F-actin regulates the polarized secretion of pollen tube attractants in Arabidopsis synergid cells

Daichi Susaki, Rie Izumi, Takao Oi, Hidenori Takeuchi, Ji Min Shin, Naoya Sugi, Tetsu Kinoshita, Tetsuya Higashiyama, Tomokazu Kawashima, Daisuke Maruyama

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

Abstract

Pollen tube attraction is a key event of sexual reproduction in flowering plants. In the ovule, two synergid cells neighboring the egg cell control pollen tube arrival via the active secretion of attractant peptides such as AtLURE1 and XIUQIU from the filiform apparatus (FA) facing toward the micropyle. Distinctive cell polarity together with longitudinal F-actin and microtubules are hallmarks of the synergid cell in various species, though the functions of these cellular structures are unclear. In this study, we used genetic and pharmacological approaches to indicate the roles of cytoskeletal components in FA formation and pollen tube guidance in Arabidopsis thaliana. Genetic inhibition of microtubule formation reduced invaginations of the plasma membrane but did not abolish micropylar AtLURE1.2 accumulation. By contrast, the expression of a dominant-negative form of ACTIN8 induced disorganization of the FA and loss of polar AtLURE1.2 distribution toward the FA. Interestingly, after pollen tube reception, F-actin became unclear for a few hours in the persistent synergid cell, which may be involved in pausing and resuming pollen tube attraction during early polytubey block. Our data suggest that F-actin plays a central role in maintaining cell polarity and in mediating male-female communication in the synergid cell.

Original languageEnglish
Pages (from-to)1222-1240
Number of pages19
JournalPlant Cell
Volume35
Issue number4
DOIs
StatePublished - Apr 2023

Bibliographical note

Publisher Copyright:
© 2022 American Society of Plant Biologists. All rights reserved.

Funding

This work was supported by TOYOAKI Scholarship Foundation, Japan Society for the Promotion of Science (JSPS) KAKENHI [Grant Numbers: JP17H05846, JP19H04869, JP20H03280, JP20H05778 and JP20H05781 to D.M.; JP19K16172 and JP22K15145 to D.S.; JP18K14729 and JP20K15817 to H.T.; JP22H05172 and JP22H05175 to T.Ki], by the Grant for academic research from Yokohama City University (to D.M.), by the grant for 2016–2022 Research Development Fund of Yokohama City University (to D.M.), and by National Science Foundation Grant IOS-1928836 (to T.Ka.). FIB-SEM observation was supported by the Nagoya University microstructural characterization platform as a program of “Nanotechnology Platform” of the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, and we especially thank S. Arai and S. Enomoto (Nagoya Univ.) for technical support. We acknowledge B. Raj Thapa (Univ. of Kentucky) for supporting on the F-actin movement quantification, M. Tsukatani for assistance in image analysis, H. Ikeda for assistance in preparing materials, D. Kurihara (Nagoya Univ.), S. Nishikawa (Niigata Univ.), and T. Nakagawa (Shimane Univ.) for providing plasmids. We would like to thank Editage ( www.editage.com ) for English language editing.

FundersFunder number
TOYOAKI Scholarship Foundation
Yokohama City University
Nagoya University
2022 Research Development Fund of Yokohama City University
Ministry of Education, Culture, Sports, Science and Technology
National Science Foundation Arctic Social Science ProgramIOS-1928836
Japan Society for the Promotion of Science19K16172, JP22H05175, JP20H05778, JP18K14729, JP20K15817, JP20H05781, JP22H05172, JP19H04869, JP17H05846, JP20H03280, JP22K15145

    ASJC Scopus subject areas

    • Plant Science

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