Perception of Gravity in Plants

Experimentally, the gravitropic response can be studied by growing a seedling in the vertical position (the root tip down) and then placing the root in the horizontal position. The root is then subjected to gravistimulation. In this case, its extremity bends downward in order to recover its normal direction of growth (Figure 6-02). The curvature is due to a differential growth in the upper and lower halves of this organ.

It is generally accepted (Perbal and Driss-Ecole 2003) that the gravitropic response is composed of four different phases (Figure 6-03), which correspond to:

a. The perception of the stimulus (physical phase);

b. The transduction of this stimulus (change of the mechanical effect into a biochemical factor);

c. The transmission of the signal (from the gravisensing cells to the responding cells);

d. The differential growth of the upper and lower sides of the organ.

Gravisensing cells Root cap

Figure 6-03. The different phases of the gravitropic curvature of the root. Four phases are generally distinguished. The perception is the physical phase of the gravitropic reaction and corresponds to the movement of the statoliths in the gravisensing cells located in the root cap. It is followed by the transduction of the stimulus, i.e., the transformation of the mechanical effect of gravity into a biochemical factor. Both phases occur within the gravisensing cells. The transmission of gravistimulus to the reaction zone consists in an asymmetrical hormonal message (downward transport of auxin). It is responsible for a differential growth (curvature) that occurs far away from the perception zone. Note the time scale.

Perception Transduction Transmission Cur\>ature Os Is 10 s 10 min

Gravisensing cells Root cap

Figure 6-03. The different phases of the gravitropic curvature of the root. Four phases are generally distinguished. The perception is the physical phase of the gravitropic reaction and corresponds to the movement of the statoliths in the gravisensing cells located in the root cap. It is followed by the transduction of the stimulus, i.e., the transformation of the mechanical effect of gravity into a biochemical factor. Both phases occur within the gravisensing cells. The transmission of gravistimulus to the reaction zone consists in an asymmetrical hormonal message (downward transport of auxin). It is responsible for a differential growth (curvature) that occurs far away from the perception zone. Note the time scale.

At the beginning of the 20th century, Haberlandt and Nemec (see Larsen 1962) have shown that special tissues called statenchyma of shoots and roots contain movable organelles, the amyloplasts, in their cells, which sediment under the influence of gravity (Figure 6-04). Their sedimentation is due to the density of starch (1.44 g x cm"3) contained in these organelles (Sack 1991). These authors hypothesized that the amyloplasts were responsible for gravisensing and called them statoliths in reference to those observed in invertebrates. The great difference in the gravisensing of plants and animals is that the former possess statoliths that are inside specialized cells, the statocytes, whereas in the latter they are outside a group of specialized cells. It must be added that mosses, which are gravitropic, show a special sub terminal zone were amyloplasts can sediment under the influence of gravity (Schwuchow et al. 2002a, 2002b). In the rhizoid of the characean green alga

Chara, gravisensing is due to BaS04-cristal-filled statoliths (Sievers et al. 1996).

In roots, where the statenchyma has been more intensively studied, this tissue is located in the center of the cap (Volkmann and Sievers 1979, Boonsirichai et al. 2002, Perbal and Driss-Ecole 2003) (Figure 6-05A). When the root is placed in the horizontal position, these organelles move toward and sediment along the lower longitudinal wall. One of the best evidence of the involvement of the statenchyma in gravitropism was provided by Juniper et al. (1966) who showed that removing the cap of the maize root without damaging the root tip suppressed their ability to respond to a gravistimulus, i.e., a change in orientation in the gravitational field. This experiment demonstrated that at least one step of the gravitropic curvature occurred in the

Figure 6-04. Gravisensing cells (statocytes) in a lentil root (in A) and in the Asparagus shoot or epicotyl (in B). The shoot statocyte possess a large vacuole (v), whereas only veiy small vacuoles can be seen in the root statocyte. Both statocytes show a structural polarity. In both cases, the amyloplasts (a) are located close to the distal wall (dw, at the bottom of the cell). The nucleus (N) is situated near the proximal wall (pw) in the root statocyte and near the distal wall (dw) in the shoot statocytes. g: direction of gravity; Iw; longitudinal wall; nu; nucleolus; er; endoplasmic reticulum.

