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FMT, a protein that affects mitochondrial distribution, interacts with translation-related proteins in Arabidopsis thaliana

Abstract

Key message

Two translation-related proteins are identified as FMT-interacting proteins. However, FMT, unlike mutants of other CLU genes in fly and human, has no clear impact on the accumulation of mitochondrial proteins.

Abstract

Organelle distribution is critical for effective metabolism and stress response and is controlled by various environmental factors. Clustered mitochondria (CLU) superfamily genes affect mitochondrial distribution and their disruptions cause mitochondria to cluster within a cell in various species including yeast, fly, mammals and Arabidopsis. In Arabidopsis thaliana, Friendly mitochondria (FMT) is a CLU gene that is required for normal mitochondrial distribution, but its molecular function is unclear. Here, we demonstrate that FMT interacts with some translation-related proteins (translation initiation factor eIFiso4G1 and glutamyl-tRNA synthetase OVA9), as well as itself. We also show FMT forms dynamic particles in the cytosol that sometimes move with mitochondria, and their movements are mainly controlled by actin filaments but also by microtubules. Similar results have been reported for animal CLU orthologs. However, an fmt mutant, unlike animal clu mutants, did not show any clear decrease of nuclear-encoded mitochondrial protein levels. This difference may reflect a functional divergence of FMT from other CLU superfamily genes.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Drs. Takashi Ueda (The University of Tokyo), Richard J. Cyr (Pennsylvania State University) and Nam-Hai Chua (The Rockefeller University) for their kind donation of vectors. We also thank the Salk Institute for providing the seeds of Arabidopsis T-DNA insertion mutants. This work was supported by grants from the Takeda Science Foundation to SA and partly from the Japan Society for the Promotion of Science (Grant Number 20H00417 and 20H05680 to N. T., and 19H02927 and 19KK0391 to S. A.).

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NT and SA conceived and designed research. NK and MS conducted experiments. YF contributed CoIP–MS experiment and analysis. MF and SA contributed microscopic observations. HA, NK and MS analyzed data. HA, NK, MS and SA wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Shin-ichi Arimura.

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Communicated by Kinya Toriyama.

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299_2020_2634_MOESM1_ESM.tif

Mitochondrial distribution in stem epidermal cells of fmt mutants. Mitochondria in stem epidermal cells of wild type (left), fmt-tag2 (middle) and fmt-2 (right) were observed. Mitochondria are visualized by mt-GFP (green) in all lines. Scale bar = 20 µm (TIF 19023 KB)

299_2020_2634_MOESM2_ESM.tif

Schematic drawing of constructs used in Y2H assay. The boxes indicate domains predicted by Conserved Domain Database. Numbers indicate the positions of amino acid residues from N-terminus (position 1) to C-terminus (position 1420). The purple bars indicate the regions cloned into the vectors which contains each of the domains (TIF 2386 KB)

Supplementary file 3 (XLSX 23 KB)

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Ayabe, H., Kawai, N., Shibamura, M. et al. FMT, a protein that affects mitochondrial distribution, interacts with translation-related proteins in Arabidopsis thaliana. Plant Cell Rep 40, 327–337 (2021). https://doi.org/10.1007/s00299-020-02634-9

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Keywords

  • Arabidopsis thaliana
  • Mitochondria
  • Mitochondrial dynamics
  • Organellar translation
  • Friendly mitochondria