Root layers: complex regulation of developmental patterning

Developmental patterning events involve cell fate specification and maintenance processes in diverse, multicellular organisms. The simple arrangement of tissue layers in the Arabidopsis thaliana root provides a highly tractable system for the study of these processes. This review highlights recent work addressing the patterning of root tissues focusing on the factors involved and their complex regulation. In the past two years studies of root patterning have indicated that chromatin remodeling, protein movement, transcriptional networks, and an auxin gradient, all contribute to the complexity inherent in developmental patterning events within the root. As a result, future research advances in this field will require tissue-specific information at both the single gene and global level.

Introduction

Over the past two decades studies of primary root patterning in Arabidopsis thaliana initiated using classical genetic approaches were extended to the molecular level by the advent of molecular biology techniques, and then were propelled into the genomics era with the sequencing of the Arabidopsis genome. These approaches have led to substantial insights into cell fate specification and the positioning of the stem cell niche within the root. The simplicity and transparency of the Arabidopsis are the keys that have unlocked these discoveries. The Arabidopsis primary root is composed of concentric rings of tissue layers along the radial axis and morphologically distinguishable developmental zones along the longitudinal axis.

Specifically, from the root tip to the junction between the root and the stem exist distinct zones that are visible as regions of small, actively dividing cells (called meristematic cells), elongated cells, and terminally differentiated cells marked by the root hairs of the epidermis (Figure 1, Figure 3). As such, the position of each cell along this axis can be used to infer its developmental age.

The root has an outer layer of epidermis and an inner core of vascular tissue that is spatially separated by a layer of ground tissue (Figure 2a). This elegant radial organization is derived from asymmetric cell divisions of stem cell initials and the daughter cells they produce. For instance, the ground tissue is generated from asymmetric division of the cortex–endodermal initial cell (CEI) to renew itself and produce a daughter cell (CED) that subsequently divides to generate the endodermal and cortex cell lineages [1^•].

A small population of cells that rarely divides, called the quiescent center (QC), is surrounded by undifferentiated stem cells, such as the CEI, from which the different tissue layers arise. Analogous to animal systems, the QC and stem cells of the Arabidopsis root, together termed the plant stem cell niche, possess the ability to renew themselves and are essentially ageless unlike the daughter cells they produce [2, 3]. Since plants are immobile, this pattern is not achieved by cell migration as it is in many animals, but rather specified by positional information exchanged between cells [1^•].

In the past two years, microarray profiling of these cell populations comprising the QC, root cell layers, and longitudinal zones, termed the ‘root map’, has resulted in abundant gene expression information in both space and time with resolution unprecedented in any other multicellular organism [4^•]. Modeling of the localization and directional activity of the PINFORMED1 (PIN) proteins that transport auxin has unveiled an auxin gradient robust to perturbations in auxin concentrations [5^••]. Remarkably, the PLETHORA (PLT) transcription factors are expressed in graded patterns resembling this auxin gradient and, when mutated, shift the boundaries between zones along the longitudinal axis [6^•].

By contrast, along the radial axis the GRAS family transcription factor SHORTROOT (SHR) has been demonstrated to specify a single layer of endodermis within the ground tissue via its movement from the central vascular tissue into neighboring cells where its interaction with a transcription factor of the same family, SCARECROW (SCR), leads to its sequestration into the nucleus. Once in the nucleus, SHR is restricted from moving to outer cell layers and specifies this single layer of endodermis by regulating a number of transcription factors, including SCR that in turn positively regulates itself [7^••]. This is just one example of a tightly controlled, complex regulatory process embedded in the beguilingly simple patterning of the root. A direct link was also recently demonstrated between chromatin remodeling of the upstream region of the HDZIP transcription factor GLABRA2 (GL2) by the GL2 modulator (GEM) and epidermal patterning [8^••]. This review focuses on these landmarks in root patterning research in relation to other findings over the past two years in a framework of the root's tissue layers and their underlying complexity at the molecular level.