Wortmannin-induced vacuole fusion enhances amyloplast dynamics in Arabidopsis zigzag1 hypocotyls

J Exp Bot. 2016 Dec;67(22):6459-6472. doi: 10.1093/jxb/erw418. Epub 2016 Nov 5.

Abstract

Gravitropism in Arabidopsis shoots depends on the sedimentation of amyloplasts in the endodermis, and a complex interplay between the vacuole and F-actin. Gravity response is inhibited in zigzag-1 (zig-1), a mutant allele of VTI11, which encodes a SNARE protein involved in vacuole fusion. zig-1 seedlings have fragmented vacuoles that fuse after treatment with wortmannin, an inhibitor of phosphatidylinositol 3-kinase, and underscore a role of phosphoinositides in vacuole fusion. Using live-cell imaging with a vertical stage microscope, we determined that young endodermal cells below the apical hook that are smaller than 70 μm in length are the graviperceptive cells in dark-grown hypocotyls. This result was confirmed by local wortmannin application to the top of zig-1 hypocotyls, which enhanced shoot gravitropism in zig-1 mutants. Live-cell imaging of zig-1 hypocotyl endodermal cells indicated that amyloplasts are trapped between juxtaposed vacuoles and their movement is severely restricted. Wortmannin-induced fusion of vacuoles in zig-1 seedlings increased the formation of transvacuolar strands, enhanced amyloplast sedimentation and partially suppressed the agravitropic phenotype of zig-1 seedlings. Hypergravity conditions at 10 g were not sufficient to displace amyloplasts in zig-1, suggesting the existence of a physical tether between the vacuole and amyloplasts. Our results overall suggest that vacuole membrane remodeling may be involved in regulating the association of vacuoles and amyloplasts during graviperception.

Keywords: Amyloplasts; SNARE; cytoskeleton; gravitropism; vacuole; wortmannin..

MeSH terms

  • Androstadienes / pharmacology*
  • Arabidopsis / drug effects
  • Arabidopsis / growth & development*
  • Arabidopsis / ultrastructure
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / physiology
  • Gravitropism / drug effects
  • Gravitropism / physiology
  • Hypocotyl / drug effects
  • Hypocotyl / growth & development
  • Microscopy
  • Qb-SNARE Proteins / genetics*
  • Qb-SNARE Proteins / physiology
  • Vacuoles / drug effects*
  • Vacuoles / physiology
  • Vacuoles / ultrastructure
  • Wortmannin

Substances

  • Androstadienes
  • Arabidopsis Proteins
  • Qb-SNARE Proteins
  • vesicle transport v-SNARE 11 protein, Arabidopsis
  • Wortmannin