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Plant Physiol. 2016 Dec;172(4):2471-2490. Epub 2016 Oct 27.

Plant-Specific Preprotein and Amino Acid Transporter Proteins Are Required for tRNA Import into Mitochondria.

Murcha MW1,2,3,4,5,6,7, Kubiszewski-Jakubiak S8,9,10,11,12,13,14, Teixeira PF8,9,10,11,12,13,14, Gügel IL8,9,10,11,12,13,14, Kmiec B8,9,10,11,12,13,14, Narsai R8,9,10,11,12,13,14, Ivanova A8,9,10,11,12,13,14, Megel C8,9,10,11,12,13,14, Schock A8,9,10,11,12,13,14, Kraus S8,9,10,11,12,13,14, Berkowitz O8,9,10,11,12,13,14, Glaser E8,9,10,11,12,13,14, Philippar K8,9,10,11,12,13,14, Maréchal-Drouard L8,9,10,11,12,13,14, Soll J8,9,10,11,12,13,14, Whelan J1,2,3,4,5,6,7.

Author information

1
Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia (M.W.M., S.K.-J., A.I.); monika.murcha@uwa.edu.au.
2
Department of Biochemistry and Biophysics, Stockholm University, Arrhenius Laboratories for Natural Sciences, SE-10691 Stockholm, Sweden (P.F.T., B.K., E.G.); monika.murcha@uwa.edu.au.
3
Department Biology 1-Botany, Biocenter Ludwig-Maximilians-University Munich, 82152 Planegg, Germany (I.L.G., A.S., S.K., K.P., J.S.); monika.murcha@uwa.edu.au.
4
Munich Centre for Integrated Protein Science, Ludwig-Maximilians-University Munich, 81377 Munich, Germany (I.L.G., A.S., S.K., J.S.); monika.murcha@uwa.edu.au.
5
Australian Research Council Centre of Excellence in Plant Energy Biology, Department of Animal, Plant, and Soil Science, School of Life Science, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., O.B., J.W.); monika.murcha@uwa.edu.au.
6
Center for Human and Molecular Biology, Plant Biology, Saarland University, 66123 Saarbruecken, Germany (K.P.); and monika.murcha@uwa.edu.au.
7
Institut de Biologie Moléculaire des Plantes-Centre National de la Recherche Scientifique, Université de Strasbourg, 67084 Strasbourg cedex, France (L.M.-D., C.M.) monika.murcha@uwa.edu.au.
8
Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia (M.W.M., S.K.-J., A.I.).
9
Department of Biochemistry and Biophysics, Stockholm University, Arrhenius Laboratories for Natural Sciences, SE-10691 Stockholm, Sweden (P.F.T., B.K., E.G.).
10
Department Biology 1-Botany, Biocenter Ludwig-Maximilians-University Munich, 82152 Planegg, Germany (I.L.G., A.S., S.K., K.P., J.S.).
11
Munich Centre for Integrated Protein Science, Ludwig-Maximilians-University Munich, 81377 Munich, Germany (I.L.G., A.S., S.K., J.S.).
12
Australian Research Council Centre of Excellence in Plant Energy Biology, Department of Animal, Plant, and Soil Science, School of Life Science, La Trobe University, Bundoora, Victoria 3086, Australia (R.N., O.B., J.W.).
13
Center for Human and Molecular Biology, Plant Biology, Saarland University, 66123 Saarbruecken, Germany (K.P.); and.
14
Institut de Biologie Moléculaire des Plantes-Centre National de la Recherche Scientifique, Université de Strasbourg, 67084 Strasbourg cedex, France (L.M.-D., C.M.).

Abstract

A variety of eukaryotes, in particular plants, do not contain the required number of tRNAs to support the translation of mitochondria-encoded genes and thus need to import tRNAs from the cytosol. This study identified two Arabidopsis (Arabidopsis thaliana) proteins, Tric1 and Tric2 (for tRNA import component), which on simultaneous inactivation by T-DNA insertion lines displayed a severely delayed and chlorotic growth phenotype and significantly reduced tRNA import capacity into isolated mitochondria. The predicted tRNA-binding domain of Tric1 and Tric2, a sterile-α-motif at the C-terminal end of the protein, was required to restore tRNA uptake ability in mitochondria of complemented plants. The purified predicted tRNA-binding domain binds the T-arm of the tRNA for alanine with conserved lysine residues required for binding. T-DNA inactivation of both Tric proteins further resulted in an increase in the in vitro rate of in organello protein synthesis, which was mediated by a reorganization of the nuclear transcriptome, in particular of genes encoding a variety of proteins required for mitochondrial gene expression at both the transcriptional and translational levels. The characterization of Tric1/2 provides mechanistic insight into the process of tRNA import into mitochondria and supports the theory that the tRNA import pathway resulted from the repurposing of a preexisting protein import apparatus.

PMID:
27789739
PMCID:
PMC5129730
DOI:
10.1104/pp.16.01519
[Indexed for MEDLINE]
Free PMC Article

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