A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells

Nat Plants. 2019 Jan;5(1):95-105. doi: 10.1038/s41477-018-0328-1. Epub 2018 Dec 17.

Abstract

Plant vacuoles are dynamic organelles that play essential roles in regulating growth and development. Two distinct models of vacuole biogenesis have been proposed: separate vacuoles are formed by the fusion of endosomes, or the single interconnected vacuole is derived from the endoplasmic reticulum. These two models are based on studies of two-dimensional (2D) transmission electron microscopy and 3D confocal imaging, respectively. Here, we performed 3D electron tomography at nanometre resolution to illustrate vacuole biogenesis in Arabidopsis root cells. The whole-cell electron tomography analysis first identified unique small vacuoles (SVs; 400-1,000 nm in diameter) as nascent vacuoles in early developmental cortical cells. These SVs contained intraluminal vesicles and were mainly derived/matured from multivesicular body (MVB) fusion. The whole-cell vacuole models and statistical analysis on wild-type root cells of different vacuole developmental stages demonstrated that central vacuoles were derived from MVB-to-SV transition and subsequent fusions of SVs. Further electron tomography analysis on mutants defective in MVB formation/maturation or vacuole fusion demonstrated that central vacuole formation required functional MVBs and membrane fusion machineries.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Fusion
  • Electron Microscope Tomography / methods*
  • Guanine Nucleotide Exchange Factors / genetics
  • Imaging, Three-Dimensional
  • Multivesicular Bodies / metabolism
  • Mutation
  • Plant Cells
  • Plant Roots / cytology*
  • Plants, Genetically Modified
  • SNARE Proteins / metabolism
  • Vacuoles / physiology*
  • Vesicular Transport Proteins / genetics

Substances

  • Arabidopsis Proteins
  • FREE1 protein, Arabidopsis
  • Guanine Nucleotide Exchange Factors
  • MON1 protein, Arabidopsis
  • SNARE Proteins
  • Vesicular Transport Proteins