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PubMed1989

Gravitropism in a starchless mutant of Arabidopsis: implications for the starch-statolith theory of gravity sensing.

The starch-statolith theory of gravity reception has been tested with a mutant of Arabidopsis thaliana (L.) Heynh. which, lacking plastid phosphoglucomutase (EC 2.7.5.1) activity, does not synthesize starch. The hypocotyls and seedling roots of the mutant were examined by light and electron microscopy to confirm that they did not contain starch. In upright wild-type (WT) seedlings, starch-filled plastids in the starch sheath of the hypocotyl and in three of the five columellar layers of the root cap were piled on the cell floors, and sedimented to the ceilings when the plants were inverted. However, starchless plastids of the mutant were not significantly sedimented in these cells in either upright or inverted seedlings. Gravitropism of light-grown seedling roots was vigorous: e.g., 10 degrees curvature developed in mutants rotated on a clinostat following a 5 min induction at 1 g, compared with 14 degrees in the WT. Curvatures induced during intervals from 2.5 to 30 min were 70% as great in the mutant as the WT. Thus under these conditions the presence of starch and the sedimentation of plastids are unnecessary for reception of gravity by Arabidopsis roots. Gravitropism by hypocotyls of light-grown seedlings was less vigorous than that by roots, but the mutant hypocotyls exhibited an average of 70-80% as much curvature as the WT. Roots and hypocotyls of etiolated seedlings and flower stalks of mature plants were also gravitropic, although in these cases the mutant was generally less closely comparable to the WT. Thus, starch is also unnecessary for gravity reception in these tissues.

Arabidopsis↗
PubMed2003

Otolith formation in a mutant Medaka with a deficiency in gravity-sensing.

Mutant Medaka ha exhibit spontaneous mutation that is characterized by frequent inhibition or perturbation in the formation of utricular otoliths and/or semicircular canals. Three major features of otolith morphogenesis were observed in ha strain: 1) The initial appearance of otoliths was delayed, mispositioned, and malformed compared to normal embryos. 2) No utricular otoliths appeared on macula of any ha fry just after hatching. A symmetric state of otoliths was seen only when saccular otoliths were situated on macula in both inner ears. 3) In some fry, formation of utricular otoliths was observed in their later development. However, no new utricular otoliths appeared after fish were seventy or more days old after hatching. These observations show that otolith morphogenesis in ha is very different from that of wild-type. In this study, we classified adult ha into four different phenotypes using the existence or absence of utricular otoliths as our criteria. We concluded that dysfunction of utricular otoliths and semicircular canals cause a defect that affects the gravity-sensing abilities of medaka ha.

Animals↗
PubMed2001

Nodal endoplasmic reticulum, a specialized form of endoplasmic reticulum found in gravity-sensing root tip columella cells.

The endoplasmic reticulum (ER) of columella root cap cells has been postulated to play a role in gravity sensing. We have re-examined the ultrastructure of columella cells in tobacco (Nicotiana tabacum) root tips preserved by high-pressure freezing/freeze-substitution techniques to gain more precise information about the organization of the ER in such cells. The most notable findings are: the identification of a specialized form of ER, termed "nodal ER," which is found exclusively in columella cells; the demonstration that the bulk of the ER is organized in the form of a tubular network that is confined to a peripheral layer under the plasma membrane; and the discovery that this ER-rich peripheral region excludes Golgi stacks, vacuoles, and amyloplasts but not mitochondria. Nodal ER domains consist of an approximately 100-nm-diameter central rod composed of oblong subunits to which usually seven sheets of rough ER are attached along their margins. These domains form patches at the interface between the peripheral ER network and the ER-free central region of the cells, and they occupy defined positions within central and flanking columella cells. Over one-half of the nodal ER domains are located along the outer tangential walls of the flanking cells. Cytochalasin D and latrunculin A cause an increase in size and a decrease in numbers of nodal ER domains. We postulate that the nodal ER membranes locally modulate the gravisensing signals produced by the sedimenting amyloplasts, and that the confinement of all ER membranes to the cell periphery serves to enhance the sedimentability of the amyloplasts in the central region of columella cells.

Endoplasmic Reticulum↗
PubMed2004

Tip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids.

