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

  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.

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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