Arabidopsis class I formins control membrane-originated actin polymerization at pollen tube tips

PLoS Genet. 2018 Nov 12;14(11):e1007789. doi: 10.1371/journal.pgen.1007789. eCollection 2018 Nov.

Abstract

A population of dynamic apical actin filaments is required for rapid polarized pollen tube growth. However, the cellular mechanisms driving their assembly remain incompletely understood. It was postulated that formin is a major player in nucleating apical actin assembly, but direct genetic and cytological evidence remains to be firmly established. Here we found that both Arabidopsis formin 3 (AtFH3) and formin 5 (AtFH5) are involved in the regulation of apical actin polymerization and actin array construction in pollen tubes, with AtFH3 playing a more dominant role. We found that both formins have plasma membrane (PM) localization signals but exhibit distinct PM localization patterns in the pollen tube, and loss of their function reduces the amount of apical actin filaments. Live-cell imaging revealed that the reduction in filamentous actin is very likely due to the decrease in filament elongation. Furthermore, we found that the rate of tip-directed vesicle transport is reduced and the pattern of apical vesicle accumulation is altered in formin loss-of-function mutant pollen tubes, which explains to some extent the reduction in pollen tube elongation. Thus, we provide direct genetic and cytological evidence showing that formin is an important player in nucleating actin assembly from the PM at pollen tube tips.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / chemistry
  • Actin Cytoskeleton / metabolism
  • Actins / chemistry
  • Actins / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Genes, Plant
  • Mutagenesis, Insertional
  • Plants, Genetically Modified
  • Pollen Tube / genetics
  • Pollen Tube / growth & development*
  • Pollen Tube / metabolism*
  • Polymerization
  • Protein Multimerization

Substances

  • Actins
  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • FH5 protein, Arabidopsis

Grants and funding

This work was supported by grants from National Natural Science Foundation of China (31471266 and 31671390). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.