MicroRNA miR396 Regulates the Switch between Stem Cells and Transit-Amplifying Cells in Arabidopsis Roots

Abstract

To ensure an adequate organ mass, the daughters of stem cells progress through a transit-amplifying phase displaying rapid cell division cycles before differentiating. Here, we show that Arabidopsis thaliana microRNA miR396 regulates the transition of root stem cells into transit-amplifying cells by interacting with GROWTH-REGULATING FACTORs (GRFs). The GRFs are expressed in transit-amplifying cells but are excluded from the stem cells through inhibition by miR396. Inactivation of the GRFs increases the meristem size and induces periclinal formative divisions in transit-amplifying cells. The GRFs repress PLETHORA (PLT) genes, regulating their spatial expression gradient. Conversely, PLT activates MIR396 in the stem cells to repress the GRFs. We identified a pathway regulated by GRF transcription factors that represses stem cell-promoting genes in actively proliferating cells, which is essential for the progression of the cell cycle and the orientation of the cell division plane. If unchecked, the expression of the GRFs in the stem cell niche suppresses formative cell divisions and distorts the organization of the quiescent center. We propose that the interactions identified here between miR396 and GRF and PLT transcription factors are necessary to establish the boundary between the stem cell niche and the transit-amplifying region.

The PLETHORA Gene Regulatory Network Guides Growth and Cell Differentiation in Arabidopsis Roots

“…How are these feed-forward loops kept in check? A possible mechanism may be provided by GRF corepressors that were recently shown to control PLT levels in the root (Rodriguez et al, 2015). Here, we find that GRF2 is regulated by PLTs and bound by PLT2, suggesting a negative feedback loop for the stabilization of PLT levels.…”

“…During growth, cells undergo transitions from division toward expansion and differentiation in distinct developmental zones and interactions between plant growth factors of the auxin and cytokinin classes play an important role in this process (Heidstra and Sabatini, 2014). In addition, root meristem growth factor (RGF) peptides and their receptors (RGFRs) as well as nuclear GROWTH-REGULATING FACTOR (GRF) corepressor proteins regulate meristematic activity by influencing the activity of PLETHORA (PLT) proteins (Matsuzaki et al, 2010;Rodriguez et al, 2015;Ou et al, 2016;Shinohara et al, 2016).…”

Transcriptome Profiling of Wheat Inflorescence Development from Spikelet Initiation to Floral Patterning Identified Stage-Specific Regulatory Genes

“…These highly expressed miRNAs were of particular interest because, in Arabidopsis, miR159, miR167, and miR319 and their targets form a regulatory circuit during floral organ patterning (Rubio-Somoza and Weigel, 2013). Moreover, the miR319-TCP module directly regulates miR396 expression, which in turn represses a number of growthregulating factors (GRFs), while GRFs may repress meristem cell-promoting genes in actively proliferating cells (Schommer et al, 2014;Rodriguez et al, 2015). In wheat, the high expression levels of miR159b and miR319b were sharply down-regulated from DR to TS, while miR396e remained low in the first three stages and was significantly increased (.50-fold) in TS ( Fig.…”

A Case for Distributed Control of Local Stem Cell Behavior in Plants

“…For example, a small family of R OOT G ROWTH F ACTORS ( RGF s), which are expressed in the QC and columella, have been shown to diffuse into the proximal meristem and positively regulate growth (Matsuzaki et al, 2010; Zhou et al, 2010). In addition, it was shown recently that microRNA396 , which is transcribed in the QC and columella, non-cell autonomously represses redundant G ROWTH R EGULATING F ACTOR s ( GRF s), which are localized exclusively in the proximal meristem and were shown to have a role in locally promoting division rates (Rodriguez et al, 2015; Wang et al, 2011). Both factors have been implicated in the regulation of the PL E T HORA ( PLT ) gene family (Matsuzaki et al, 2010; Wang et al, 2011), which regulates division rates and maturation state throughout the meristem (Aida et al, 2004; Galinha et al, 2007).…”