Details
| Original language | English |
|---|---|
| Pages (from-to) | 420-441 |
| Number of pages | 22 |
| Journal | Plant Journal |
| Volume | 101 |
| Issue number | 2 |
| Early online date | 14 Sept 2019 |
| Publication status | Published - 17 Jan 2020 |
Abstract
Mitochondria host vital cellular functions, including oxidative phosphorylation and co-factor biosynthesis, which are reflected in their proteome. At the cellular level plant mitochondria are organized into hundreds of discrete functional entities, which undergo dynamic fission and fusion. It is the individual organelle that operates in the living cell, yet biochemical and physiological assessments have exclusively focused on the characteristics of large populations of mitochondria. Here, we explore the protein composition of an individual average plant mitochondrion to deduce principles of functional and structural organisation. We perform proteomics on purified mitochondria from cultured heterotrophic Arabidopsis cells with intensity-based absolute quantification and scale the dataset to the single organelle based on criteria that are justified by experimental evidence and theoretical considerations. We estimate that a total of 1.4 million protein molecules make up a single Arabidopsis mitochondrion on average. Copy numbers of the individual proteins span five orders of magnitude, ranging from >40 000 for Voltage-Dependent Anion Channel 1 to sub-stoichiometric copy numbers, i.e. less than a single copy per single mitochondrion, for several pentatricopeptide repeat proteins that modify mitochondrial transcripts. For our analysis, we consider the physical and chemical constraints of the single organelle and discuss prominent features of mitochondrial architecture, protein biogenesis, oxidative phosphorylation, metabolism, antioxidant defence, genome maintenance, gene expression, and dynamics. While assessing the limitations of our considerations, we exemplify how our understanding of biochemical function and structural organization of plant mitochondria can be connected in order to obtain global and specific insights into how organelles work.
Keywords
- antioxidant defence, Arabidopsis thaliana, cofactor synthesis, intensity-based absolute quantification, mitochondrial fission, mitochondrial genome, oxidative phosphorylation, plant mitochondrion, proteomics, RNA editing, single organelle, TCA cycle
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Genetics
- Agricultural and Biological Sciences(all)
- Plant Science
- Biochemistry, Genetics and Molecular Biology(all)
- Cell Biology
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In: Plant Journal, Vol. 101, No. 2, 17.01.2020, p. 420-441.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
T1 - Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics
AU - Fuchs, Philippe
AU - Rugen, Nils
AU - Carrie, Chris
AU - Elsässer, Marlene
AU - Finkemeier, Iris
AU - Giese, Jonas
AU - Hildebrandt, Tatjana M.
AU - Kühn, Kristina
AU - Maurino, Veronica G.
AU - Ruberti, Cristina
AU - Schallenberg-Rüdinger, Mareike
AU - Steinbeck, Janina
AU - Braun, Hans Peter
AU - Eubel, Holger
AU - Meyer, Etienne H.
AU - Müller-Schüssele, Stefanie J.
AU - Schwarzländer, Markus
N1 - Funding Information: We thank Michael Senkler (Hannover) for excellent bioinformatics support. We further thank Ian Max Møller (Aarhus) and José Gualberto (Strasbourg), as well as both anonymous reviewers for critical reading and very helpful comments that have strengthened this manuscript. This work was enabled through the collaborative DFG research grant PAK918 (EU54/4‐1, IF1655/3‐1, MA2379/14‐1, MU4137/1‐1, SCHA1953/3‐1, SCHW1719/5‐1) as part of the ‘Plant Mitochondria in New Light’ initiative.
PY - 2020/1/17
Y1 - 2020/1/17
N2 - Mitochondria host vital cellular functions, including oxidative phosphorylation and co-factor biosynthesis, which are reflected in their proteome. At the cellular level plant mitochondria are organized into hundreds of discrete functional entities, which undergo dynamic fission and fusion. It is the individual organelle that operates in the living cell, yet biochemical and physiological assessments have exclusively focused on the characteristics of large populations of mitochondria. Here, we explore the protein composition of an individual average plant mitochondrion to deduce principles of functional and structural organisation. We perform proteomics on purified mitochondria from cultured heterotrophic Arabidopsis cells with intensity-based absolute quantification and scale the dataset to the single organelle based on criteria that are justified by experimental evidence and theoretical considerations. We estimate that a total of 1.4 million protein molecules make up a single Arabidopsis mitochondrion on average. Copy numbers of the individual proteins span five orders of magnitude, ranging from >40 000 for Voltage-Dependent Anion Channel 1 to sub-stoichiometric copy numbers, i.e. less than a single copy per single mitochondrion, for several pentatricopeptide repeat proteins that modify mitochondrial transcripts. For our analysis, we consider the physical and chemical constraints of the single organelle and discuss prominent features of mitochondrial architecture, protein biogenesis, oxidative phosphorylation, metabolism, antioxidant defence, genome maintenance, gene expression, and dynamics. While assessing the limitations of our considerations, we exemplify how our understanding of biochemical function and structural organization of plant mitochondria can be connected in order to obtain global and specific insights into how organelles work.
AB - Mitochondria host vital cellular functions, including oxidative phosphorylation and co-factor biosynthesis, which are reflected in their proteome. At the cellular level plant mitochondria are organized into hundreds of discrete functional entities, which undergo dynamic fission and fusion. It is the individual organelle that operates in the living cell, yet biochemical and physiological assessments have exclusively focused on the characteristics of large populations of mitochondria. Here, we explore the protein composition of an individual average plant mitochondrion to deduce principles of functional and structural organisation. We perform proteomics on purified mitochondria from cultured heterotrophic Arabidopsis cells with intensity-based absolute quantification and scale the dataset to the single organelle based on criteria that are justified by experimental evidence and theoretical considerations. We estimate that a total of 1.4 million protein molecules make up a single Arabidopsis mitochondrion on average. Copy numbers of the individual proteins span five orders of magnitude, ranging from >40 000 for Voltage-Dependent Anion Channel 1 to sub-stoichiometric copy numbers, i.e. less than a single copy per single mitochondrion, for several pentatricopeptide repeat proteins that modify mitochondrial transcripts. For our analysis, we consider the physical and chemical constraints of the single organelle and discuss prominent features of mitochondrial architecture, protein biogenesis, oxidative phosphorylation, metabolism, antioxidant defence, genome maintenance, gene expression, and dynamics. While assessing the limitations of our considerations, we exemplify how our understanding of biochemical function and structural organization of plant mitochondria can be connected in order to obtain global and specific insights into how organelles work.
KW - antioxidant defence
KW - Arabidopsis thaliana
KW - cofactor synthesis
KW - intensity-based absolute quantification
KW - mitochondrial fission
KW - mitochondrial genome
KW - oxidative phosphorylation
KW - plant mitochondrion
KW - proteomics
KW - RNA editing
KW - single organelle
KW - TCA cycle
UR - http://www.scopus.com/inward/record.url?scp=85074860583&partnerID=8YFLogxK
U2 - 10.1111/tpj.14534
DO - 10.1111/tpj.14534
M3 - Article
C2 - 31520498
AN - SCOPUS:85074860583
VL - 101
SP - 420
EP - 441
JO - Plant Journal
JF - Plant Journal
SN - 0960-7412
IS - 2
ER -