Cytoskeleton Dynamics Control the First Asymmetric Cell Division in Arabidopsis Zygote


The asymmetric cell division of the zygote is the initial and crucial developmental step in most multicellular organisms. In flowering plants, whether zygote polarity is inherited from the preexisting organization in the egg cell or reestablished after fertilization has remained elusive. How dynamically the intracellular organization is generated during zygote polarization is also unknown. Here, we used a live-cell imaging system with Arabidopsis zygotes to visualize the dynamics of the major elements of the cytoskeleton, microtubules (MTs), and actin filaments (F-actins), during the entire process of zygote polarization. By combining image analysis and pharmacological experiments using specific inhibitors of the cytoskeleton, we found features related to zygote polarization. The preexisting alignment of MTs and F-actin in the egg cell is lost on fertilization. Then, MTs organize into a transverse ring defining the zygote subapical region and driving cell outgrowth in the apical direction. F-actin forms an apical cap and longitudinal arrays and is required to position the nucleus to the apical region of the zygote, setting the plane of the first asymmetrical division. Our findings show that, in flowering plants, the preexisting cytoskeletal patterns in the egg cell are lost on fertilization and that the zygote reorients the cytoskeletons to perform directional cell elongation and polar nuclear migration.

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Published in Proceedings of the National Academy of Sciences of the United States of America, v. 113, no. 49, p. 14157-14162.

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This work was supported by the Institute of Transformative Bio-Molecules of Nagoya University and the Japan Advanced Plant Science Network. This work was also supported by Japan Society for the Promotion of Science (JSPS) on Grant-in-Aid for Young Scientists A JP25711017 (to T. Higaki); Grants-in-Aid for Challenging Exploratory Research JP15K14542 (to Y.S.) and JP16K14753 (to M.U.); Grants-in-Aid for Scientific Research on Innovative Areas JP24114007 (to S.H.), JP16H06465 (to T. Higashiyama), JP16H06464 (to T. Higashiyama), JP16K21727 (to T. Higashiyama), JP24113514 (to M.U.), JP26113710 (to M.U.), JP15H05962 (to M.U.), and JP15H05955 (to M.U.); Grant-in-Aid for Scientific Research B JP16H04802 (to S.H.); Grants-in-Aid for Young Scientists B JP24770045 (to M.U.) and JP26840093 (to M.U.); and Japan Science and Technology Agency, Exploratory Research for Advanced Technology Grant JP25-J-J4216 (to M.U.). T.K. and F.B. were supported by the Gregor Mendel Institute and the European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) Grant 2163 B16 provided by the Austrian Science Fund (FWF).