Polar organization and gravity-oriented, polarized growth of characean rhizoids are dependent on the actin cytoskeleton. In this report, we demonstrate that the prominent center of the Spitzenkörper serves as the apical actin polymerization site in the extending tip. After cytochalasin D-induced disruption of the actin cytoskeleton, the regeneration of actin microfilaments (MFs) starts with the reappearance of a flat, brightly fluorescing actin array in the outermost tip. The actin array rounds up, produces actin MFs that radiate in all directions and is then relocated into its original central position in the center of the Spitzenkörper. The emerging actin MFs rearrange and cross-link to form the delicate, subapical meshwork, which then controls the statolith positioning, re-establishes the tip-high calcium gradient and mediates the reorganization of the Spitzenkörper with its central ER aggregate and the accumulation of secretory vesicles. Tip growth and gravitropic sensing, which includes control of statolith positioning and gravity-induced sedimentation, are not resumed until the original polar actin organization is completely restored. Immunolocalization of the actin-binding proteins, actin-depolymerizing factor (ADF) and profilin, which both accumulate in the center of the Spitzenkörper, indicates high actin turnover and gives additional support for the actin-polymerizing function of this central, apical area. Association of villin immunofluorescence with two populations of thick undulating actin cables with uniform polarity underlying rotational cytoplasmic streaming in the basal region suggests that villin is the major actin-bundling protein in rhizoids. Our results provide evidence that the precise coordination of apical actin polymerization and dynamic remodeling of actin MFs by actin-binding proteins play a fundamental role in cell polarization, gravity sensing and gravity-oriented polarized growth of characean rhizoids.

Actin Depolymerizing Factors↗
PubMed1997

Evidence for the involvement of carbonic anhydrase and urease in calcium carbonate formation in the gravity-sensing organ of Aplysia californica.

To better understand the mechanisms that could modulate the formation of otoconia, calcium carbonate granules in the inner ear of vertebrate species, we examined statoconia formation in the gravity-sensing organ, the statocyst, of the gastropod mollusk Aplysia californica using an in vitro organ culture model. We determined the type of calcium carbonate present in the statoconia and investigated the role of carbonic anhydrase (CA) and urease in regulating statocyst pH as well as the role of protein synthesis and urease in statoconia production and homeostasis in vitro. The type of mineral present in statoconia was found to be aragonitic calcium carbonate. When the CA inhibitor, acetazolamide (AZ), was added to cultures of statocysts, the pH initially (30 min) increased and then decreased. The urease inhibitor, acetohydroxamic acid (AHA), decreased statocyst pH. Simultaneous addition of AZ and AHA caused a decrease in pH. Inhibition of urease activity also reduced total statoconia number, but had no effect on statoconia volume. Inhibition of protein synthesis reduced statoconia production and increased statoconia volume. In a previous study, inhibition of CA was shown to decrease statoconia production. Taken together, these data show that urease and CA play a role in regulating statocyst pH and the formation and maintenance of statoconia. CA produces carbonate ion for calcium carbonate formation and urease neutralizes the acid formed due to CA action, by production of ammonia.

Animals↗
PubMed1973

Gravity sensing by plants.

A brief description of the effects of gravity on plants, particularly their orientation with reference to its direction, is followed by a presentation of evidence for the operation of specific "gravity sensors", statoliths, subcellular bodies which move or reorient themselves upon reorientation of a plant organ with respect to the direction of the force of gravity. In the singly reacting apical cells of rhizoids of Chara, the statoliths locally regulate the growth of the cell wall simply by blocking or permitting the access of carriers of cell wall material. In multicellular structures (root and stem tips etc.) the statoliths, most likely amyloplasts (starch-containing plastids), must act by creating in the organ a transversal polarity which can be transmitted to the growing region, often several millimetres away. In addition, gravity produces what may be called tonic effects, which quantitatively modify the reaction of the organ to the gravitational stimulation.

Chlorophyta↗
PubMed2001

Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots.

Quantitative analysis of statolith sedimentation behavior was accomplished using videomicroscopy of living columella cells of corn (Zea mays) roots, which displayed no systematic cytoplasmic streaming. Following 90 degrees rotation of the root, the statoliths moved downward along the distal wall and then spread out along the bottom with an average velocity of 1.7 microm min(-1). When statolith trajectories traversed the complete width or length of the cell, they initially moved horizontally toward channel-initiation sites and then moved vertically through the channels to the lower side of the reoriented cell where they again dispersed. These statoliths exhibited a significantly lower average velocity than those sedimenting on distal-to-side trajectories. In addition, although statoliths undergoing distal-to-side sedimentation began at their highest velocity and slowed monotonically as they approached the lower cell membrane, statoliths crossing the cell's central region remained slow initially and accelerated to maximum speed once they reached a channel. The statoliths accelerated sooner, and the channeling effect was less pronounced in roots treated with cytochalasin D. Parallel ultrastructural studies of high-pressure frozen-freeze-substituted columella cells suggest that the low-resistance statolith pathway in the cell periphery corresponds to the sharp interface between the endoplasmic reticulum (ER)-rich cortical and the ER-devoid central region of these cells. The central region is also shown to contain an actin-based cytoskeletal network in which the individual, straight, actin-like filaments are randomly distributed. To explain these findings as well as the results of physical simulation experiments, we have formulated a new, tensegrity-based model of gravity sensing in columella cells. This model envisages the cytoplasm as pervaded by an actin-based cytoskeletal network that is denser in the ER-devoid central region than in the ER-rich cell cortex and is linked to stretch receptors in the plasma membrane. Sedimenting statoliths are postulated to produce a directional signal by locally disrupting the network and thereby altering the balance of forces acting on the receptors in different plasma membrane regions.

