1. Plant Biology
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Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis

  1. Kurataka Otsuka
  2. Akihito Mamiya
  3. Mineko Konishi
  4. Mamoru Nozaki
  5. Atsuko Kinoshita
  6. Hiroaki Tamaki
  7. Masaki Arita
  8. Masato Saito
  9. Kayoko Yamamoto
  10. Takushi Hachiya
  11. Ko Noguchi
  12. Takashi Ueda
  13. Yusuke Yagi
  14. Takehito Kobayashi
  15. Takahiro Nakamura
  16. Yasushi Sato
  17. Takashi Hirayama
  18. Munetaka Sugiyama  Is a corresponding author
  1. The University of Tokyo, Japan
  2. Tokyo Metropolitan University, Japan
  3. Shimane University, Japan
  4. Tokyo University of Pharmacy and Life Sciences, Japan
  5. National Institute for Basic Biology, Japan
  6. Kyushu University, Japan
  7. Ehime University, Japan
  8. Okayama University, Japan
Research Article
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Cite this article as: eLife 2021;10:e61611 doi: 10.7554/eLife.61611

Abstract

Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) mutants of Arabidopsis, root redifferentiation defective 1 (rrd1), rrd2, and root initiation defective 4 (rid4), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e., fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis.

Data availability

The microarray data has been deposited in the Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE34595. All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

The following data sets were generated

Article and author information

Author details

  1. Kurataka Otsuka

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Akihito Mamiya

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Mineko Konishi

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Mamoru Nozaki

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Atsuko Kinoshita

    Biological Sciences, Tokyo Metropolitan University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9095-389X
  6. Hiroaki Tamaki

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Masaki Arita

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Masato Saito

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Kayoko Yamamoto

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  10. Takushi Hachiya

    Department of Molecular and Functional Genomics, Interdisciplinary Center for Science Research, Shimane University, Matsue, Japan
    Competing interests
    The authors declare that no competing interests exist.
  11. Ko Noguchi

    School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3588-3643
  12. Takashi Ueda

    Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5190-892X
  13. Yusuke Yagi

    Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, Fukuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  14. Takehito Kobayashi

    Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, Fukuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  15. Takahiro Nakamura

    Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, Fukuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  16. Yasushi Sato

    Biology and Environmental Science, Graduate School of Science and Engineering, Ehime University, Matsuyama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  17. Takashi Hirayama

    Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  18. Munetaka Sugiyama

    Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo, Japan
    For correspondence
    sugiyama@ns.bg.s.u-tokyo.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7050-8964

Funding

Japan Society for the Promotion of Science (Grants-in-Aid for JSPS Fellows (No. 09J08676))

  • Kurataka Otsuka

Japan Society for the Promotion of Science London (Grants-in-Aid for JSPS Fellows (No. 17J05722))

  • Akihito Mamiya

Ministry of Education, Culture, Sports, Science and Technology (Graduate Program for Leaders in Life Innovation (GPLLI))

  • Akihito Mamiya

Ministry of Education, Culture, Sports, Science and Technology (Grant-in-Aid for Scientific Research on Priority Areas (No. 19060001))

  • Munetaka Sugiyama

Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research (B) (No. 25291057))

  • Munetaka Sugiyama

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Freiburg, Germany

Publication history

  1. Received: July 30, 2020
  2. Accepted: January 13, 2021
  3. Accepted Manuscript published: January 14, 2021 (version 1)
  4. Version of Record published: January 29, 2021 (version 2)

Copyright

© 2021, Otsuka et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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