Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

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

References

  • Arimura S, Fujimoto M, Doniwa Y, Kadoya N, Nakazono M, Sakamoto W, Tsutsumi N (2008) Arabidopsis ELONGATED MITOCHONDRIA1 is required for the localization of dynamin-related protein DRP3A to mitochondrial fission sites. Plant Cell 20:1555–1566

    Article  CAS  Google Scholar 

  • Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K, Modla S, Czymmek K, Dinesh-Kumar SP (2015) Chloroplast stromules function during innate immunity. Dev Cell 34:45–57

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  CAS  Google Scholar 

  • Cox RT, Spradling AC (2009) clueless, a conserved Drosophila gene required for mitochondrial subcellular localization, interacts genetically with parkin. Dis Model Mech 2:490–499

    Article  CAS  Google Scholar 

  • Doniwa Y, Arimura SI, Tsutsumi N (2007) Mitochondria use actin filaments as rails for fast translocation in Arabidopsis and tobacco cells. Plant Biotechnol 24:441–447

    Article  CAS  Google Scholar 

  • El Zawily AM, Schwarzländer M, Finkemeier I, Johnston IG, Benamar A, Cao Y, Gissot C, Meyer AJ, Wilson K, Datla R, Macherel D, Jones NS, Logan DC (2014) FRIENDLY regulates mitochondrial distribution, fusion, and quality control in Arabidopsis. Plant Physiol 166(2):808–828

    Article  Google Scholar 

  • Exposito-Rodriguez M, Laissue P, Yvon-Durocher G, Smirnoff N, Mullineaux P (2017) Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat Commun 8:49

    Article  Google Scholar 

  • Feng XG, Arimura S, Hirano HY, Sakamoto W, Tsutsumi N (2004) Isolation of mutants with aberrant mitochondrial morphology from Arabidopsis thaliana. Genes Genet Syst 79:301–305

    Article  CAS  Google Scholar 

  • Fields SD, Conrad MN, Clarke M (1998) The S. cerevisiae CLU1 and D. discoideum cluA genes are functional homologues that influence mitochondrial morphology and distribution. J Cell Sci 111(Pt 12):1717–1727

    CAS  PubMed  Google Scholar 

  • Fields SD, Arana Q, Heuser J, Clarke M (2002) Mitochondrial membrane dynamics are altered in cluA- mutants of Dictyostelium. J Muscle Res Cell Motil 23:829–838

    Article  CAS  Google Scholar 

  • Fujimoto M, Arimura S, Ueda T, Takanashi H, Hayashi Y, Nakano A, Tsutsumi N (2010) Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc Natl Acad Sci USA 107:6094–6099

    Article  CAS  Google Scholar 

  • Gao J, Schatton D, Martinelli P, Hansen H, Pla-Martin D, Barth E, Becker C, Altmueller J, Frommolt P, Sardiello M, Rugarli EI (2014) CLUH regulates mitochondrial biogenesis by binding mRNAs of nuclear-encoded mitochondrial proteins. J Cell Biol 207(2):213–223

    Article  CAS  Google Scholar 

  • Gotoh E, Suetsugu N, Yamori W, Ishishita K, Kiyabu R, Fukuda M, Higa T, Shirouchi B, Wada M (2018) Chloroplast accumulation response enhances leaf photosynthesis and plant biomass production. Plant Physiol 2018(178):1358–1369

    Article  Google Scholar 

  • Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y, Hashimoto T, Baskin TI (2012) RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol 53:699–708

    Article  CAS  Google Scholar 

  • Huang J, Fujimoto M, Fujiwara M, Fukao Y, Arimura S, Tsutsumi N (2015) Arabidopsis dynamin-related proteins, DRP2A and DRP2B, function coordinately in post-Golgi trafficking. Biochem Biophys Res Commun 456:238–244

    Article  CAS  Google Scholar 

  • Islam MS, Niwa Y, Takagi S (2009) Light-dependent intracellular positioning of mitochondria in Arabidopsis thaliana mesophyll cells. Plant Cell Physiol 50(6):1032–1040

    Article  CAS  Google Scholar 

  • Islam MS, Van Nguyen T, Sakamoto W, Takagi S (2020) Phototropin‐ and photosynthesis‐dependent mitochondrial positioning in Arabidopsis thaliana mesophyll cells. J Integr Plant Biol.

