Plant Gravitropism. Unraveling the Ups and Downs of a Complex Process

Abstract

Wind and heavy rain can have a devastating effect on crop production if they occur late during the life cycle of the plants. They often flatten the crop on the ground, leaving seed and other harvestable products at the mercy of soil moisture and pathogens and inaccessible to mechanical harvesting machinery. However, farmers will not worry much if a storm of similar strength hits a crop earlier in its cycle. They know that younger plants are able to straighten up and resume upward growth. This example illustrates the significance of tropism, or the ability of plant organs to direct their growth along a path that is dictated by their surrounding environment. In nature, plant organs can use a variety of environmental cues to guide their growth, including gravity, touch, light, gradients in temperature, humidity, ions, chemicals, and oxygen. In the example illustrated above, the stems of younger crops were able to perceive a change in their orientation within the gravity field. The corresponding information was then translated into a complex growth response called gravitropism that allowed them to straighten up and to eventually resume growth at a defined angle from the gravity vector, the gravitational set point angle (GSPA). The GSPA associated with specific plant organs is a function of the identity of the species and organ under consideration, its developmental phase, the physiological status of the plant, and a variety of environmental parameters to which the plant has been exposed. A plant organ is capable of detecting any deviation from its assigned GSPA and responds to the corresponding stimulus (gravitropic stimulus) by developing differential cellular elongation on opposite flanks, resulting in tip curvature and subsequent realignment with the GSPA (Firn and Digby, 1997). Gravitropism has been observed and analyzed in a variety of plant organs, including roots, hypocotyls, and inflorescence stems of dicots; roots, coleoptiles, and pulvini of monocots; and rhizoids and protonemata of algae and moss. It also has been observed and studied in fungal fruiting bodies. In 1999, an Update discussing the status of our understanding of gravitropism in roots of higher plants was published (Chen et al., 1999). Since then, there have been several developments in the field that have provided new insights on the different issues related to gravitropism in multiple plant systems. These breakthroughs are discussed in this Update. For a plant organ to guide its growth along a defined GSPA, it must perceive any change in its orientation within the gravity field. The corresponding physical information must be transduced into a physiological and/or biochemical signal, which must be transported to the response site where differential growth generates a curvature, allowing the growing tip to regain its orientation along the GSPA. As discussed in our previous Update (Chen et al., 1999), different cells are specialized to carry out these successive phases of gravitropism in monocots and dicots. For instance, in roots, gravity is perceived mainly by the columella cells of the root cap, whereas the differential growth response associated with gravistimulation occurs in the elongation zone (EZ; Figs. 1A and 2). In shoots, cells located in specialized tissues at the periphery of the vasculature, including the endodermis of hypocotyls (Fig. 1B), and the bundle sheath parenchyma in inflorescence stems and cereal pulvini perceive gravity and generate a signal that is transported laterally to the more peripheral tissues. There, the signal promotes the differential growth responsible for gravitropic curvature (Fig. 1B). On the other hand, in lower plants and algae exhibiting single-cell tip growth (i.e. rhizoids and protonemata), gravity perception and curvature response occur in the same cell (Fig. 1C). Hence, different species and organs adopt different molecular, cytological, and physiological strategies to guide their growth along specified GSPAs. Gravitropism in higher plants and algae. A, In roots of higher plants, the site of gravity sensing (i.e. the root cap) is spatially distinct from the site of the response (the EZ). Amyloplasts present in root columella cells settle to the bottom side of the cell (arrowheads) when the root is reoriented. There is overwhelming support that this process (starch-statolith hypothesis) constitutes one of the primary mechanisms of gravity sensing in plants. Depending on various environmental and endogenous factors, the reoriented root attains a specific GSPA with respect to the vertical. B, In shoots are located in the cell to the In rhizoids of the function of the in of which In to higher plants, the and response phases of gravitropism occur in the same of a root columella cell the and the It has been that the in the is in the physical information of to a physiological signal that to the gravity The of in In roots is transported the into the root where it in the of There, it is transported lat