A Mitochondrial LYR Protein Is Required for Complex I Assembly

Aneta Ivanova, Mabel Gill-Hille, Shaobai Huang, Rui M. Branca, Beata Kmiec, Pedro F. Teixeira, Janne Lehtiö, James Whelan, Monika W. Murcha

Research output: Contribution to journalArticle

Abstract

Complex I biogenesis requires the expression of both nuclear and mitochondrial genes, the import of proteins, cofactor biosynthesis, and the assembly of at least 49 individual subunits. Assembly factors interact with subunits of Complex I but are not part of the final holocomplex. We show that in Arabidopsis (Arabidopsis thaliana), a mitochondrial matrix protein (EMB1793, At1g76060), which we term COMPLEX I ASSEMBLY FACTOR 1 (CIAF1), contains a LYR domain and is required for Complex I assembly. T-DNA insertion mutants of CIAF1 lack Complex I and the Supercomplex I+III. Biochemical characterization shows that the assembly of Complex I is stalled at 650 and 800 kD intermediates in mitochondria isolated from ciaf1 mutant lines.I. Yeast-two-hybrid interaction and complementation assays indicate that CIAF1 specifically interacts with the 23-kD TYKY-1 matrix domain subunit of Complex I and likely plays a role in Fe-S insertion into this subunit. These data show that CIAF1 plays an essential role in assembling the peripheral matrix arm Complex I subunits into the Complex I holoenzyme.

Original languageEnglish
Pages (from-to)1632-1650
Number of pages19
JournalPlant Physiology
Volume181
Issue number4
DOIs
Publication statusPublished - 1 Dec 2019

Fingerprint

Mitochondrial Proteins
Arabidopsis
mutants
Holoenzymes
Mitochondrial Genes
Protein Biosynthesis
imports
Mitochondria
mitochondria
Arabidopsis thaliana
proteins
Yeasts
biosynthesis
yeasts
DNA
assays
Proteins
genes
T-DNA
biogenesis

Cite this

Ivanova, Aneta ; Gill-Hille, Mabel ; Huang, Shaobai ; Branca, Rui M. ; Kmiec, Beata ; Teixeira, Pedro F. ; Lehtiö, Janne ; Whelan, James ; Murcha, Monika W. / A Mitochondrial LYR Protein Is Required for Complex I Assembly. In: Plant Physiology. 2019 ; Vol. 181, No. 4. pp. 1632-1650.
@article{ba885e37af3941f9843685a0ee9d1761,
title = "A Mitochondrial LYR Protein Is Required for Complex I Assembly",
abstract = "Complex I biogenesis requires the expression of both nuclear and mitochondrial genes, the import of proteins, cofactor biosynthesis, and the assembly of at least 49 individual subunits. Assembly factors interact with subunits of Complex I but are not part of the final holocomplex. We show that in Arabidopsis (Arabidopsis thaliana), a mitochondrial matrix protein (EMB1793, At1g76060), which we term COMPLEX I ASSEMBLY FACTOR 1 (CIAF1), contains a LYR domain and is required for Complex I assembly. T-DNA insertion mutants of CIAF1 lack Complex I and the Supercomplex I+III. Biochemical characterization shows that the assembly of Complex I is stalled at 650 and 800 kD intermediates in mitochondria isolated from ciaf1 mutant lines.I. Yeast-two-hybrid interaction and complementation assays indicate that CIAF1 specifically interacts with the 23-kD TYKY-1 matrix domain subunit of Complex I and likely plays a role in Fe-S insertion into this subunit. These data show that CIAF1 plays an essential role in assembling the peripheral matrix arm Complex I subunits into the Complex I holoenzyme.",
author = "Aneta Ivanova and Mabel Gill-Hille and Shaobai Huang and Branca, {Rui M.} and Beata Kmiec and Teixeira, {Pedro F.} and Janne Lehti{\"o} and James Whelan and Murcha, {Monika W.}",
year = "2019",
month = "12",
day = "1",
doi = "10.1104/pp.19.00822",
language = "English",
volume = "181",
pages = "1632--1650",
journal = "Plant Physiology (Online)",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "4",