Actins↗
PubMed1993

Centrifugation causes adaptation of microfilaments: studies on the transport of statoliths in gravity sensing Chara rhizoids.

The actin cytoskeleton is involved in the positioning of statoliths in tip growing Chara rhizoids. The balance between the acropetally acting gravity force and the basipetally acting net outcome of cytoskeletal force results in the dynamically stable position of the statoliths 10-30 micrometers above the cell tip. A change of the direction and/or the amount of one of these forces in a vertically growing rhizoid results in a dislocation of statoliths. Centrifugation was used as a tool to study the characteristics of the interaction between statoliths and microfilaments (MFs). Acropetal and basipetal accelerations up to 6.5 g were applied with the newly constructed slow-rotating-centrifuge-microscope (NIZEMI). Higher accelerations were applied by means of a conventional centrifuge, namely acropetally 10-200 g and basipetally 10-70 g. During acropetal accelerations (1.4-6g), statoliths were displaced to a new stable position nearer to the cell vertex (12-6.5 micrometers distance to the apical cell wall, respectively), but they did not sediment on the apical cell wall. The original position of the statoliths was reestablished within 30 s after centrifugation. Sedimentation of statoliths and reduction of the growth rates of the rhizoids were observed during acropetal accelerations higher than 50 g. When not only the amount but also the direction of the acceleration were changed in comparison to the natural condition, i.e., during basipetal accelerations (1.0-6.5 g), statoliths were displaced into the subapical zone (up to 90 micrometers distance to the apical cell wall); after 15-20 min the retransport of statoliths to the apex against the direction of acceleration started. Finally, the natural position in the tip was reestablished against the direction of continuous centrifugation. Retransport was observed during accelerations up to 70 g. Under the 1 g condition that followed the retransported statoliths showed an up to 5-fold increase in sedimentation time onto the lateral cell wall when placed horizontally. During basipetal centrifugations > or = 70 g all statoliths entered the basal vacuolar part of the rhizoid where they were cotransported in the streaming cytoplasm. It is concluded that the MF system is able to adapt to higher mass accelerations and that the MF system of the polarly growing rhizoid is polarly organized.

Acceleration↗
PubMed1991

Possible mechanisms of indirect gravity sensing by cells.

We have to distinguish between (a) direct gravisensing, in which specialized cells function as parts of a gravisensing organ and (b) indirect gravisensing, in which other cells that have no specialized gravity detectors are nevertheless affected by the inertial acceleration. In both cases, cells may detect (a) the direction of gravity ("up" versus "down"), and /or (b) the amplitude (0 - 1 g) of gravity. This chapter argues that the weight of single normal-sized cells (approximately 10 microns in diameter) is too small compared with other cellular forces to allow them the distinction between up and down. However, the weight of the surrounding medium is much larger. Cells may be able to sense certain environmental changes caused by gravity and thus may sense indirectly at least the amplitude of gravitational forces. In particular, the fluid environment of the cell can be expected at normal gravity to support microconvective currents that cease to flow at microgravity. Thus, the absence of gravity may be transduced into the accumulation of metabolites and ions from the cells and depletion of fresh nutrients. These changes, in turn, can affect the contacts of cells, their membrane potential, their cytoskeleton, and thus, ultimately, their behavior. As to ground-based simulations of microgravity, the above considerations suggest that the averaging of the vectorial force of gravity in clinorotation is inadequate for simulation because it may actually increase rather than suppress convective mixing above the normal levels.

Animals↗
PubMed1977

Light- and gravity-sensing guidance systems in plants.

The present state of our knowledge of phototropic and geotropic responses in plant organs is summarized, and an attempt made to identify aspects of these responses that might be studied advantageously in a 0 g environment. The paper aims to provide a background for non-specialists and to initiate critical discussion of the best ways to exploit the facilities provided by the Spacelab project in the study of plant guidance systems.

Avena↗
PubMed1997

Central root cap cells are depleted of endoplasmic microtubules and actin microfilament bundles: implications for their role as gravity-sensing statocytes.

