Mechanisms Regulating SHORT-ROOT Intercellular Movement

Abstract

Signaling centers within developing organs regulate morphogenesis in both plants and animals. The putative transcription factor SHORT-ROOT (SHR) is an organizing signal regulating the division of specific stem cells in the Arabidopsis root. Comparison of gene transcription with protein localization indicates that SHR moves in a highly specific manner from the cells of the stele in which it is synthesized outward. Here, we provide evidence that SHR intercellular trafficking is both regulated and targeted. First, we show that subcellular localization of SHR in the stele is intrinsic to the SHR protein. Next, we show that SHR must be present in the cytoplasm to move, providing evidence that SHR movement is regulated. Finally, we describe an informative new shr allele, in which the protein is present in the cytoplasm yet does not move. Thus, in contrast to proteins that move by a process resembling diffusion, a cytoplasmic pool of SHR is not sufficient for movement.

Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification

“…As JKD and BIB form nuclear complexes with both SCR and SHR, it is plausible that BIRD proteins and SCR cooperate in the endodermis to prevent movement of SHR beyond one cell layer, in agreement with previously described data on the role of SCR (Gallagher et al, 2004;Cui et al, 2007;Koizumi et al, 2012).…”

“…Intercellular signaling through mobile transcriptional regulators has been shown to be essential for plant growth and development (Lucas et al, 1995;Nakajima et al, 2001;Kim et al, 2003;Kurata et al, 2005;Gallagher and Benfey, 2009). In the Arabidopsis thaliana root meristem, the cell fate determinant SHORT-ROOT (SHR) is produced in the stele and moves one cell layer outward to instruct ground tissue development Nakajima et al, 2001;Sena et al, 2004;Gallagher et al, 2004;Gallagher and Benfey, 2009). After movement from the stele, SHR binds to its target SCR (SCARECROW) and promotes the asymmetric cell division (ACD) of the cortex-endodermis initial/daughter (CEI/CEID) as a bipartite SCR-SHR complex to generate the ground tissue (GT) consisting of two layers: cortex and endodermis (Di Laurenzio et al, 1996;Helariutta et al, 2000;Cui et al, 2007).…”

“…In addition, callose accumulation at plasmodesmata, symplastic channels that allow passage of hormones, proteins, and RNAs (Du et al, 2007;Schlereth et al, 2010;Matsuzaki et al, 2010), results in plasmodesmata closure and reduces SHR intercellular trafficking (Vatén et al, 2011). Furthermore, nuclear targeting of SHR by fusing a nuclear localization signal or by expressing SCR in the vasculature blocks SHR movement (Gallagher et al, 2004;Koizumi et al, 2012), suggesting that nuclear retention determines the range of SHR movement. Finally, JACKDAW (JKD) was identified as a factor that constrains SHR movement to a single cell layer and regulates the action range of SHR and SCR, while the JKD homolog MAGPIE (MGP) promotes SHR-dependent ACD (Welch et al, 2007).…”

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

“…The SHR pathway has been characterized primarily in Arabidopsis, where a single gene encodes a mobile protein that moves outward from its expression domain in the vasculature to specify cell fate in surrounding cell layers Nakajima et al, 2001;Gallagher et al, 2004;Levesque et al, 2006;Cui et al, 2007). Phylogenetic analysis revealed that the presence of a single SHR gene is typical of eudicot genomes, except where within-species genome duplications have occurred (Fig.…”

SEUSS Integrates Gibberellin Signaling with Transcriptional Inputs from the SHR-SCR-SCL3 Module to Regulate Middle Cortex Formation in the Arabidopsis Root

“…SHR is transcribed in the vascular tissue and the pericycle, collectively known as the stele. SHR protein, which localizes to the cytoplasm and the nucleus in the stele, is able to move from the cytoplasm of the stele cells to the adjacent SCRexpressing layer (Nakajima et al, 2001;Gallagher et al, 2004), including stem cells of the cortex/endodermis, their daughter cells, the endodermis, and the quiescent center. SHR protein becomes exclusively localized to the nucleus in cells of the SCR-expressing layer, where SHR directly up-regulates SCR to limit its own movement via SCR-dependent nuclear sequestration, thereby preventing its further movement into the cortex and maintaining its levels in the endodermis (Cui et al, 2007;Koizumi et al, 2012a).…”