Gravitropism in Higher Plants1

Abstract

Since 1806, we have known that plant organs use gravity as a guide for growth (Knight, 1806). The gravity-directed growth process, called gravitropism, dictates upward shoot growth to ensure a proper positioning of the leaves for efficient photosynthesis and gas exchange. It also directs roots to grow downward in soil, where they can reach out to take up the water and mineral ions required for plant growth and development. Gravitropism dictates upward shoot growth, as illustrated by the trees shown at the end of the corn field. The corn plants, on the other hand, were recently prostrated by a heavy storm (a). However, in a few hours, their shoots curved upward, as a result of gravitropism (b). At the end of the 19th century, Ciesielski (1872) and Darwin (1880)demonstrated that a structure at the tip of the roots, the cap, is essential for root gravitropism. They postulated that the root cap could perceive a change in root-tip orientation within the gravitational field (gravistimulus). Graviperception would then produce a physiological signal that, upon transmission to the elongation zone, would promote a differential cellular elongation on opposite flanks, which is responsible for the development of a curvature. The resulting curvature would allow the root tip to resume growth along a gravitropically more acceptable vector. These important early observations along with the proposed model for gravity perception marked the beginning of numerous studies that extended throughout the entire 20th century and helped us to gain a better understanding of the various physiological and molecular processes underlying gravitropism. In this Update we discuss our current knowledge of the gravitropic response of higher plants, with a special emphasis on roots. Different root-tip cells are involved in the sensing of and response to a gravistimulus (reorientation within the gravity field). The root tip of a 5-d-old Arabidopsis seedling contains a root cap made of columella and peripheral cells, a promeristem, a DEZ composed of cells that expand both longitudinally and radially, and a CEZ consisting of cells that preferentially elongate. Gravity sensing occurs primarily in the columella cells, called statocytes, of the root cap, whereas the curvature response to a gravistimulus occurs in the DEZ and CEZ. The root shown in this picture was viewed under a light microscope using Nomarski optics. Root width = 160 μm. The primary mechanism for gravity sensing in roots involves the sedimentation of amyloplasts in the root-cap columella cells. a, In this light micrograph starch-filled amyloplasts (dark brown) are revealed in the root-cap columella cells of a vertically grown Arabidopsis seedling by staining with an iodine/potassium iodide solution (Kiss et al., 1996). One of these columella cells, chosen as an example, is identified by a white circle in a and is schematized in b. The columella cell contains a nucleus (N) at the top, a peripheral ER, and sedimentable amyloplasts (a) at the physical bottom. c, Upon gravistimulation (reorientation of the root to the horizontal), the statocyte amyloplasts sediment from their original position (punctuated, light gray circles) to the new physical bottom of the cell (darker gray circles). According to the amyloplast-statolith hypothesis, amyloplast sedimentation is the primary mechanism by which gravity sensing occurs. In all of the panels, the root tip and statocytes were drawn according to their orientation relative to the gravity vector, g, represented by an arrow. The statocytes are highly polarized cells that contain a peripheral ER, a nucleus positioned in the middle or at the top, and dense amyloplasts sedimented at the physical bottom (Fig. 3b). When a plant organ is tilted within the field of gravity, amyloplasts sediment to the new physical bottom of the statocytes (Fig. 3, b and c). Amyloplast sedimentation is believed to activate receptors that trigger a signal transduction pathway leading to the formation of a physiological signal, which is responsible for organ-tip curvature (Evans and Ishikawa, 1997). Both direct and indirect evidence support a role for amyloplast sedimentation in gravitropic sensing. First, decapped roots do not respond to gravistimulation despite wild-type rates of growth (Darwin, 1880). Hence, the root cap appears to be essential for root gravitropism (Sack, 1997). Second, centrifugation experiments in which lateral acceleration forces were applied to different regions of a plant positioned along the general radius of a centrifuge demonstrated that the primary site of gravity sensing in roots overlaps with the root cap (for review, see Poff and Martin, 1989). Third, a good correlation exists between amyloplast density and gravitropic sensitivity in plants carrying amyloplasts, the starch content of which was reduced by physiological treatments or by mutations in genes required for its synthesis or accumulation (Sack, 1991; Kiss et al., 1996). Fourth, deve