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PubMed2003

Perception mechanism of gravity stimuli in hypergravity-induced growth inhibition of azuki bean roots.

We reported that elongation growth of plant shoots and roots is suppressed by hypergravity, with the rate decreasing in proportion to logarithm of the magnitude of gravity. In hypergravity-induced growth inhibition of shoots, graviperception is supposed to be independent of that in gravitropism and to involve mechanoreceptors. However, the graviperception mechanism in the hypergravity-induced growth inhibition of roots is not known. In the present study, we compared the mechanism in the hypergravity-induced growth inhibition of roots with that in gravitropism. The removal of root cap did not influence hypergravity-induced growth inhibition of roots, although the gravitropic curvature was completely inhibited. Hypergravity had no effects on growth of azuki bean roots in the presence of lanthanum or gadolinium, which are blockers of mechanoreceptors. On the contrary, lanthanum or gadolinium at the same concentration did not influence gravitropism of roots. These results suggest that the graviperception mechanism in the hypergravity-induced growth inhibition of roots is independent of that in gravitropism. Hypergravity-induced growth inhibition of azuki bean roots was observed irrespective of the direction of stimuli, which disappeared in the presence of lanthanum or gadolinium. Thus, in the hypergravity-induced growth inhibition, roots may perceive the gravity signal by mechanoreceptors on the plasma membrane independently of the direction of stimuli, and may utilize it to regulate their growth rate.

Fabaceae↗
PubMed1989

Differential growth and hormone redistribution in gravireacting maize roots.

When growing roots are placed in a horizontal position gravity induces a positive curvature. It is classically considered to be the consequence of a faster elongation rate by the upper side compared to the lower side. A critical examination indicates that the gravireaction is caused by differential cell extension depending on several processes. Some of the endogenous regulators which may control the growth and gravitropism of elongating roots are briefly presented. The growth inhibitors produced or released from the root cap move preferentially in a basipetal direction and accumulate in the lower side of the elongation zone of horizontally maintained roots. The identity of these compounds is far from clear, but one of these inhibitors could be abscisic acid (ABA). However, indol-3y1 acetic acid (IAA) is also important for root growth and gravitropism. ABA may interact with IAA. Two other aspects of root cell extension have also to be carefully considered. An elongation gradient measured from the tip to the base of the root was found to be important for the growth of both vertical and horizontal gravireactive roots. It was changed significantly during the gravipresentation and can be considered as the origin of the differential elongation. Sephadex beads have been used as both growth markers and as monitors of surface pH changes when they contain some pH indicator. This technique has shown that the distribution of cell extension along the main root axis is related to a pH gradient, the proton efflux being larger for faster growing parts of roots. A lateral movement of calcium is obtained when Ca2+ is applied across the tips of horizontally placed roots with a preferential transport towards the lower side. Endogenous calcium, which may accumulate inside the endoplasmic reticulum of some cap cells, may also act in the gravireception. These observations and several others strongly suggest that calcium may play an essential role in controlling root growth and several steps of the root gravireaction.

Abscisic Acid↗
PubMed2003

Physiological and genetic characterization of hydrotropic mutants of Arabidopsis thaliana.

Roots display positive hydrotropism in response to moisture gradient. Hydrotropism regulates the directional growth by interaction with other growth movements. Using the seedlings of pea, cucumber, maize and wheat, we have revealed that the root cap perceives the moisture gradient and that auxin and calcium are involved in hydrotropism. However, molecular mechanisms for stimulus perception or signal transduction in hydrotropism are still remained unrevealed. To dissect the molecular mechanism underlying hydrotropism in seedling roots, we established a method for screening Arabidopsis mutants defective in root hydrotropism. Among about 20,000 M2 seedlings of Arabidopsis plants treated with EMS, we successfully obtained 12 mutants of which root hydrotropism was reduced to various extents. We named them root hydrotropism (rhy) and examined their gravitropism, phototropism, waving response and elongation growth as well as hydrotropism in roots. Roots of rhy1 mutant showed ahydrotropic response although the other responses and elongation growth of rhy1 mutant were normal. Roots of rhy2 and rhy3 mutants showed a reduced hydrotropism and abnormal responses in gravitropism, phototropism or waving pattern. Genetic analysis of the progeny produced by the backcross of rhy1 mutant to wild type suggested that rhy1 was a recessive mutation. We also examined the map position of the rhy1 locus.

Arabidopsis↗
PubMed1993

Organization of cortical microtubules in graviresponding maize roots.

Immunofluorescence labeling of cortical microtubules (MTs) was used to investigate the relationship between MT arrangement and changes in growth rate of the upper and lower sides of horizontally placed roots of maize (Zea mays L. cv. Merit). Cap cells and cells of the elongation zone of roots grown vertically in light or darkness showed MT arrangements that were transverse (perpendicular) to the growth direction. Microtubules of cells basal to the elongation zone typically showed oblique orientation. Two hours after horizontal reorientation, cap cells of gravicompetent, light-grown and curving roots contained MTs parallel to the gravity vector. The MT arrangement on the upper side of the elongation zone remained transverse but the MTs of the outer four to five layers of cortical cells along the lower side of the elongation zone showed reorientation parallel to the axis of the root. The MTs of the lower epidermis retained their transverse orientation. Dark-grown roots did not curve and did not show reorientation of MTs in cells of the root cap or elongation zone. The data indicate that MT depolymerization and reorientation is correlated with reduction in growth rate, and that MT reorientation is one of the steps of growth control of graviresponding roots.

