Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria

Monika W. Murcha, Szymon Kubiszewski-Jakubiak, P.F. Teixeira, I.L. Gügel, B. Kmiec, R. Narsai, Aneta Ivanova, C. Megel, A. Schock, S. Kraus, O. Berkowitz, E. Glaser, K. Philippar, L. Maréchal-Drouard, J. Soll, J. Whelan

Research output: Contribution to journalArticle

5 Citations (Scopus)
338 Downloads (Pure)

Abstract

© 2016 American Society of Plant Biologists. All rights reserved.
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-a-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.
Original languageEnglish
Pages (from-to)2471-2490
Number of pages20
JournalPlant Physiology
Volume172
Issue number4
Early online date29 Nov 2016
DOIs
Publication statusPublished - Dec 2016

Fingerprint

amino acid transporters
Amino Acid Transport Systems
Transfer RNA
imports
Mitochondria
mitochondria
Proteins
proteins
inactivation
DNA
cytosol
transcriptome
alanine
translation (genetics)
biologists
eukaryotic cells
Arabidopsis Proteins
lysine
genes
Arabidopsis thaliana

Cite this

Murcha, M. W., Kubiszewski-Jakubiak, S., Teixeira, P. F., Gügel, I. L., Kmiec, B., Narsai, R., ... Whelan, J. (2016). Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria. Plant Physiology, 172(4), 2471-2490. https://doi.org/10.1104/pp.16.01519
Murcha, Monika W. ; Kubiszewski-Jakubiak, Szymon ; Teixeira, P.F. ; Gügel, I.L. ; Kmiec, B. ; Narsai, R. ; Ivanova, Aneta ; Megel, C. ; Schock, A. ; Kraus, S. ; Berkowitz, O. ; Glaser, E. ; Philippar, K. ; Maréchal-Drouard, L. ; Soll, J. ; Whelan, J. / Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria. In: Plant Physiology. 2016 ; Vol. 172, No. 4. pp. 2471-2490.
@article{b35f65f834ec43a793173154a8300a72,
title = "Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria",
abstract = "{\circledC} 2016 American Society of Plant Biologists. All rights reserved.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-a-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.",
author = "Murcha, {Monika W.} and Szymon Kubiszewski-Jakubiak and P.F. Teixeira and I.L. G{\"u}gel and B. Kmiec and R. Narsai and Aneta Ivanova and C. Megel and A. Schock and S. Kraus and O. Berkowitz and E. Glaser and K. Philippar and L. Mar{\'e}chal-Drouard and J. Soll and J. Whelan",
year = "2016",
month = "12",
doi = "10.1104/pp.16.01519",
language = "English",
volume = "172",
pages = "2471--2490",
journal = "Plant Physiology (Online)",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "4",

}

Murcha, MW, Kubiszewski-Jakubiak, S, Teixeira, PF, Gügel, IL, Kmiec, B, Narsai, R, Ivanova, A, Megel, C, Schock, A, Kraus, S, Berkowitz, O, Glaser, E, Philippar, K, Maréchal-Drouard, L, Soll, J & Whelan, J 2016, 'Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria' Plant Physiology, vol. 172, no. 4, pp. 2471-2490. https://doi.org/10.1104/pp.16.01519

Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria. / Murcha, Monika W.; Kubiszewski-Jakubiak, Szymon; Teixeira, P.F.; Gügel, I.L.; Kmiec, B.; Narsai, R.; Ivanova, Aneta; Megel, C.; Schock, A.; Kraus, S.; Berkowitz, O.; Glaser, E.; Philippar, K.; Maréchal-Drouard, L.; Soll, J.; Whelan, J.

In: Plant Physiology, Vol. 172, No. 4, 12.2016, p. 2471-2490.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Plant specific Preprotein and Amino Acid Transporter proteins are required for tRNA import into mitochondria

AU - Murcha, Monika W.

AU - Kubiszewski-Jakubiak, Szymon

AU - Teixeira, P.F.

AU - Gügel, I.L.

AU - Kmiec, B.

AU - Narsai, R.

AU - Ivanova, Aneta

AU - Megel, C.

AU - Schock, A.

AU - Kraus, S.

AU - Berkowitz, O.

AU - Glaser, E.

AU - Philippar, K.

AU - Maréchal-Drouard, L.

AU - Soll, J.

AU - Whelan, J.

PY - 2016/12

Y1 - 2016/12

N2 - © 2016 American Society of Plant Biologists. All rights reserved.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-a-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.

AB - © 2016 American Society of Plant Biologists. All rights reserved.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-a-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.

U2 - 10.1104/pp.16.01519

DO - 10.1104/pp.16.01519

M3 - Article

VL - 172

SP - 2471

EP - 2490

JO - Plant Physiology (Online)

JF - Plant Physiology (Online)

SN - 0032-0889

IS - 4

ER -