  • Iwabuchi K, Minamino R, Takagi S (2010) Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis leaf cells. Plant Physiol 152:1309–1319

    Article  CAS  Google Scholar 

  • Iwabuchi K, Hidema J, Tamura K, Takagi S, Hara-Nishimura I (2016) Plant nuclei move to escape ultraviolet-induced DNA damage and cell death. Plant Physiol 170:678–685

    Article  CAS  Google Scholar 

  • Jaipargas EA, Mathur N, Bou Daher F, Wasteneys GO, Mathur J (2016) High light intensity leads to increased peroxule-mitochondria interactions in plants. Front Cell Dev Biol 4:6

    Article  Google Scholar 

  • Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Nat Acad Sci USA 106:13106–13111

    Article  CAS  Google Scholar 

  • Kong SG, Wada M (2016) Molecular basis of chloroplast photorelocation movement. J Plant Res 129:159–166

    Article  CAS  Google Scholar 

  • Larkin RM, Stefano G, Ruckle ME, Stavoe AK, Sinkler CA, Brandizzi F, Malmstrom CM, Osteryoung KW (2016) Reduced chloroplast coverage genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment. Proc Nat Acad Sci USA 113(8):E1116–E1125

    Article  CAS  Google Scholar 

  • Lellis AD, Patrick RM, Mayberry LK, Lorence A, Campbell ZC, Roose JL, Frankel LK, Bricker TM, Hellmann HA, Mayberry RW, Zavala AS, Choy GS, Wylie DC, Abdul-Moheeth M, Masood A, Prater AG, Van Hoorn HE, Cole NA, Browning KS (2019) eIFiso4G augments the synthesis of specific plant proteins involved in normal chloroplast function. Plant physiol.

  • Li ZY, Xu ZS, He GY, Yang GX, Chen M, Li LC, Ma Y (2013) The voltage-dependent anion channel 1 (AtVDAC1) negatively regulates plant cold responses during germination and seedling development in Arabidopsis and interacts with calcium sensor CBL1. Int J Mol Sci 14:701–713

    Article  CAS  Google Scholar 

  • Logan DC, Scott I, Tobin AK (2003) The genetic control of plant mitochondrial morphology and dynamics. Plant J 36:500–509

    Article  CAS  Google Scholar 

  • Michaud M, Ubrig E, Filleur S, Erhardt M, Ephritikhine G, Maréchal-Drouard L, Duchêne AM (2014) Differential targeting of VDAC3 mRNA isoforms influences mitochondria morphology. Proc Nat Acad Sci USA 111:8991–8996

    Article  CAS  Google Scholar 

  • Mitchell SF, Jain S, She M, Parker R (2012) Global analysis of yeast mRNPs. Nat Struct Mol Biol 20:127–133

    Article  Google Scholar 

  • Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H (2007) ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res 35:D863–D869

    Article  CAS  Google Scholar 

  • Oikawa K, Matsunaga S, Mano S, Kondo M, Yamada K, Hayashi M, Kagawa T, Kadota A, Sakamoto W, Higashi S, Watanabe M, Mitsui T, Shigemasa A, Iino T, Hosokawa Y, Nishimura M (2015) Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat Plants 1:15035

    Article  CAS  Google Scholar 

  • Sanyal SK, Kanwar P, Fernandes JL, Mahiwal S, Yadav AK, Samtani H, Srivastava AK, Suprasanna P, Pandey GK (2020) Arabidopsis mitochondrial voltage-dependent anion channels are involved in maintaining reactive oxygen species homeostasis, oxidative and salt stress tolerance in yeast. Front Plant Sci 11:50

