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Plant J. 2019 Sep 14. doi: 10.1111/tpj.14534. [Epub ahead of print]

Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics.

Author information

1
Institut für Biologie und Biotechnologie der Pflanzen (IBBP), Westfälische Wilhelms-Universität, Schlossplatz 7-8, 48143, Münster, Germany.
2
Institut für Nutzpflanzenforschung und Ressourcenschutz (INRES), Rheinische Friedrich-Wilhelms-Universität Bonn, Friedrich-Ebert-Allee 144, 53113, Bonn, Germany.
3
Institut für Pflanzengenetik, Leibniz Universität Hannover, Herrenhäuser Str. 2, 30419, Hannover, Germany.
4
Department Biologie I - Botanik, Ludwig-Maximilians-Universität München, Grosshadernerstr. 2-4, 82152, Planegg-Martinsried, Germany.
5
Institut für Zelluläre und Molekulare Botanik (IZMB), Rheinische Friedrich-Wilhelms-Universität Bonn, Kirschallee 1, 53115, Bonn, Germany.
6
Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Weinbergweg 10, 06120, Halle/Saale, Germany.
7
Institute of Developmental and Molecular Biology of Plants, and Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University Düsseldorf, Universitätsstraße 1, 40225, Düsseldorf, Germany.

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 (VDAC1) to sub-stoichiometric copy numbers, i.e. less than a single copy per single mitochondrion, for several pentatricopeptide repeat (PPR) 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:

Arabidopsis thaliana ; RNA editing; TCA cycle; antioxidant defence; cofactor synthesis; intensity-based absolute quantification; mitochondrial fission; mitochondrial genome; oxidative phosphorylation; plant mitochondrion; proteomics; single organelle

PMID:
31520498
DOI:
10.1111/tpj.14534

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