To branch or not to branch: the role of pre-patterning in lateral root formation

Abstract

The establishment of a pre-pattern or competence to form new organs is a key feature of the postembryonic plasticity of plant development, and the elaboration of such pre-patterns leads to remarkable heterogeneity in plant form. In root systems, many of the differences in architecture can be directly attributed to the outgrowth of lateral roots. In recent years, efforts have focused on understanding how the pattern of lateral roots is established. Here, we review recent findings that point to a periodic mechanism for establishing this pattern, as well as roles for plant hormones, particularly auxin, in the earliest steps leading up to lateral root primordium development. In addition, we compare the development of lateral root primordia with in vitro plant regeneration and discuss possible common molecular mechanisms.

Keywords: Auxin; Callus formation; Lateral root development; Periodic gene expression; Pre-patterning.

Fig. 1.

Structure and development of the Arabidopsis root. (A) Median longitudinal section depicting developmental time (black arrow) in the longitudinal axis. A prebranch site (magenta) forms after an oscillation of gene expression within the oscillation zone (dotted line). Prebranch sites indicate competence to form a lateral root primordium (LRP) in the future. After competence is established, it is predicted that xylem pole pericycle (XPP) cells within a prebranch site can be specified as lateral root founder cells (LRFCs, green hatching). LRP initiate in the differentiation zone through asymmetric cell division of LRFCs, which gives rise to smaller cells (blue). (B) Transverse section. Periodic expression of DR5:GUS occurs in the protoxylem; however, because lateral root (LR) initiation occurs in the adjacent XPP cells, signaling between these cell types might be required for LRFC specification. Note that the ground tissue comprises two cell layers: the outermost cortex and the endodermis, which is immediately exterior to the pericycle. (C) Cut-away portion of the median longitudinal section focused on a region where an LR will form. XPP cells are predicted to be sequentially specified as LRFCs (green hatching), then activated to undergo cell division (green/white hatching). LRFC activation results in the coordinated migration of nuclei (white circles) towards the common cell wall in a pair of longitudinally abutted cells. These cells then undergo asymmetric division, giving rise to smaller cells (blue), to generate a stage I LRP. The primordium grows through the outer cell layers of the primary root until it emerges from the epidermis. Drawing is not to scale.

Fig. 2.

LRs emerge from the outside of curves in the primary root. Schematics of root bends formed under various experimental conditions. (A) Root waving occurs as roots grow along the surface of agar plates. LRP develop and eventually emerge from the outside of the curves. The arrowheads indicate positions of incipient LRP. (B) Bends can be induced to form in the root through manual manipulation of the seedling either by pulling the shoot downward (left) or by pushing the root tip upward (right). (C) Gravistimulation-induced bends. If seedlings are reoriented with respect to the gravity vector, a bend will form as the root tip responds to realign the tip to gravity through differential growth. (D) In the absence of gravitropic response in either the root or shoot, a bend can be induced by root growth into a barrier (purple bar). (E) Bends can also be induced by cutting the agar on either side of a growing root (gray dotted line) and sliding the agar to one side, thereby creating two bends in the root. In these gel-sliding assays, neither the root tip nor shoot is exposed to manual contact or reorientation. Arrowheads (B-E) indicate the position of LRP emergence in response to induced bends.

Fig. 3.

Prebranch sites mark the positions at which LRP will subsequently develop and emerge. (A) An oscillation in DR5:LUC expression (chemiluminescence signal imaged at 5-6 minute exposure times) in the oscillation zone (OZ) leads to the formation of a prebranch site (asterisk). (B) Quantification of the oscillation of DR5:LUC expression in two individual roots. The oscillation has a period of ∼6 hours and appears to precede the changes in growth direction of the root tip during root waving. Blue/dark blue arrows indicate the time points at which bends were formed in each of the primary roots. ADU, analog-digital units. (C) Overlay of a luciferase and brightfield image (taken 5 days after the luciferase image) to show emerged lateral roots. Arrowheads indicate positions at which LRP have yet to emerge. (B,C) Adapted with permission (Moreno-Risueno et al., 2010).