}

Ivanova, A, Gill-Hille, M, Huang, S, Branca, RM, Kmiec, B, Teixeira, PF, Lehtiö, J, Whelan, J & Murcha, MW 2019, 'A Mitochondrial LYR Protein Is Required for Complex I Assembly' Plant Physiology, vol. 181, no. 4, pp. 1632-1650. https://doi.org/10.1104/pp.19.00822

A Mitochondrial LYR Protein Is Required for Complex I Assembly. / Ivanova, Aneta; Gill-Hille, Mabel; Huang, Shaobai; Branca, Rui M.; Kmiec, Beata; Teixeira, Pedro F.; Lehtiö, Janne; Whelan, James; Murcha, Monika W.

In: Plant Physiology, Vol. 181, No. 4, 01.12.2019, p. 1632-1650.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A Mitochondrial LYR Protein Is Required for Complex I Assembly

AU - Ivanova, Aneta

AU - Gill-Hille, Mabel

AU - Huang, Shaobai

AU - Branca, Rui M.

AU - Kmiec, Beata

AU - Teixeira, Pedro F.

AU - Lehtiö, Janne

AU - Whelan, James

AU - Murcha, Monika W.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Complex I biogenesis requires the expression of both nuclear and mitochondrial genes, the import of proteins, cofactor biosynthesis, and the assembly of at least 49 individual subunits. Assembly factors interact with subunits of Complex I but are not part of the final holocomplex. We show that in Arabidopsis (Arabidopsis thaliana), a mitochondrial matrix protein (EMB1793, At1g76060), which we term COMPLEX I ASSEMBLY FACTOR 1 (CIAF1), contains a LYR domain and is required for Complex I assembly. T-DNA insertion mutants of CIAF1 lack Complex I and the Supercomplex I+III. Biochemical characterization shows that the assembly of Complex I is stalled at 650 and 800 kD intermediates in mitochondria isolated from ciaf1 mutant lines.I. Yeast-two-hybrid interaction and complementation assays indicate that CIAF1 specifically interacts with the 23-kD TYKY-1 matrix domain subunit of Complex I and likely plays a role in Fe-S insertion into this subunit. These data show that CIAF1 plays an essential role in assembling the peripheral matrix arm Complex I subunits into the Complex I holoenzyme.

AB - Complex I biogenesis requires the expression of both nuclear and mitochondrial genes, the import of proteins, cofactor biosynthesis, and the assembly of at least 49 individual subunits. Assembly factors interact with subunits of Complex I but are not part of the final holocomplex. We show that in Arabidopsis (Arabidopsis thaliana), a mitochondrial matrix protein (EMB1793, At1g76060), which we term COMPLEX I ASSEMBLY FACTOR 1 (CIAF1), contains a LYR domain and is required for Complex I assembly. T-DNA insertion mutants of CIAF1 lack Complex I and the Supercomplex I+III. Biochemical characterization shows that the assembly of Complex I is stalled at 650 and 800 kD intermediates in mitochondria isolated from ciaf1 mutant lines.I. Yeast-two-hybrid interaction and complementation assays indicate that CIAF1 specifically interacts with the 23-kD TYKY-1 matrix domain subunit of Complex I and likely plays a role in Fe-S insertion into this subunit. These data show that CIAF1 plays an essential role in assembling the peripheral matrix arm Complex I subunits into the Complex I holoenzyme.

UR - http://www.scopus.com/inward/record.url?scp=85075812755&partnerID=8YFLogxK

U2 - 10.1104/pp.19.00822

DO - 10.1104/pp.19.00822

M3 - Article

VL - 181

SP - 1632

EP - 1650

JO - Plant Physiology (Online)

JF - Plant Physiology (Online)

SN - 0032-0889

IS - 4

ER -

Ivanova A, Gill-Hille M, Huang S, Branca RM, Kmiec B, Teixeira PF et al. A Mitochondrial LYR Protein Is Required for Complex I Assembly. Plant Physiology. 2019 Dec 1;181(4):1632-1650. https://doi.org/10.1104/pp.19.00822