Elsevier

Biochimie

Volume 78, Issue 6, 1996, Pages 518-529
Biochimie

Editing and import: Strategies for providing plant mitochondria with a complete set of functional transfer RNAs

https://doi.org/10.1016/0300-9084(96)84758-4Get rights and content

Abstract

The recombinations and mutations that plant mitochondrial DNA has undergone during evolution have led to the inactivation or complete loss of a number of the ‘native’ transfer RNA genes deriving from the genome of the ancestral endosymbiont. Following sequence divergence in their genes, some native mitochondrial tRNAs are ‘rescued’ by editing, a post-transcriptional process which changes the RNA primary sequence. According to in vitro studies with the native mitochondrial tRNAPhe from potato and tRNAHis from larch, editing is required for efficient processing. Some of the native tRNA genes which have been inactivated or lost have been replaced by tRNA genes present in plastid DNA sequences acquired by the mitochondrial genome during evolution, which raises the problem of the transcriptional regulation of tRNA genes in plant mitochondria. Finally, tRNAs for which no gene is present in the mitochondrial genome are imported from the cytosol. This process is highly specific for certain tRNAs, and it has been suggested that the cognate aminoacyl-tRNA synthetases may be responsible for this specificity. Indeed, a mutation which blocks recognition of the cytosolic Arabidopsis thaliana tRNAAla by the corresponding alanyl-tRNA synthetase also prevents mitochondrial import of this tRNA in transgenic plants. Conversely, no significant mitochondrial co-import of the normally cytosol-specific tRNAAsp was detected in transgenic plants expressing the yeast cytosolic aspartyl-tRNA synthetase fused to a mitochondrial targeting sequence, suggesting that, although necessary, recognition by a cognate aminoacyl-tRNA synthetase might not be sufficient to allow tRNA import into plant mitochondria.

References (92)

  • L.R. Ceci et al.

    Location of a single tRNA-His gene on the master chromosome of sunflower mitochondrial DNA

    Plant Sci

    (1989)
  • S. Binder et al.

    Transcription initiation sites in mitochondria of Oenothera berteriana

    J Biol Chem

    (1993)
  • S. Binder et al.

    A novel pea mitochondrial in vitro transcription system recognizes homologous and heterologous mRNA and tRNA promoters

    J Biol Chem

    (1995)
  • L. Maréchal-Drouard et al.

    A nuclear-encoded potato (Solanum tuberosum) mitochondrial tRNALeu and its cytosolic counterpart have identical nucleotide sequences

    FEBS Lett

    (1990)
  • I. Tarassov et al.

    An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA

    J Mol Biol

    (1995)
  • D.T. Chen et al.

    In vivo expression and mitochondrial import of normal and mutated tRNAThr in Leishmania

    Mol Biochem Parasitol

    (1994)
  • A. Brennicke et al.

    The mitochondrial genome on its way to the nucleus: Different stages of gene transfer in higher plants

    FEBS Lett

    (1993)
  • M.M. Bradford

    A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding

    Anal Biochem

    (1976)
  • G. Burger et al.

    Genes encoding the same three subunits of respiratory complex II are present in the mitochondrial DNA of two phylogenetically distant eukaryotes

  • L. Bonen et al.

    Genetic plasticity and its consequences: perspectives on gene organization and expression in plant mitochondria

    Can J Bot

    (1993)
  • W. Schuster et al.

    Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenotheta: is genetic information transferred between organelles via RNA?

    EMBO J

    (1987)
  • V. Knoop et al.

    Copia-, gypsy- and LINE-like retrotransposon fragments in the mitochondrial genome of Arabidopsis thaliana

    Genetics

    (1996)
  • S. Anderson et al.

    Sequence and organization of the human mitochondrial genome

    Nature

    (1981)
  • K. Oda et al.

