TRM4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA3

New Phytol. 2019 Jan;221(2):881-895. doi: 10.1111/nph.15442. Epub 2018 Sep 13.

Abstract

The differentiation of the seed coat epidermal (SCE) cells in Arabidopsis thaliana leads to the production of a large amount of pectin-rich mucilage and a thick cellulosic secondary cell wall. The mechanisms by which cortical microtubules are involved in the formation of these pectinaceous and cellulosic cell walls are still largely unknown. Using a reverse genetic approach, we found that TONNEAU1 (TON1) recruiting motif 4 (TRM4) is implicated in cortical microtubule organization in SCE cells, and functions as a novel player in the establishment of mucilage structure. TRM4 is preferentially accumulated in the SCE cells at the stage of mucilage biosynthesis. The loss of TRM4 results in compact seed mucilage capsules, aberrant mucilage cellulosic structure, short cellulosic rays and disorganized cellulose microfibrils in mucilage. The defects could be rescued by transgene complementation of trm4 alleles. Probably, this is a consequence of a disrupted organization of cortical microtubules, observed using fluorescently tagged tubulin proteins in trm4 SCE cells. Furthermore, TRM4 proteins co-aligned with microtubules and interacted directly with CELLULOSE SYNTHASE 3 in two independent assays. Together, the results indicate that TRM4 is essential for microtubule array organization and therefore correct cellulose orientation in the SCE cells, as well as the establishment of the subsequent mucilage architecture.

Keywords: Arabidopsis; TONNEAU1 recruiting motif (TRM); cellulose deposition; cellulose synthase (CESA); microtubule organization; mucilage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis / ultrastructure
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Wall / metabolism
  • Cell Wall / ultrastructure
  • Cellulose / metabolism*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism*
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism*
  • Microtubules / metabolism
  • Microtubules / ultrastructure
  • Pectins / metabolism
  • Plant Mucilage / metabolism
  • Seeds / genetics
  • Seeds / physiology
  • Seeds / ultrastructure

Substances

  • AT1G74160 protein, Arabidopsis
  • Arabidopsis Proteins
  • Microtubule-Associated Proteins
  • Plant Mucilage
  • Pectins
  • Cellulose
  • At5g05170 protein, Arabidopsis
  • Glucosyltransferases