ARP2/3-independent WAVE/SCAR pathway and class XI myosin control sperm nuclear migration in flowering plants

Mohammad Foteh Ali, Umma Fatema, Xiongbo Peng, Samuel W. Hacker, Daisuke Maruyama, Meng Xiang Sun, Tomokazu Kawashima

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

After eukaryotic fertilization, gamete nuclei migrate to fuse parental genomes in order to initiate development of the next generation. In most animals, microtubules control female and male pronuclear migration in the zygote. Flowering plants, on the other hand, have evolved actin filament (F-actin)-based sperm nuclear migration systems for karyogamy. Flowering plants have also evolved a unique double-fertilization process: two female gametophytic cells, the egg and central cells, are each fertilized by a sperm cell. The molecular and cellular mechanisms of how flowering plants utilize and control F-actin for double-fertilization events are largely unknown. Using confocal microscopy live-cell imaging with a combination of pharmacological and genetic approaches, we identified factors involved in F-actin dynamics and sperm nuclear migration in Arabidopsis thaliana (Arabidopsis) and Nicotiana tabacum (tobacco). We demonstrate that the F-actin regulator, SCAR2, but not the ARP2/3 protein complex, controls the coordinated active F-actin movement. These results imply that an ARP2/3-independent WAVE/SCAR-signaling pathway regulates F-actin dynamics in female gametophytic cells for fertilization. We also identify that the class XI myosin XI-G controls active F-actin movement in the Arabidopsis central cell. XI-G is not a simple transporter, moving cargos along F-actin, but can generate forces that control the dynamic movement of F-actin for fertilization. Our results provide insights into the mechanisms that control gamete nuclear migration and reveal regulatory pathways for dynamic F-actin movement in flowering plants.

Original languageEnglish
Pages (from-to)32757-32763
Number of pages7
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number51
DOIs
StatePublished - Dec 22 2020

Bibliographical note

Funding Information:
supported by a start-up fund from the Department of Plant and Soil Sciences and the College of Agriculture, Food and Environment, University of Kentucky.

Funding Information:
We thank Drs. Robert B. Goldberg and Anthony Clark for their critical comments on this manuscript; Dr. Yukinosuke Ohnishi for image processing; and Dr. Daniel B. Szymanski (Purdue University) for dis2-1 and arpc4-t2 seeds. This work was supported by NSF Grant IOS- 1928836 (to T.K.); National Institute of Food and Agriculture, US Department of Agriculture Hatch Program Grant 1014280 (to T.K.); the National Natural Science Foundation of China Grants 31570317 and 31270362 (to X.P. and M.-X.S.); and the Ministry of Education, Culture, Sports, Science and Technology of Japan Grants-in-Aid for Scientific Research on Innovative Areas Grants 17H05846 and 19H04869 (to D.M.). M.F.A., U.F., and T.K. were supported by a start-up fund from the Department of Plant and Soil Sciences and the College of Agriculture, Food and Environment, University of Kentucky.

Funding Information:
M.-X.S.); and the Ministry of Education, Culture, Sports, Science and Technology of Japan Grants-in-Aid for Scientific Research on Innovative Areas Grants 17H05846 and 19H04869 (to D.M.). M.F.A., U.F., and T.K. were

Funding Information:
ACKNOWLEDGMENTS. We thank Drs. Robert B. Goldberg and Anthony Clark for their critical comments on this manuscript; Dr. Yukinosuke Ohnishi for image processing; and Dr. Daniel B. Szymanski (Purdue University) for dis2-1 and arpc4-t2 seeds. This work was supported by NSF Grant IOS-1928836 (to T.K.); National Institute of Food and Agriculture, US Department of Agriculture Hatch Program Grant 1014280 (to T.K.); the National Natural Science Foundation of China Grants 31570317 and 31270362 (to X.P. and

Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.

Keywords

  • F-actin
  • Fertilization
  • Myosin
  • Nuclear migration
  • WAVE/SCAR

ASJC Scopus subject areas

  • General

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