    Transfer RNA genes in the mitochondrial genome from a liverworm, Manchantia polymorphic: The absence of chloroplast-like transfer RNAs

    Nucleic Acid Res

    (1992)
  • A. Tzagaloff et al.

    Genetics of mitochondrial biogenesis

    Annu Rev Biochem

    (1986)
  • F. Weber-Lotfi et al.

    Localization of tRNA genes on the Petunia hybrida 3704 mitochondrial genome

    Plant Mol Biol

    (1993)
  • L. Ceci et al.

    Identification and mapping of tRNA genes on the Helianthus annuus mitochondrial genome

    DNA Sequence

    (1996)
  • A. Sangaré et al.

    Localization and organization of tRNA genes on the mitochondrial genomes of fertile and male-sterile lines of maize

    Mol Gen Genet

    (1990)
  • L. Maréchal et al.

    Sequence and codon recognition of bean mitochondria and chloroplast tRNAsTrp: evidence for a high degree of homology

    Nucleic Acids Res

    (1985)
  • P.B.M. Joyce et al.

    Chloroplast-like transfer RNA genes expressed in wheat mitochondria

    Nucleic Acids Res

    (1989)
  • H. Wintz et al.

    Location and nucleotide sequence of two tRNA genes and a tRNA pseudo-gene in the maize mitochondrial genome: evidence for the transcription of a chloroplast gene in mitochondria

    Curr Genet

    (1988)
  • L. Maréchal-Drouard et al.

    Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris

    Nucleic Acids Res

    (1988)
  • L. Maréchal-Drouard et al.

    Transfer RNAs of potato (Solamum tuberosum) mitochondria have different genetic origins

    Nucleic Acids Res

    (1990)
  • L. Maréchal-Drouard et al.

    A single editing event is a prerequisite for efficient processing of potato mitochondrial phenylalanine tRNA

    Mol Cell Biol

    (1996)
  • P. Guillemaut et al.

    Purification and identification of higher plant organellar transfer RNAs

  • G. Eriani et al.

    Cytoplasmic aspartyl-tRNA synthetase from Saccharomyces cerevisiae: Study of its functional organisation by deletion amalysis

    Eur J Biochem

    (1991)
  • M. Sellami et al.

    Nucleotide sequence of the gene coding for yeast cytoplasmic aspartyl-tRNA synthetase (APS): mapping of the 5′ and 3′ termini of AspRS mRNA

    Nucleic Acids Res

    (1986)
  • M. Boutry et al.

    Targeting of bacterial chloramphenicol acetyltransferase to mitochondria in transgenic plants

    Nature

    (1987)
  • M. Rocha-Sosa et al.

    Both developmental and metabolic signals activate the promoter of a class I patatin gene

    EMBO J

    (1989)
  • J. Paszkowski et al.

    Direct gene transfer to plants

    EMBO J

    (1984)
  • J. Masson et al.

    Selection of somatic hybrids between diploid clones of potato (Solanum tuberosum L) transformed by direct gene transfer

    Theor Appl Genet

    (1989)
  • U.K. Laemmli

    Cleavage of structural proteins during the assembly of the head of bacteriophage T4

    Nature

    (1970)
  • G. Prévost et al.

    Study of the arrangement of the functional domains along the yeast cytoplasmic aspartyl-tRNA synthetase

    Eur J Biochem

    (1989)
  • G. Green et al.

    A Phaseolus vulgaris mitochondrial tRNALeu is identical to its cytoplasmic counterpart: sequencing and in vivo transcription of the gene corresponding to the cytoplasmic tRNALeu

    Plant Mol Biol

    (1987)
  • I. Small et al.

    In vivo import of a normal or mutagenized heterologous transfer RNA into the mitochondria of transgenic plants: Towards novel ways of influencing mitochondrial gene expression?

    EMBO J

    (1992)
  • R. Kumar et al.

    Striking differences in mitochondrial tRNA import among different plant species

    Mol Gen Genet

    (1996)
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