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A fragment of chloroplast DNA was transferred horizontally, probably from non-eudicots, to mitochondrial genome of Phaseolus

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Abstract

The mitochondrial genomes of some Phaseolus species contain a fragment of chloroplast trnA gene intron, named pvs-trnA for its location within the Phaseolus vulgaris sterility sequence (pvs). The purpose of this study was to determine the type of transfer (intracellular or horizontal) that gave rise to pvs-trnA. Using a PCR approach we could not find the respective portion of the trnA gene as a part of pvs outside the Phaseolus genus. However, a BLAST search revealed longer fragments of trnA present in the mitochondrial genomes of some Citrus species, Helianthus annuus and Zea mays. Basing on the identity or near-identity between these mitochondrial sequences and their chloroplast counterparts we concluded that they had relocated from chloroplasts to mitochondria via recent, independent, intracellular DNA transfers. In contrast, pvs-trnA displayed a relatively higher sequence divergence when compared with its chloroplast counterpart from Phaseolus vulgaris. Alignment of pvs-trnA with corresponding trnAfragments from 35 plant species as well as phylogenetic analysis revealed that pvs-trnA grouped with non-eudicot sequences and was well separated from all Fabalessequences. In conclusion, we propose that pvs-trnA arose via horizontal transfer of a trnA intron fragment from chloroplast of a non-eudicot plant to Phaseolus mitochondria. This is the first example of horizontal transfer of a chloroplast sequence to the mitochondrial genome in higher plants.

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Abbreviations

bp:

base pair

cox1 :

gene encoding subunit 1 of cytochrome oxidase

HGT:

horizontal gene transfer

kb:

kilo base

LRT:

likelihood ratio test

ML:

maximum-likelihood

nad1 :

gene encoding subunit 1 of respiratory chain NADH dehydrogenase

pvs :

Phaseolus vulgaris sterility sequence

trnA :

gene encoding alanine tRNA

trnI :

gene encoding isoleucine tRNA

WNJ:

weighted neighbour-joining

References

  • K.L. Adams Y.L. Qiu M. Stoutemyer J.D. Palmer (2002) ArticleTitlePunctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer during angiosperm evolution Proc. Natl. Acad. Sci. USA 99 9905–9912

    Google Scholar 

  • H. Akaike (1974) ArticleTitleA new look at the statistical model identification IEEE Transactions on Automatic Control 19 716–723 Occurrence Handle10.1109/TAC.1974.1100705

    Article  Google Scholar 

  • J.M. Archibald M.B. Rogers M. Toop K.I. Ishida P.J. Keeling (2003) ArticleTitleLateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga, Bigelowiella natans Proc. Natl. Acad. Sci. USA 100 7678–7683

    Google Scholar 

  • M. Arrieta-Montiel A. Lyznik M. Woloszynska H. Janska J. Tohme S. Mackenzie (2001) ArticleTitleTracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean Genetics 158 851–864

    Google Scholar 

  • U. Bergthorsson K.L. Adams B. Thomason J.D. Palmer (2003) ArticleTitleWidespread horizontal transfer of mitochondrial genes in flowering plants Nature 424 197–201 Occurrence Handle10.1038/nature01743 Occurrence Handle1:CAS:528:DC%2BD3sXlt1Ckt7g%3D Occurrence Handle12853958

    Article  CAS  PubMed  Google Scholar 

  • W.J. Bruno N.D. Socci A.L. Halpern (2000) ArticleTitleWeighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction Mol. Biol. Evol. 17 189–197

    Google Scholar 

  • C.D. Chase V.M. Ortega (1992) ArticleTitleOrganization of ATPA coding and 3′ flanking sequences associated with cytoplasmic male sterility in Phaseolus vulgaris L Curr. Genet. 22 147–153

    Google Scholar 

  • Y. Cho Y.L. Qiu P. Kuhlman J.D. Palmer (1998) ArticleTitleExplosive invasion of plant mitochondria by a group I intron Proc. Natl. Acad. Sci. USA 95 14244–14249

