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Edited by Tetsuya Higashiyama, Nagoya University, Nagoya, Japan, and accepted by Editorial Board Member June B. Nasrallah November 9, 2020 (received for review July 23, 2020)
Significance
Flowering plants have evolved a unique double-fertilization process along with an actin filament (F-actin)-based gamete nuclear migration mechanism. However, how dynamic F-actin movement is controlled in the female gametophytic cells remains unclear. We identified that the movement of F-actin is promoted via an ARP2/3-independent WAVE/SCAR-signaling pathway. We also discovered that the plant class XI myosin XI-G has a function involved in the active movement of F-actin required for sperm nuclear migration, which is different from the canonical myosin function as a cargo transporter. These breakthroughs also provide us with opportunities to further understand how flowering plants control double fertilization and plant cytoskeleton dynamics.
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.
Footnotes
- ↵1To whom correspondence may be addressed. Email: tomo.k{at}uky.edu.
Author contributions: M.F.A., X.P., M.-X.S., and T.K. designed research; M.F.A., U.F., X.P., and S.W.H. performed research; D.M. contributed new reagents/analytic tools; M.F.A. and T.K. analyzed data; and M.F.A. and T.K. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission. T.H. is a guest editor invited by the Editorial Board.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2015550117/-/DCSupplemental.
Data Availability.
All study data are included in the article and supporting information.
Published under the PNAS license.
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ARP2/3-independent WAVE/SCAR pathway and class XI myosin control sperm nuclear migration in flowering plants
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- Plant Biology
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