Control of Arabidopsis root development

Abstract

The Arabidopsis root has been the subject of intense research over the past decades. This research has led to significantly improved understanding of the molecular mechanisms underlying root development. Key insights into the specification of individual cell types, cell patterning, growth and differentiation, branching of the primary root, and responses of the root to the environment have been achieved. Transcription factors and plant hormones play key regulatory roles. Recently, mechanisms involving protein movement and the oscillation of gene expression have also been uncovered. Root gene regulatory networks controlling root development have been reconstructed from genome-wide profiling experiments, revealing novel molecular connections and models. Future refinement of these models will lead to a more complete description of the complex molecular interactions that give rise to a simple growing root.

Figure 1

The making of an embryonic root: a schematic of early embryogenesis. (a) The 1–16-cell embryonic stages. WOX genes are expressed in differential and overlapping patterns that might regulate cell fate decisions, including the specification of apical-basal polarity at the 2-cell stage by WOX2 in the apical cell (yellow) and WOX8 and WOX9 in the basal cell (pink). Auxin also establishes this polarity as the PIN7 transporter (light blue) directs auxin apically from the basal and suspensor cells into the apical portion of the embryo. The blue arrows denote the direction of auxin flow in these early stages; the blue stars indicate the cells where auxin response maxima are observed. (b) The early and late globular stages. During these stages the precursor cell to embryonic root formation, the hypophyseal cell (peach), is specified and then divides asymmetrically to produce different root cell lineages. Expression of the transcription factor MP (green) results in upregulation of TMO7 RNA in the proembryo. In turn, some of the TMO7 proteins move into the presumptive hypophyseal cell to specify hypophyseal cell identity. Auxin also establishes this identity as it is transported into the hypophyseal cell by PIN1 carriers (yellow) of the proembryo and out of this cell by basally localized PIN7 carriers (gray) in the suspensor cells. As a result of transport, a maximum of auxin response is seen in the hypophyseal cell and the uppermost suspensor cell of the early globular stage (blue stars). Cytokinin response (red stars) is observed in the same cells as auxin response at this stage. However, after hypophyseal division, cytokinin and auxin responses are found in the apical and basal daughter cells, respectively, of the late-globular-stage embryo. This inverse expression profile is thought to be important for subsequent specification of embryonic root tissues. Yellow and blue arrows indicate the direction of auxin transport.

Figure 2

Patterning the root apical meristem. (a) Organization of the root apical meristem. Different cell types are arranged in cell files along the length of the root. The magnified region shows the stem cell niche and regulatory interactions that maintain it. SHR expressed in the stele moves into the quiescent center (QC) and cortex/endodermal initial (CEI) cells to maintain QC and stem cell identity; WOX5 maintains identity of the surrounding stem cells. WOX5 expression is confined to the QC through repression by ACR4, triggered by the CLE40 signal originating from differentiating columella cells. PLT expression throughout the niche also maintains QC and stem cell identity. (b) Organization of cell types within the stele. The diagram shows a cross section of the root tip. The pattern of cell types in the stele is bilaterally symmetric: A central axis of xylem is flanked by two phloem bundles. (c) Divisions of the CEI. The CEI first divides anticlinally to give rise to the CEI daughter (CEID) cell. The CEID then divides periclinally to give rise to the cortex and endodermal cell lineages. Activation of CYCD6 by SHR and SCR plays an important role in this asymmetric cell division. (d) Divisions of the epidermis/lateral root cap (LRC) initial. The epidermis/ LRC initial divides first periclinally to produce an LRC cell and then anticlinally to produce an epidermal cell. FEZ, expressed in the initial, represses SMB in the LRC daughter cell. SMB then represses FEZ, restricting it to the initial cells. Figure adapted from Reference .

Figure 3

Developmental zones of the Arabidopsis root. (a) Distinct developmental zones, shown in a longitudinal section through the primary root. Cell division occurs in the meristematic zone, cell expansion and elongation occur in the elongation zone, and cell differentiation (indicated by the formation of root hairs) occurs in the differentiation zone. The zone of transition between the meristematic and elongation zones is also indicated. (b) Cross section of the root tip showing the Casparian strip, which forms an impermeable barrier between endodermal cells such that water and nutrients must pass through endodermal cells en route to the vasculature. (c) Specification of root hairs. WER binds to a complex of other factors and activates GL2 and CPC in nonhair cells. CPC then moves to presumptive hair cells, where it competes with WER for binding to the complex. Signaling through SCM represses WER, which tips the balance in favor of CPC. The CPC-containing complex cannot upregulate GL2 expression, allowing specification of hair cell fate. The greater surface area between hair cells and overlying cortex cells may allow greater transmission of a JKD-dependent signal, which preferentially activates SCM in presumptive hair cells.

Figure 4

Lateral root development. (a) Schematic of the differentiation zone, showing a slice through the longitudinal axis of the primary root in the differentiation zone. Lateral roots are initiated in the pericycle cell layer (red) when anticlinal cell divisions occur in a subset of cells in this layer. (b) Stages of lateral root development. In stage I, small pericycle cells are seen that result from the anticlinal divisions in this layer. During stage II, the cells of stage I divide periclinally to form inner and outer layers. By stage III, the dome shape of the lateral root primordium (LRP) is apparent owing to the periclinal divisions of the outer layer and absence of these divisions in the more peripheral cells. The three-layered LRP of stage III becomes a four-layered LRP as a result of periclinal divisions during stage IV. In stage V, the cells of all layers undergo anticlinal divisions to generate an LRP that begins to push through the cortex layer of the primary root. In stage VI, the LRP starts to resemble a mature root tip, with epidermal, cortex, and endodermal cell layers from the outside to the inside of the LRP, respectively. The innermost tissue, the stele, becomes distinguishable and the LRP continues to undergo anticlinal cell divisions as it enlarges during stage VII. At the end of this stage, the LRP is about to emerge from the epidermis of the parent primary root as a lateral root.