Auxin-Regulated Lateral Root Organogenesis

Abstract

Plant fitness is largely dependent on the root, the underground organ, which, besides its anchoring function, supplies the plant body with water and all nutrients necessary for growth and development. To exploit the soil effectively, roots must constantly integrate environmental signals and react through adjustment of growth and development. Important components of the root management strategy involve a rapid modulation of the root growth kinetics and growth direction, as well as an increase of the root system radius through formation of lateral roots (LRs). At the molecular level, such a fascinating growth and developmental flexibility of root organ requires regulatory networks that guarantee stability of the developmental program but also allows integration of various environmental inputs. The plant hormone auxin is one of the principal endogenous regulators of root system architecture by controlling primary root growth and formation of LR. In this review, we discuss recent progress in understanding molecular networks where auxin is one of the main players shaping the root system and acting as mediator between endogenous cues and environmental factors.

Figure 1.

Lateral root priming and founder cell specification. (A) Schematic representation of the Arabidopsis seedling. Specific steps during lateral root (LR) development including priming, LR primordia (LRP) specification and initiation, and LR emergence are highlighted along the primary root (PR) in gray boxes. Pericycle cells involved in early stages of LR development are depicted in yellow. (B) Priming of pericycle founder cells (FCs) starts in the basal meristem and is driven by auxin reflux from the LR cap (LRC) (red arrows) to epidermal root cells. In the LRC, auxin flow is reinforced by the conversion of indole-3-butyric (IBA) to indole-3-acetic acid (IAA) (black dashed line). Factors promoting or repressing LR priming are included in the scheme (black arrows and bar-headed lines, respectively). Auxin priming of a xylem-pole pericycle (XPP) cell is highlighted in yellow. (C) Specification of FCs triggers the inhibition of FC establishment and LR initiation in flanking XPP cells. Polar localization of PIN3 (marked in green) regulates active auxin flow from the endodermis to the FC. Auxin signaling promoting or repressing expression of the indicated modules is given in red (arrows or bar-headed lines, respectively). Factors involved in FC specification and inhibition in the neighboring cells and their signaling pathways are depicted (black arrows and bar-headed lines). Auxin accumulates in the FC (yellow), while the neighboring FC flanking cells have a higher cytokinin content (blue). (Pc) Pericycle, (En) endodermis, (MZ) meristematic zone, (OZ) oscillation zone.

Figure 2.

Lateral root primordia development: from initiation to outgrowth. (A) Swelling of founder cells (FCs), nuclear movement, cytoskeleton rearrangements, and first asymmetric cell divisions defines the onset of lateral root primordia (LRP) development. Auxin signaling (red bar-headed lines) promotes the degradation of Aux/IAA repressing factors such as IAA14 and IAA3 and thereby stimulates the expression of downstream ARF, LBD transcription factors, and cell cycle and cell wall remodeling genes. Different factors are acting in the neighboring cells in which ectopic LRP initiation is inhibited. The initial cells of LRP accumulate higher auxin concentrations and are reported in yellow. (B) LRP organogenesis and outgrowth is regulated through several auxin signaling modules. The auxin signaling cascade and expression of specific factors involved are indicated in the relevant cell layers. At the surface of the developing LRP, a cuticle layer is formed to prevent adhesion when penetrating the overlaying tissues. In the cortex, LAX3 and PIN3 localization are marked in red and green, respectively. (MT) Microtubule, (Pc) pericycle, (En) endodermis, (Co) cortex, (Ep) epidermis.

Figure 3.

Auxin and cytokinin define the gravitropic set point angle of the lateral root (LR) upon emergence. PIN-driven auxin flow to LR columella cells (yellow) is depicted as a red central arrow. Asymmetric cytokinin distribution in the LR cap (LRC) cell and in the upper side of LR is highlighted in blue. Interactions among factors interfering with the gravitropic angle are indicated (bar-headed lines). Differential cell elongation between the upper and lower side of LR is represented as double-headed black arrows.

Figure 4.

Environmental factors regulating lateral root (LR) development. Schematic representation of environmental cues, signaling pathways, and molecular mechanism regulating LR organogenesis. Factors promoting or repressing LR developments are indicated as black arrows or bar-headed lines, respectively.