Figure 6-04. Gravisensing cells (statocytes) in a lentil root (in A) and in the Asparagus shoot or epicotyl (in B). The shoot statocyte possess a large vacuole (v), whereas only veiy small vacuoles can be seen in the root statocyte. Both statocytes show a structural polarity. In both cases, the amyloplasts (a) are located close to the distal wall (dw, at the bottom of the cell). The nucleus (N) is situated near the proximal wall (pw) in the root statocyte and near the distal wall (dw) in the shoot statocytes. g: direction of gravity; Iw; longitudinal wall; nu; nucleolus; er; endoplasmic reticulum.

Taken together with the Picard's experiment (see Larsen 1962), which proved at the beginning of the 20th century that sensitivity to gravity was greater in the root tip than in any other region of the root, these results indicated that the perception of gravity mainly took place in the central root cap cells or statocytes. However, it is possible that other cells could be gravisensitive to a lesser extend (Wolverton et al. 2002). More recently, it has been demonstrated (Blancaflor et al. 1998) by using a method of cell ablation with a laser beam that statocytes of Arabidopsis thaliana have a sensitivity that depends upon their state of differentiation, and therefore their location in the cap. Thus, it is well accepted that roots statocytes (Figure 6-04A) are responsible for gravisensing (Rosen et al. 1999, Boonsirichai et al. 2002, Blancaflor and Masson 2003).

In shoots, the role of statocytes was demonstrated only recently (Perbal and Rivière 1980). In these organs, the statocytes are located in a cellular layer which surrounds the vascular bundle (Figure 6-04B). Fukaki et al. (1998) have shown that two agravitropic (i.e., which do not respond to a gravistimulus) mutants (sgr 1, sgr 7) of Arabidopsis thaliana did not possess this tissue, which confirmed the role of statocytes in shoot gravitropism, even if it does not prove that the perception of gravity occurs in this cell layer.

Although it is well accepted that statocytes are involved in gravisensing, the role of amyloplasts in graviperception is less clear (Barlow 1995, Sack 1997). Studies on starch-depleted mutants (Kiss et al. 1989, Caspar and Pickard 1989) as well as experiments leading to experimentally reducing the volume of starch by various treatments have not demonstrated that the amyloplasts are the unique graviperceptors (Sack 1997). Some authors have therefore proposed that the whole protoplasm' could play this role (Wayne et al. 1992), and it has been demonstrated that this possibility cannot be discarded if amyloplasts act by exerting pressure on structures lining the plasma membrane (Perbal 1999). In this case, the pressure exerted by the amyloplasts on these structures should be greater than that of the protoplasm. The hypothesis of the protoplasm playing the role of graviperceptor could explain the reason why starch-depleted mutants (Kiss et al. 1989, Caspar and Pickard 1989) can still respond to gravistimulus (Figure 6-05). It implies that gravireceptors are very sensitive to pressure and that the amyloplasts do not need a large amount of starch to be efficient. The results obtained by Kiss et al. (1996) on root gravitropism in intermediate-starch mutants of Arabidopsis thaliana showed that 51-60% of the level of starch is near the threshold amount needed for full sensitivity. The statolith apparatus (the amyloplast bulk) could be therefore overbuilt in the sense that it could be larger than necessary (Aarrouf and Perbal 1996).

It is well known that the phase of perception occurs even at low temperature (4°C), although no gravitropic response takes place for hours (Wyatt et al. 2002). If Arabidopsis plants stimulated in the horizontal position at 4°C are placed in the vertical position at room temperature their

' Protoplasm is the substance inside the membrane of a living cell. At the simplest level, it is divisible into cytoplasm and nucleoplasm.

inflorescence curves, which means that there is a persistence of the signal. At 4°C, the amyloplasts sediment but the stimulus is not transmitted.

Simulation Time (min)

Figure 6-05. Root gravitropism of the starch-depleted (TC7) and the wild type (WT) mutants of Arabidopsis thaliana. In A, the angle of curvature is graphed as a function of time in h. In B, the response is graphed as a function of the logarithm of the stimulation time (in min). The presentation time (minimal time of stimulation to induce a visible response) is estimated by extrapolating the regression line down to zero curvature. The presentation time is approximately 24 s for the WT and 78 s for the TC7 mutants. Adapted from Kiss et al. (1989).

Simulation Time (min)

Figure 6-05. Root gravitropism of the starch-depleted (TC7) and the wild type (WT) mutants of Arabidopsis thaliana. In A, the angle of curvature is graphed as a function of time in h. In B, the response is graphed as a function of the logarithm of the stimulation time (in min). The presentation time (minimal time of stimulation to induce a visible response) is estimated by extrapolating the regression line down to zero curvature. The presentation time is approximately 24 s for the WT and 78 s for the TC7 mutants. Adapted from Kiss et al. (1989).

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