Indirect immunofluorescence, using monoclonal antibodies to actin and tubulin, applied to sections of root tips of Lepidium, Lycopersicon, Phleum, and Zea, revealed features of the cytoskeleton that were unique to the statocytes of their root caps. Although the cortical microtubules (CMTs) lay in dense arrays against the periphery of the statocytes, these same cells showed depleted complements of endoplasmic microtubules (EMTs) and of actin microfilament (AMF) bundles, both of which are characteristic of the cytoskeleton of other post-mitotic cells in the proximal portion of the root apex. The scarcity of the usual cytosketetal components within the statocytes is considered responsible for the exclusion of the larger organelles (e.g., nucleus, plastids, ER elements) from the interior of the cell and for the absence of cytoplasmic streaming. Furthermore, the depletion of dense EMT networks and AMF bundles in statocyte cytoplasm is suggested as being closely related to the elevated cytoplasmic calcium content of these cells which, in turn, may also favour the formation of the large sedimentable amyloplasts by not permitting plastid divisions. These latter organelles are proposed to act as statoliths due to their dynamic interactions with very fine and highly unstable AMFs which enmesh the statoliths and merge into peripheral AMFs-CMTs-ER-plasma membrane complexes. Rather indirect evidence for these interactions was provided by showing enhanced rates of statolith sedimentation after chemically-induced disintegration of CMTs. All these unique properties of the root cap statocytes are supposed to effectively enhance the gravity-perceptive function of these highly specialized cells.

Actin Cytoskeleton↗
PubMed2004

Mechanotransduction in root gravity sensing cells.

The analysis of the dose-response curve of the gravitropic reaction of lentil seedling roots has shown that these organs are more sensitive when they have been grown in microgravity than when they have been grown on a 1 g centrifuge in space before gravistimulation. This difference of gravisensitivity is not due to the volume or the density of starch grains of statoliths, which are about the same in both conditions (1 g or microgravity). However, the distribution of statoliths within the statocyte may be responsible for this differential sensitivity, since the dispersion of these organelles is greater in microgravity than in 1 g. When lentil roots grown in microgravity or in 1 g are stimulated at 0.93 g for 22 min, the amyloplasts sediment following two different trajectories. They move from the proximal half of the statocytes toward the lower longitudinal wall in the microgravity grown sample and from the distal half toward the longitudinal wall in the 1 g grown sample. At the end of the stimulation, they reach a similar position within the statocytes. If the roots of both samples are left in microgravity for 3 h, the amyloplasts move toward the cell centre in a direction that makes an average angle of 40 degrees with respect to the lower longitudinal wall. The actin filaments, which are responsible for this movement, may have an overall orientation of 40 degrees with respect to this wall. Thus, when roots grown in microgravity are stimulated on the minicentrifuge the amyloplasts slide on the actin filaments, whereas they move perpendicular to them in 1 g grown roots. Our results suggest that greater sensitivity of seedling roots grown in microgravity should be due to greater dispersion of statoliths, to better contacts between statoliths and the actin network and to greater number of activated mechanoreceptors. One can hypothesize that stretch activated ion channels (SACs) located in the plasma membrane are responsible for the transduction of gravistimulus. These SACs may be connected together by elements of the cytoskeleton lining the plasma membrane and to the actin filaments. They could be stimulated by the action of statoliths on the actin network and/or on these elements of the cytoskeleton which link the mechanoreceptors (SACs).

Actins↗
PubMed2003

Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana.

Plants must sense and respond to diverse stimuli to optimize the architecture of their root system for water and nutrient scavenging and anchorage. We have therefore analyzed how information from two of these stimuli, touch and gravity, are integrated to direct root growth. In Arabidopsis thaliana, touch stimulation provided by a glass barrier placed across the direction of growth caused the root to form a step-like growth habit with bends forming in the central and later the distal elongation zones. This response led to the main root axis growing parallel to, but not touching the obstacle, whilst the root cap maintained contact with the barrier. Removal of the graviperceptive columella cells of the root cap using laser ablation reduced the bending response of the distal elongation zone. Similarly, although the roots of the gravisensing impaired pgm1-1 mutant grew along the barrier at the same average angle as wild-type, this angle became more variable with time. These observations imply a constant gravitropic re-setting of the root tip response to touch stimulation from the barrier. In wild-type plants, transient touch stimulation of root cap cells, but not other regions of the root, inhibited both subsequent gravitropic growth and amyloplast sedimentation in the columella. Taken together, these results suggest that the cells of the root cap sense touch stimuli and their subsequent signaling acts on the columella cells to modulate their graviresponse. This interaction of touch and gravity signaling would then direct root growth to avoid obstacles in the soil while generally maintaining downward growth.

Arabidopsis↗