Gravity Signaling in Flowering Plant Roots

Abstract

Roots typically grow downward into the soil where they anchor the plant and take up water and nutrients necessary for plant growth and development. While the primary roots usually grow vertically downward, laterals often follow a gravity set point angle that allows them to explore the surrounding environment. These responses can be modified by developmental and environmental cues. This review discusses the molecular mechanisms that govern root gravitropism in flowering plant roots. In this system, the primary site of gravity sensing within the root cap is physically separated from the site of curvature response at the elongation zone. Gravity sensing involves the sedimentation of starch-filled plastids (statoliths) within the columella cells of the root cap (the statocytes), which triggers a relocalization of plasma membrane-associated PIN auxin efflux facilitators to the lower side of the cell. This process is associated with the recruitment of RLD regulators of vesicular trafficking to the lower membrane by LAZY proteins. PIN relocalization leads to the formation of a lateral gradient of auxin across the root cap. Upon transmission to the elongation zone, this auxin gradient triggers a downward curvature. We review the molecular mechanisms that control this process in primary roots and discuss recent insights into the regulation of oblique growth in lateral roots and its impact on root-system architecture, soil exploration and plant adaptation to stressful environments.

Keywords: auxin; elongation zone; flowering plant; gravitropism; lateral root; primary root; statocyte; statolith.

Figure 1

Model illustrating some of the molecular mechanisms that underlie root gravitropism in flowering plants. (A) An Arabidopsis thaliana root tip is positioned horizontally (gravistimulated). Auxin flow along the root tip is indicated with yellow bars whose widths represent flow intensity. In roots, auxin is transported from the shoot through the vasculature into the root tip where it is redistributed laterally to peripheral tissues and transported back to the elongation zone (EZ). The gravity vector (g) is represented by a red arrow. (B) Upon gravistimulation, amyloplasts sediment within the columella cells of the root cap, triggering a signal transduction pathway that leads to LZY protein association with the plasma membrane where it recruits RLD regulators of vesicular trafficking. RLD then directs PIN3 (and possibly PIN7) transcytosis toward the lower membrane, resulting in preferential downward transport of auxin and lateral auxin gradient formation across the cap [68]. (C,D) The auxin gradient generated across the cap upon gravistimulation is transported to the elongation zone where it promotes differential cell elongation between opposite sides and downward curvature. (C) Epidermal cells on the lower side of the root elongation zone (EZ) are exposed to high auxin levels, which promote PIN2 retention at the plasma membrane through a pathway that involves uncharacterized receptors. Increased auxin levels also activate CNGC14 ion channels, leading to increased cytosolic Ca²⁺ levels and activation of a H⁺/OH^- antiporter. This pathway leads to an increase in apoplastic pH responsible for wall-polymer crosslinking and inhibition of cell elongation [69]. The plasma membrane associated auxin receptors (labeled IAA-R) involved in these processes remain poorly characterized. (D) In the upper half of the root, transporting cells are exposed to lower auxin levels, resulting in a decreased retention of PIN2 within the plasma membrane and lower auxin transport potential on this side of the root. Furthermore, decreased auxin levels lead to the activation of H⁺ pumps, resulting in an acidification of the apoplast. Decreased apoplastic pH leads to the activation of expansin and XTH enzymes responsible for increased elongation. The combination of decreased expansion on the lower side and increased elongation on the upper half results in downward root curvature at the distal side of the elongation zone. The molecular players are represented by symbols whose identity is revealed in the legend on the right of the figure. Yellow arrows indicate auxin transport. Dotted arrows represent signal transduction pathways. Blue arrows represent endo- and exocytosis. Question marks identify molecules or steps within pathways that are not well characterized. The various steps represented in this model are described and discussed in the text with appropriate references. Contribution of canonical nuclear SCF^TIR-dependent expression regulation to the pathways described here is not represented in this figure. This figure was inspired from [68,69,70].