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Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes

Yusuke Kimata, Takehide Kato, Takumi Higaki, Daisuke Kurihara, Tomomi Yamada, Shoji Segami, Miyo Terao Morita, Masayoshi Maeshima, Seiichiro Hasezawa, Tetsuya Higashiyama, Masao Tasaka, and Minako Ueda
PNAS February 5, 2019 116 (6) 2338-2343; published ahead of print February 5, 2019 https://doi.org/10.1073/pnas.1814160116
Yusuke Kimata
aDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602 Aichi, Japan;
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Takehide Kato
bGraduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, 630-0192 Nara, Japan;
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Takumi Higaki
cDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha, Kashiwa, 277-8562 Chiba, Japan;dInternational Research Organization for Advanced Science and Technology, Kumamoto University, Chuo-ku, 860-8555 Kumamoto, Japan;
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Daisuke Kurihara
aDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602 Aichi, Japan;
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Tomomi Yamada
aDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602 Aichi, Japan;eInstitute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601 Aichi, Japan;
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Shoji Segami
fGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601 Aichi, Japan;
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Miyo Terao Morita
fGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601 Aichi, Japan;gNational Institute for Basic Biology, Myodaiji, Okazaki, 444-8585 Aichi, Japan
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Masayoshi Maeshima
fGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601 Aichi, Japan;
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Seiichiro Hasezawa
cDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha, Kashiwa, 277-8562 Chiba, Japan;
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Tetsuya Higashiyama
aDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602 Aichi, Japan;eInstitute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601 Aichi, Japan;
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Masao Tasaka
bGraduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, 630-0192 Nara, Japan;
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Minako Ueda
aDivision of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602 Aichi, Japan;eInstitute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601 Aichi, Japan;
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  • ORCID record for Minako Ueda
  • For correspondence: m-ueda@itbm.nagoya-u.ac.jp
  1. Edited by Dominique C. Bergmann, Stanford University, Stanford, CA, and approved December 14, 2018 (received for review August 27, 2018)

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Significance

The vacuole is one of the largest plant organelles. It occupies the basal region of the zygote and is mostly inherited in the basal daughter cell after zygotic division. In spite of the obvious asymmetry, how dynamically the vacuole is distributed and whether it contributes to apical–basal axis formation are unknown. In the present study, we report that the vacuole actively changes its shape and size and positions along actin filaments. We further show that vacuolar distribution supports nuclear localization at the opposite cell end, and thus ensures asymmetric division of the zygote. These results provide insights into cooperative organelle positioning during zygote polarization and the crucial roles of vacuoles in the initial steps of plant ontogeny.

Abstract

In most flowering plants, the asymmetric cell division of the zygote is the initial step in establishing the apical–basal axis of the mature plant. The zygote is polarized, possessing the nucleus at the apical tip and large vacuoles at the basal end. Despite their known polar localization, whether the positioning of the vacuoles and the nucleus is coordinated and what the role of the vacuole is in the asymmetric zygotic division remain elusive. In the present study, we utilized a live-cell imaging system to visualize the dynamics of vacuoles during the entire process of zygote polarization in Arabidopsis. Image analysis revealed that the vacuoles formed tubular strands around the apically migrating nucleus. They gradually accumulated at the basal region and filled the space, resulting in asymmetric distribution in the mature zygote. To assess the role of vacuoles in the zygote, we screened various vacuole mutants and identified that shoot gravitropism2 (sgr2), in which the vacuolar structural change was impaired, failed to form tubular vacuoles and to polarly distribute the vacuole. In sgr2, large vacuoles occupied the apical tip and thus nuclear migration was blocked, resulting in a more symmetric zygotic division. We further observed that tubular vacuole formation and asymmetric vacuolar distribution both depended on the longitudinal array of actin filaments. Overall, our results show that vacuolar dynamics is crucial not only for the polar distribution along actin filaments but also for adequate nuclear positioning, and consequently zygote-division asymmetry.

  • Arabidopsis thaliana
  • zygote
  • vacuole
  • apical–basal axis
  • live-cell imaging

Footnotes

  • ↵1Y.K. and T.K. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: m-ueda{at}itbm.nagoya-u.ac.jp.
  • Author contributions: Y.K., T.K., D.K., M.T.M., S.H., T. Higashiyama, M.T., and M.U. designed research; Y.K., T.K., T.Y., S.S., and M.U. performed research; Y.K., T. Higaki, and M.U. analyzed data; and Y.K., T. Higaki, D.K., M.T.M., M.M., and M.U. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1814160116/-/DCSupplemental.

Published under the PNAS license.

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Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes
Yusuke Kimata, Takehide Kato, Takumi Higaki, Daisuke Kurihara, Tomomi Yamada, Shoji Segami, Miyo Terao Morita, Masayoshi Maeshima, Seiichiro Hasezawa, Tetsuya Higashiyama, Masao Tasaka, Minako Ueda
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2338-2343; DOI: 10.1073/pnas.1814160116

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Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes
Yusuke Kimata, Takehide Kato, Takumi Higaki, Daisuke Kurihara, Tomomi Yamada, Shoji Segami, Miyo Terao Morita, Masayoshi Maeshima, Seiichiro Hasezawa, Tetsuya Higashiyama, Masao Tasaka, Minako Ueda
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2338-2343; DOI: 10.1073/pnas.1814160116
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