    Google Scholar 

  • M.P. Cummings J.M. Nugent R.G. Olmstead J.D. Palmer (2003) ArticleTitlePhylogenetic analysis reveals five independent transfers of the chloroplast gene rbcL to the mitochondrial genome in angiosperms Curr Genet 43 131–138 Occurrence Handle1:CAS:528:DC%2BD3sXivVynur4%3D Occurrence Handle12695853

    CAS  PubMed  Google Scholar 

  • C.C. Davis K.J. Wurdack (2004) ArticleTitleHost-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales Science 305 676–678

    Google Scholar 

  • F. Cruz Particlede la J. Davies (2000) ArticleTitleHorizontal gene transfer and the origin of species: lessons from bacteria Trends Microbiol. 8 128–133

    Google Scholar 

  • W.F. Doolittle (1999) ArticleTitlePhylogenetic classification and the universal tree Science 284 2124–2128 Occurrence Handle10.1126/science.284.5423.2124

    Article  Google Scholar 

  • J. Felsenstein (2004) PHYLIP (Phylogeny Inference Package) version 3.6 b Distributed by the author. Department of Genome Sciences University of Washington, Seattle

    Google Scholar 

  • M.W. Gray (1992) ArticleTitleThe endosymbiont hypothesis revisited Int. Rev. Cytol. 141 233–357

    Google Scholar 

  • N Goldman JP Anderson AG Rodrigo (2000) ArticleTitleLikelihood-based tests of topologies in phylogenetics Syst. Biol. 49 652–670

    Google Scholar 

  • S. Guindon O. Gascuel (2003) ArticleTitleA simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst. Biol. 52 696–704

    Google Scholar 

  • F. Hervieu L. Charbonnier H. Bannerot G. Pelletier (1993) ArticleTitleThe cytoplasmic male sterility (CMS) determinant of common bean is widespread in Phaseolus vulgaris L and Phaseolus coccineus L. Curr. Genet. 24 149–155

    Google Scholar 

  • H. Janska R. Sarria M. Woloszynska M. Arrieta-Montiel S. Mackenzie (1998) ArticleTitleStoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility Plant Cell 10 1163–1180 Occurrence Handle10.1105/tpc.10.7.1163 Occurrence Handle1:CAS:528:DyaK1cXkvFejt7s%3D Occurrence Handle9668135

    Article  CAS  PubMed  Google Scholar 

  • H. Janska M. Woloszynska (1997) ArticleTitleThe dynamic nature of plant mitochondrial genome organization Acta Biochim. Polon. 44 239–250

    Google Scholar 

  • C. Johns M. Lu A. Lyznik S. Mackenzie (1992) ArticleTitleA mitochondrial DNA sequence is associated with abnormal pollen development in cytoplasmic male sterile bean plants Plant Cell 4 435–449

    Google Scholar 

  • A. Kanno M. Nakazono A. Hirai T. Kameya (1997) ArticleTitleMaintenance of chloroplast-derived sequences in the mitochondrial DNA of Gramineae Curr. Genet. 32 413–419

    Google Scholar 

  • H Kishino M Hasegawa (1989) ArticleTitleEvaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea J. Mol. Evol. 29 170–179

    Google Scholar 

  • CG Kurland B Canback OG Berg (2003) ArticleTitle Horizontal gene transfer: A critical view Proc. Natl. Acad. Sci. U. S. A. 100 9658–9662

    Google Scholar 

  • J.G. Lawrence H. Hendrickson (2003) ArticleTitleLateral gene transfer: when will adoloscence end Mol. Microbiol. 50 739–749

    Google Scholar 

  • S.A. Mackenzie (1991) ArticleTitleIdentification of a sterility-inducing cytoplasm in a fertile accession line of Phaseolus vulgaris L Genetics 127 411–416

    Google Scholar 

  • W. Martin (2003) ArticleTitleGene transfer from organelles to the nucleus: Frequent and in big chunks Proc. Natl. Acad. Sci. USA 100 8612–8614

    Google Scholar 

  • Y. Notsu S. Masood T. Nishikawa N. Kubo G. Akiduki M. Nakazono A. Hirai K. Kadowaki (2002) ArticleTitleThe complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants Mol. Genet. Genomics 268 434–445

