A PHABULOSA-Controlled Genetic Pathway Regulates Ground Tissue Patterning in the Arabidopsis Root

Curr Biol. 2021 Jan 25;31(2):420-426.e6. doi: 10.1016/j.cub.2020.10.038. Epub 2020 Nov 10.

Abstract

In both animals and plants, development involves anatomical modifications. In the root of Arabidopsis thaliana, maturation of the ground tissue (GT)-a tissue comprising all cells between epidermal and vascular ones-is a paradigmatic example of these modifications, as it generates an additional tissue layer, the middle cortex (MC).1-4 In early post-embryonic phases, the Arabidopsis root GT is composed of one layer of endodermis and one of cortex. A second cortex layer, the MC, is generated by asymmetric cell divisions in about 80% of Arabidopsis primary roots, in a time window spanning from 7 to 14 days post-germination (dpg). The cell cycle regulator CYCLIN D6;1 (CYCD6;1) plays a central role in this process, as its accumulation in the endodermis triggers the formation of MC.5 The phytohormone gibberellin (GA) is a key regulator of the timing of MC formation, as alterations in its signaling and homeostasis result in precocious endodermal asymmetric cell divisions.3,6,7 However, little is known on how GAs are regulated during GT maturation. Here, we show that the HOMEODOMAIN LEUCINE ZIPPER III (HD-ZIPIII) transcription factor PHABULOSA (PHB) is a master regulator of MC formation, controlling the accumulation of CYCD6;1 in the endodermis in a cell non-autonomous manner. We show that PHB activates the GA catabolic gene GIBBERELLIN 2 OXIDASE 2 (GA2ox2) in the vascular tissue, thus regulating the stability of the DELLA protein GIBBERELLIN INSENSITIVE (GAI)-a GA signaling repressor-in the root and, hence, CYCD6;1 expression in the endodermis.

Keywords: CYCD6;1; cyclin D6;1; gibberellin; ground tissue; homeodomain leucin zipper III; microRNA; middle cortex; root development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism*
  • Asymmetric Cell Division / genetics
  • Cyclins / genetics*
  • Gene Expression Regulation, Developmental*
  • Gene Expression Regulation, Plant*
  • Gibberellins / metabolism
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • MicroRNAs / metabolism
  • Mixed Function Oxygenases / genetics
  • Plant Roots / growth & development
  • Plants, Genetically Modified

Substances

  • Arabidopsis Proteins
  • CYCD6;1 protein, Arabidopsis
  • Cyclins
  • Gibberellins
  • Homeodomain Proteins
  • MicroRNAs
  • PHB protein, Arabidopsis
  • Mixed Function Oxygenases
  • gibberellin 2-dioxygenase