Arabidopsis thaliana: A Model for the Study of Root and Shoot Gravitropism

Abstract

For most plants, shoots grow upward and roots grow downward. These growth patterns illustrate the ability for plant organs to guide their growth at a specified angle from the gravity vector (gravitropism). They allow shoots to grow upward toward light, where they can photosynthesize, and roots to grow downward into the soil, where they can anchor the plant as well as take up water and mineral ions.Gravitropism involves several steps organized in a specific response pathway. These include the perception of a gravistimulus (reorientation within the gravity field), the transduction of this mechanical stimulus into a physiological signal, the transmission of this signal from the site of sensing to the site of response, and a curvature-response which allows the organ tip to resume growth at a predefined set angle from the gravity vector.The primary sites for gravity sensing are located in the cap for roots, and in the endodermis for shoots. The curvature response occurs in the elongation zones for each organ. Upon gravistimulation, a gradient of auxin appears to be generated across the stimulated organ, and be transmitted to the site of response where it promotes a differential growth response. Therefore, while the gravity-induced auxin gradient has to be transmitted from the cap to the elongation zones in roots, there is no need for a longitudinal transport in shoots, as sites for gravity sensing and response overlap in this organ.A combination of molecular genetics, physiology, biochemistry and cell biology, coupled with the utilization of Arabidopsis thaliana as a model system, have recently allowed the identification of a number of molecules involved in the regulation of each phase of gravitropism in shoots and roots of higher plants. In this review, we attempt to summarize the results of these experiments, and we conclude by comparing the molecular and physiological mechanisms that underlie gravitropism in these organs.

Abbreviations: GSPA: gravitational set point angle; IAA: indole-3-acetic acid; NAA: 1-naphthalene acetic acid; NPA: 1-N-naphthylphthalamic acid; 2,4-D: 2,4-dichlorphenoxy acetic acid; TIBA: 2,3,5-triiodobenzoic acid.

Figure 1.

Plant organs grow using a combination of cell division in apical meristems and cell expansion in elongation zones. A. Root from a 3 day-old light-grown Arabidopsis seedling (left), showing the cap, elongation zones (EZ) and mature zone (MZ). The insert (right) represents a confocal image of a propidium iodide –stained Arabidopsis root tip showing the root cap (with its L1, L2 and L3 layers of columella cells, and lateral cap (LRC) cells), the promeristem (with its quiescent center cells (QC) surrounded by initials), the distal elongation zone (DEZ) and a small region of the central elongation zone (CEZ). The root proper is composed of several cell layers, including the epidermis (Ep), the cortex (C), the endodermis (En) and the stele (St). B. Top of an inflorescence stem showing the stem ended by a shoot apical meristem (SAM), flowers and siliques. The entire stem region located below the SAM in this picture is part of the elongation zone (EZ). The middle drawing corresponds to a region of the shoot stem. Microscopical image of a longitudinal section of this region (indicated by the rectangle in the drawing) is represented on the right, showing the epidermis (Ep), three layers of cortical cells (C), one layer of endodermis (En), and the stele (St). Sedimenting amyloplasts are represented by black arrowheads.

Figure 2.

Root gravitropism in Arabidopsis thaliana seedlings. (A) shows a 4 day-old Arabidopsis thaliana seedling (WS ecotype) transferred onto the surface of a 0.8% agar-based 1/2 MS medium (Sedbrook et al., 1999), immediately after reorientation of the plate to position the seedling horizontally (gravistimulation). (B) 33 hours later, both root and hypocotyl have reoriented their growth such that the root is growing vertically downward, and the hypocotyl upward. In both A and B, the gravity vector was directed downward on the picture. (C) Kinetics of root gravitropism after a 90° reorientation similar to the one described in A. The mean root tip angle from the horizontal is shown on the Y axis (in degrees), while the time elapsed since gravistimulation is represented on the X axis (in hours). n = 150 – 200. Error bars represent standard deviations.

Figure 3.

Shoot Gravitropism of Arabidopsis thaliana. (A) and (B) Gravitropic response of inflorescence stems after 0 min (A) and 90-min (B) of horizontal gravistimulation at 23°C in the dark. 5-week-old wild-type plants (Columbia) were used. (C) Gravitropic response of a decapitated inflorescence stem segment of Arabidopsis thaliana. The stem segment was placed horizontally at time 0 h at 23°C in the dark. The shape of the stem was traced at the indicated times. A white rectangle indicates gel block as a holder. The basal side of the stem segment was embedded in the gel block. The apical side was free to move.

Figure 4.

sgr1/scr and sgr7/shr inflorescence stems lack an endodermal layer. Left and middle: Schematic model of longitudinal section of inflorescence stem, as defined in figure 1B legend. Generally, wild-type inflorescence stem has one layer of epidermis, three layers of cortex, and one layer of endodermis (middle, and figure 1B). In contrast, inflorescence stems of sgr1/scr and sgr7/shr lack the endodermis (right).

Figure 5.

Endodermal cells of sgr2 and sgr4/zig mutants contain abnormally positioned amyloplasts. Longitudinal sections through inflorescence stems of wild-type (A), sgr2-1 (B), and zig-1 (C). Growth orientation of stems was maintained during fixation. Arrowheads indicate amyloplasts. Vertical arrows represent the gravity vector.

Figure 6.

Spatial relationship between gravity sensing tissue and elongation zone in roots and shoots. In a root (left), the gravity vector (g) is perceived in the columella cells in the root cap. A signal (arrow) is transmitted from the columella cells to the elongation zone in an apical-to-basal fashion. In an inflorescence stem (right), gravity sensing is carried out in the endodermal cells and a signal (arrow) is transmitted in an inner-to-outer fashion.

Figure 7.

The chemiosmotic model of polar auxin transport in plants. IAA is in equilibrium between its protonated and ionic forms. In the apoplast, a reasonably large amount of IAA is in the protonated form, due to the low pH. Protonated IAA can enter the cell by passive diffusion through the plasma membrane, as well as through a transmembrane auxin influx carrier (green oval). Once within the cell, most of this IAA is converted into the ionized form. It can exit the cell by active transport through an auxin efflux carrier, made of at least one transmembrane protein (red cylinder), a regulatory NPA-binding protein (green octogon), and a potential linker protein (yellow triangle). The direction of auxin transport is dictated by the polar distribution of the auxin efflux carrier within the transporting cells (Müller et al., 1998). In this model auxin transport is represented by yellow arrows.

Figure 8.

Model for gravity perception in inflorescence stems in Arabidopsis. (A) Inflorescence stem segment after gravitropic overshooting, displaying a ‘U’ shape. This stem segment was analyzed 2 hr after gravistimulation, as shown in Figure 3C. Thick lines indicate the lower side of the stem. Thin stem units located at the apical half of the stem segment should perceive a gravistimulus that is opposite to the initial stimulus. (B) Cross-section of a horizontally-oriented stem. Black arrows indicate the orientation of gravity. Blue arrows indicate the radial vector. A comparison between these two directions may provide each endodermal cell with a unique directional information. g, gravity orientation