Stem integrity in Arabidopsis thaliana requires a load-bearing epidermis

Development. 2021 Feb 26;148(4):dev198028. doi: 10.1242/dev.198028.

Abstract

Because plant cells are glued to each other via their cell walls, failure to coordinate growth among adjacent cells can create cracks in tissues. Here, we find that the unbalanced growth of inner and outer tissues in the clavata3 de-etiolated3 (clv3 det3) mutant of Arabidopsis thaliana stretched epidermal cells, ultimately generating cracks in stems. Stem growth slowed before cracks appeared along clv3 det3 stems, whereas inner pith cells became drastically distorted and accelerated their growth, yielding to stress, after the appearance of cracks. This is consistent with a key role of the epidermis in restricting growth. Mechanical property measurements recorded using an atomic force microscope revealed that epidermal cell wall stiffness decreased in det3 and clv3 det3 epidermises. Thus, we hypothesized that stem integrity depends on the epidermal resistance to mechanical stress. To formally test this hypothesis, we used the DET3 gene as part of a tissue-specific strategy to complement cell expansion defects. Epidermis-driven DET3 expression restored growth and restored the frequency of stem cracking to 20% of the clv3 det3 mutant, demonstrating the DET3-dependent load-bearing role of the epidermis.

Keywords: Arabidopsis thaliana; Cell wall stiffness; Epidermis; Mechanical confliction; Stem cracking; clv3 det3 mutant.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Differentiation
  • Cell Wall / metabolism
  • Epidermal Cells / cytology
  • Epidermal Cells / metabolism*
  • Epidermis / metabolism*
  • Gene Expression Regulation, Plant
  • Plant Stems / cytology
  • Plants, Genetically Modified
  • Vacuolar Proton-Translocating ATPases / genetics
  • Vacuolar Proton-Translocating ATPases / metabolism
  • Weight-Bearing / physiology*

Substances

  • AT2G27250 protein, Arabidopsis
  • Arabidopsis Proteins
  • Det3 protein, Arabidopsis
  • Vacuolar Proton-Translocating ATPases