The lncRNA APOLO and the transcription factor WRKY42 target common cell wall EXTENSIN encoding genes to trigger root hair cell elongation

Plant Signal Behav. 2021 Aug 3;16(8):1920191. doi: 10.1080/15592324.2021.1920191. Epub 2021 May 4.

Abstract

Plant long noncoding RNAs (lncRNAs) are key chromatin dynamics regulators, directing the transcriptional programs driving a wide variety of developmental outputs. Recently, we uncovered how the lncRNA AUXIN REGULATED PROMOTER LOOP (APOLO) directly recognizes the locus encoding the root hair (RH) master regulator ROOT HAIR DEFECTIVE 6 (RHD6) modulating its transcriptional activation and leading to low temperature-induced RH elongation. We further demonstrated that APOLO interacts with the transcription factor WRKY42 in a novel ribonucleoprotein complex shaping RHD6 epigenetic environment and integrating signals governing RH growth and development. In this work, we expand this model showing that APOLO is able to bind and positively control the expression of several cell wall EXTENSIN (EXT) encoding genes, including EXT3, a key regulator for RH growth. Interestingly, EXT3 emerged as a novel common target of APOLO and WRKY42. Furthermore, we showed that the ROS homeostasis-related gene NADPH OXIDASE C (NOXC) is deregulated upon APOLO overexpression, likely through the RHD6-RSL4 pathway, and that NOXC is required for low temperature-dependent enhancement of RH growth. Collectively, our results uncover an intricate regulatory network involving the APOLO/WRKY42 hub in the control of master and effector genes during RH development.

Keywords: APOLO; EXTENSINs; NADPH oxidase C (NOXC); RHD6; Root hairs; WRKY42; long noncoding RNAS; low temperature.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Differentiation
  • Cell Proliferation
  • Cell Wall*
  • Chromatin / metabolism
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Glycoproteins / genetics
  • Glycoproteins / metabolism
  • Indoleacetic Acids / metabolism*
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • Plant Development / genetics
  • Plant Roots / growth & development*
  • Plant Roots / metabolism
  • Promoter Regions, Genetic
  • RNA, Long Noncoding / metabolism*
  • Transcription Factors / metabolism*

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • Chromatin
  • EXT3 protein, Arabidopsis
  • Glycoproteins
  • Indoleacetic Acids
  • RHD6 protein, Arabidopsis
  • RNA, Long Noncoding
  • RSL4 protein, Arabidopsis
  • Transcription Factors
  • WRKY42 protein, Arabidopsis
  • NADPH Oxidases

Grants and funding

This work was supported by grants from ANPCyT (PICT2016 [0132] and PICT2017 [0066]), Instituto Milenio iBio – Iniciativa Científica Milenio, MINECON and Fondo Nacional de Desarrollo Científico y Tecnológico [1200010] to JME; ANPCyT (PICT2016 [0007] and [0289]) and Fima Leloir Award to FA; UNL [CAI+D 2016] to LL; LL, FI, JME and FA are researchers of CONICET; JMP, MM, and VBG are fellows of the same institution. NM is a fellow of ANPCyT.