    Article  Google Scholar 

  • Schatton D, Pla-Martin D, Marx MC, Hansen H, Mourier A, Nemazanyy I, Pessia A, Zentis P, Corona T, Kondylis V, Barth E, Schauss AC, Velagapudi V, Rugarli EI (2017) CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs. J Cell Biol 216(3):675–693

    Article  CAS  Google Scholar 

  • Sen A, Damm VT, Cox RT (2013) Drosophila clueless is highly expressed in larval neuroblasts, affects mitochondrial localization and suppresses mitochondrial oxidative damage. PLoS ONE 8(1):e54283

    Article  CAS  Google Scholar 

  • Sen A, Kalvakuri S, Bodmer R, Cox RT (2015) Clueless, a protein required for mitochondrial function, interacts with the PINK1-Parkin complex in Drosophila. Dis Model Mech 8(6):577–589

    Article  CAS  Google Scholar 

  • Sheard KM, Thibault-Sennett SA, Sen A, Shewmaker F, Cox RT (2020) Clueless forms dynamic, insulin-responsive bliss particles sensitive to stress. Dev Biol 459:149–160

    Article  CAS  Google Scholar 

  • Vincent T, Vingadassalon A, Ubrig E, Azeredo K, Srour O, Cognat V, Graindorge S, Salinas T, Maréchal-Drouard L, Duchêne AM (2017) A genome-scale analysis of mRNAs targeting to plant mitochondria: Upstream AUGs in 59 untranslated regions reduce mitochondrial association. Plant J 92:1132–1142

    Article  CAS  Google Scholar 

  • Vornlocher HP, Hanachi P, Ribeiro S, Hershey JWB (1999) A 110- kilodalton subunit of translation initiation factor eIF3 and an associated 135- kilodalton protein are encoded by the Saccharomyces cerevisiae TIF32 and TIF31 genes. J Biol Chem 274:16802–16812

    Article  CAS  Google Scholar 

  • Wakim J, Goudenege D, Perrot R, Gueguen N, Desquiret-Dumas V, Chao de la Barca JM, Dalla Rosa I, Manero F, Le Mao M, Chupin S, Chevrollier A, Procaccio V, Bonneau D, Logan DC, Reynier P, Lenaers G, Khiati S (2017) CLUH couples mitochondrial distribution to the energetic and metabolic status. J Cell Sci 130(11):1940–1951

    Article  CAS  Google Scholar 

  • White RR, Lin C, Leaves I, Castro IG, Metz J, Bateman BC, Botchway SW, Ward AD, Ashwin P, Sparkes I (2020) Miro2 tethers the ER to mitochondria to promote mitochondrial fusion in tobacco leaf epidermal cells. Commun Biol 3:161

    Article  CAS  Google Scholar 

  • Zhu Q, Hulen D, Liu T, Clarke M (1997) The cluA− mutant of Dictyostelium identifies a novel class of genes required for dispersion of mitochondria. Proc Nat Acad Sci USA 94:7308–7313

    Article  CAS  Google Scholar 

Download references

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.).

Author information

Authors and Affiliations

  1. Graduate School of Agricultural & Life Sciences, University of Tokyo, Tokyo, Japan

    Hiroki Ayabe, Narumi Kawai, Mitsuhiro Shibamura, Masaru Fujimoto, Nobuhiro Tsutsumi & Shin-ichi Arimura

  2. Graduate School of Life Science, Ritsumeikan University, Shiga, Japan

    Yoichiro Fukao

Authors
  1. Hiroki Ayabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Narumi Kawai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitsuhiro Shibamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoichiro Fukao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masaru Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nobuhiro Tsutsumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shin-ichi Arimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Shin-ichi Arimura.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Kinya Toriyama.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

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)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02634-9

Keywords

Search

Navigation