    Google Scholar 

  • H.A. Schmidt K. Strimmer M. Vingron A. Haeseler Particlevon (2002) ArticleTitleTREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing Bioinformatics 18 502–504 Occurrence Handle10.1093/bioinformatics/18.3.502 Occurrence Handle1:CAS:528:DC%2BD38XivFKrsL0%3D Occurrence Handle11934758

    Article  CAS  PubMed  Google Scholar 

  • V. Schmit P. Jardin Particledu J.P. Baudoin D.G. Debouck (1993) ArticleTitleUse of chloroplast DNA polymorphisms for the phylogenetic study of seven Phaseolus taxa including P vulgaris and P. coccineus Theor. Appl. Genet. 87 506–516

    Google Scholar 

  • H Shimodaira M Hasegawa (1999) ArticleTitleMultiple comparisons of log-likelihoods with applications to phylogenetic inference Mol. Biol. Evol. 16 1114–1116

    Google Scholar 

  • I.D. Small R. Suffolk C.J. Leaver (1989) ArticleTitleEvolution of plant mitochondrial genomes via substoichiometric intermediates Cell 58 69–76 Occurrence Handle10.1016/0092-8674(89)90403-0 Occurrence Handle1:CAS:528:DyaL1MXltFSisbo%3D Occurrence Handle2752423

    Article  CAS  PubMed  Google Scholar 

  • P.S. Soltis D.E. Soltis M.W. Chase (1999) ArticleTitleAngiosperm phylogeny inferred from multiple genes as a tool for comparative biology Nature 402 402–404 Occurrence Handle10.1038/46528 Occurrence Handle1:CAS:528:DyaK1MXnvVykurg%3D Occurrence Handle10586878

    Article  CAS  PubMed  Google Scholar 

  • S. Stegemann S. Hartmann S. Ruf R. Bock (2003) ArticleTitleHigh-frequency gene transfer from the chloroplast genome to the nucleus Proc. Natl. Acad. Sci. USA 100 8828–8833

    Google Scholar 

  • K. Strimmer A. Rambaut (2002) ArticleTitleInferring confidence sets of possibly misspecified gene trees Proc. R. Soc. Lond. B 269 137–142

    Google Scholar 

  • J.D. Thompson D.G. Higgins T.J. Gibson (1994) ArticleTitleCLUSTAL 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 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • M. Unseld J.R. Marienfeld P. Brandt A. Brennicke (1997) ArticleTitleThe mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides Nat Genet. 15 57–61

    Google Scholar 

  • N. Watanabe M. Nakazono A. Kanno N. Tsutsumi A. Hirai (1994) ArticleTitleEvolutionary variations in DNA sequences transferred from chloroplast genomes to mitochondrial genomes in the Gramineae Curr. Genet. 26 512–518

    Google Scholar 

  • N. Wikström V. Savolainen M.W. Chase (2001) ArticleTitleEvolution of the angiosperms: calibrating the family tree Proc R Soc Lond B Biol Sci. 268 2211–2220

    Google Scholar 

  • M. Woloszynska J. Kieleczawa M. Ornatowska M. Wozniak H. Janska (2001) ArticleTitleThe origin and maintenance of the small repeat in the bean mitochondrial genome Mol. Genet. Genomics 265 865–872

    Google Scholar 

  • H. Won S.S. Renner (2003) ArticleTitleHorizontal gene transfer from flowering plants to Gnetum Proc. Natl. Acad. Sci. USA 100 10824–10829

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biochemistry and Molecular Biology, Department of Cell Molecular Biology, University of Wroclaw, Wroclaw, Poland

    Magdalena Woloszynska, Tomasz Bocer & Hanna Janska

  2. Institute of Genetics and Microbiology, Department of Genomics, University of Wroclaw, Wroclaw, Poland

    Pawel Mackiewicz

Authors
  1. Magdalena Woloszynska
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  2. Tomasz Bocer
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  3. Pawel Mackiewicz
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  4. Hanna Janska
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Correspondence to Magdalena Woloszynska.

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Woloszynska, M., Bocer, T., Mackiewicz, P. et al. A fragment of chloroplast DNA was transferred horizontally, probably from non-eudicots, to mitochondrial genome of Phaseolus. Plant Mol Biol 56, 811–820 (2004). https://doi.org/10.1007/s11103-004-5183-y

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