools for isolate detection and phylogenetic analysis. Fungal Genet Biol 38:159–174

    Article  PubMed  CAS  Google Scholar 

  • Pantou MP, Strunnikova OK, Shakhnazarova VYu, Vishnevskaya NA, Papalouka VG, Typas MA (2005) Molecular and immunochemical phylogeny of Verticillium species. Mycol Res 109:889–902

    Article  PubMed  CAS  Google Scholar 

  • Paquin BP, Laforest M-J, Forget L, Roewer I, Wang Z, Longcore J, Lang BF (1997) The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 31:380–395

    Article  PubMed  CAS  Google Scholar 

  • Pegg GF (1974) Verticillium diseases. Rev Plant Pathol 53:157–182

    Google Scholar 

  • Pramateftaki PV, Antoniou PP, Typas MA (2000) The complete DNA sequence of the nuclear ribosomal RNA gene complex of Verticillium dahliae: intraspecific heterogeneity within the intergenic spacer region. Fungal Genet Biol 29:135–143

    PubMed  CAS  Google Scholar 

  • Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804

    Article  PubMed  CAS  Google Scholar 

  • Saccone S, Gissi C, Reyes A, Larizza A, Sbisa E, Pesole G (2002) Mitochondrial DNA in metazoa: degree of freedom in a frozen event. Gene 286:3–12

    Article  PubMed  CAS  Google Scholar 

  • Schäfer B (2003) Genetic conservation versus variability in mitochondria: the architecture of the mitochondrial genome in the petite-negative yeast Schizosaccharomyces pombe. Curr Genet 43:311–326

    Article  PubMed  Google Scholar 

  • Schäfer B (2005) RNA maturation in mitochondria of S. cerevisiae and S. pombe. Gene 354:80–85

    Article  PubMed  Google Scholar 

  • Sung G-H, Spatafora JW, Zare R, Hodge KT, Gams W (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72:311–328

    Google Scholar 

  • Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0b8a. Sinauer Associates, Sunderland

    Google Scholar 

  • Takano H, Abe T, Sakurai R, Moriyama Y, Miyazawa Y, Nozaki H, Kawano S, Sasaki N, Kuroiwa T (2001) The complete DNA sequence of the mitochondrial genome of Physarum polycephalum. Mol Gen Genet 264:539–545

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Typas MA, Griffen AM, Bainbridge BW, Heale JB (1992) Restriction fragment length polymorphisms in mitochondrial DNA and ribosomal RNA gene complex as an aid to the characterization of species and sub-species populations in the genus Verticillium. FEMS Microbiol Lett 95:157–162

    Article  CAS  Google Scholar 

  • Wenzlau JM, Perlman PS (1990) Mobility of two optional G1C-rich clusters of the var1 gene of yeast mitochondrial DNA. Genetics 126:53–62

    PubMed  CAS  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555–556

    CAS  Google Scholar 

  • Zare R, Gams W, Culham A (2000) A revision of Verticillium sect. Prostata I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71:465–480

    Google Scholar 

  • Zare R, Gams W, Schroers H-J (2004) The type species of Verticillium is not congeneric with the plant-pathogenic species placed in Verticillium and it is not the anamorph of ȁ8Nectriaȁ9 inventa. Mycol Res 108:576–582

    Article  PubMed  Google Scholar 

  • Zeise K, von Teidemann A (2001) Morphological and physiological differentiation among vegetative compatibility groups of Verticillium dahliae in relation to V. longisporum. J Phytopathol 149:469–475

    Article  Google Scholar 

Download references

Acknowledgements

The authors express their thanks to the Alexander S. Onassis Public Benefit Foundation for the student fellowship that M.P. Pantou received.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Milton A. Typas.

Additional information

Communicated by U. Kück

Nucleotide sequence data reported are available in the GenBank database under the accession numbers DQ351941–DQ351957.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pantou, M.P., Kouvelis, V.N. & Typas, M.A. The complete mitochondrial genome of the vascular wilt fungus Verticillium dahliae: a novel gene order for Verticillium and a diagnostic tool for species identification. Curr Genet 50, 125–136 (2006). https://doi.org/10.1007/s00294-006-0079-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-006-0079-9

Keywords

Navigation