Abstract

The root stem cell niche, which in the Arabidopsis thaliana root meristem is an area of four mitotically inactive quiescent cells (QCs) and the surrounding mitotically active stem cells, is critical for root development and growth. We report here that during jasmonate-induced inhibition of primary root growth, jasmonate reduces root meristem activity and leads to irregular QC division and columella stem cell differentiation. Consistently, jasmonate reduces the expression levels of the AP2-domain transcription factors PLETHORA1 (PLT1) and PLT2, which form a developmentally instructive protein gradient and mediate auxin-induced regulation of stem cell niche maintenance. Not surprisingly, the effects of jasmonate on root stem cell niche maintenance and PLT expression require the functioning of MYC2/JASMONATE INSENSITIVE1, a basic helix-loop-helix transcription factor that involves versatile aspects of jasmonate-regulated gene expression. Gel shift and chromatin immunoprecipitation experiments reveal that MYC2 directly binds the promoters of PLT1 and PLT2 and represses their expression. We propose that MYC2-mediated repression of PLT expression integrates jasmonate action into the auxin pathway in regulating root meristem activity and stem cell niche maintenance. This study illustrates a molecular framework for jasmonate-induced inhibition of root growth through interaction with the growth regulator auxin.

Highlights

  • Postembryonic root growth of higher plants is maintained by the root meristem, in which stem cells, including the mitotically inactive quiescent center (QC) and its surrounding stem cells, reside in a specialized microenvironment called the stem cell niche (Dolan et al, 1993; Watt and Hogan, 2000; Weigel and Jurgens, 2002; Laux, 2003; Aida et al, 2004)

  • Root growth of wild-type plants was inhibited by jasmonic acid (JA) in a dose-dependent manner, while root growth of the JA-insensitive coi1-1 mutants was largely unaffected by JA (Figures 1A and 1B)

  • We investigated the JA-induced cellular changes in the three morphologically distinguishable developmental zones along the longitudinal axis of the root: the differentiation zone (DZ), the elongation zone (EZ), and the meristem zone (MZ)

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Summary

Introduction

Postembryonic root growth of higher plants is maintained by the root meristem, in which stem cells, including the mitotically inactive quiescent center (QC) and its surrounding stem cells, reside in a specialized microenvironment called the stem cell niche (Dolan et al, 1993; Watt and Hogan, 2000; Weigel and Jurgens, 2002; Laux, 2003; Aida et al, 2004). The whole process of root organogenesis, including initiation of the root pole (Friml et al, 2003), formation of the root stem cell niche (Sabatini et al, 1999; Blilou et al, 2005), maintenance of mitotic activity of the root meristem (Beemster and Baskin, 2000; Dello Ioio et al, 2007; Stepanova et al, 2008), and elongation and differentiation of cells leaving the root meristem (Rahman et al, 2007), has been demonstrated to be under the control of auxin, especially its featured gradient distribution (Tanaka et al, 2006; Benkovaand Hejatko, 2009; Petrasek and Friml, 2009). The auxin-inducible PLETHORA (PLT) genes, which encode the AP2 class of transcription factors that are essential for root stem cell niche patterning (Aida et al, 2004; Galinha et al, 2007), are good candidates for performing this translation

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