Darkness↗
PubMed1998

Automorphosis of higher plants on a 3-D clinostat.

On a three-dimensional (3-D) clinostat, various plant organs developed statocytes capable of responding to the gravity vector. The graviresponse of primary roots of garden cress and maize grown on the clinostat was the same as the control roots, whereas that of maize coleoptiles was reduced. When maize seedlings were grown in the presence of 10(-4) M gibberellic acid and kinetin, the graviresponse of both roots and shoots was suppressed. The corresponding suppression of amyloplast development was observed in the clinostatted and the hormone-treated seedlings. Maize roots and shoots showed spontaneous curvatures in different portions on the 3-D clinostat. The hormone treatment did not significantly influence such an automorphic curvature. When the root cap was removed, maize roots did not curve gravitropically. However, the removal suppressed the automorphic curvatures only slightly. On the other hand, the removal of coleoptile tip did not influence its graviresponse, whereas the spontaneous curvature of decapitated coleoptiles on the clinostat was strongly suppressed. Also, cytochalasin B differently affected the gravitropic and the automorphic curvatures of maize roots and shoots. From these results it is concluded that the graviperception and the early processes of signal transmission are unnecessary for automorphoses under simulated microgravity conditions. Moreover, the results support the view that the amyloplasts act as statoliths probably via an interaction with microfilaments.

Adenine↗
PubMed2002

The kinetics of root gravitropism: dual motors and sensors.

The Cholodny-Went theory of tropisms has served as a framework for investigation of root gravitropism for nearly three quarters of a century. Recent investigations using modern techniques have generated findings consistent with the classical theory, including confirmation of asymmetrical distribution of polar auxin transport carriers, molecular evidence for auxin asymmetry following gravistimulation, and generation of auxin response mutants with predictable lesions in gravitropism. Other results indicate that the classical model is inadequate to account for key features of root gravitropism. Initiation of curvature, for example, occurs outside the region of most rapid elongation and is driven by differential acceleration rather than differential inhibition of elongation. The evidence indicates that there are two motors driving root gravitropism, one of which appears not to be auxin regulated. We have recently developed technology that is capable of maintaining a constant angle of gravistimulation at any selected target region of a root while continuously monitoring growth and curvature kinetics. This review elaborates on the advantages of this new technology for analyzing gravitropism and describes applications of the technology that reveal (1) the existence of at least two phases to gravitropic motor output, even under conditions of constant stimulus input and (2) the existence of gravity sensing outside of the root cap. We propose a revised model of root gravitropism including dual sensors and dual motors interacting to accomplish root gravitropism, with only one of the systems linked to the classical Cholodny-Went theory.

Centrifugation↗
PubMed1994

Organelle sedimentation in gravitropic roots of Limnobium is restricted to the elongation zone.

Roots of the aquatic angiosperm Limnobium spongia (Bosc) Steud. were evaluated by light and electron microscopy to determine the distribution of organelle sedimentation towards gravity. Roots of Limnobium are strongly gravitropic. The rootcap consists of only two layers of cells. Although small amyloplasts are present in the central cap cells, no sedimentation of any organelle, including amyloplasts, was found. In contrast, both amyloplasts and nuclei sediment consistently and completely in cells of the elongation zone. Sedimentation occurs in one cell layer of the cortex just outside the endodermis. Sedimentation of both amyloplasts and nuclei begins in cells that are in their initial stages of elongation and persists at least to the level of the root where root hairs emerge. This is the first modern report of the presence of sedimentation away from, but not in, the rootcap. It shows that sedimentation in the rootcap is not necessary for gravitropic sensing in at least one angiosperm. If amyloplast sedimentation is responsible for gravitropic sensing, then the site of sensing in Limnobium roots is the elongation zone and not the rootcap. These data do not necessarily conflict with the hypothesis that sensing occurs in the cap in other roots, since Limnobium roots are exceptional in rootcap origin and structure, as well as in the distribution of organelle sedimentation. Similarly, if nuclear sedimentation is involved in gravitropic sensing, then nuclear mass would function in addition to, not instead of, that of amyloplasts.

Cell Nucleus↗
PubMed1990

Gravitropic curvature of maize roots is not preceded by rootcap asymmetry.

We tested whether the first response to gravistimulation is an asymmetry in the root tip that results from differential growth of the rootcap itself. The displacement of markers on the rootcap surface of maize (Zea mays L. cv. Merit) roots was quantified from videotaped images using customized software. The method was sensitive enough to detect marker displacements down to 15 microns and root curvature as early as 8 min after gravistimulation. No differential growth of the upper and lower sides of the cap occurred before or during root curvature. Fewer than a third of all gravistimulated roots developed an asymmetrical outline of the root tip after curvature had started, and this asymmetry did not occur in the rootcap itself. Our data support the view that the regions of gravitropic sensing and curvature are spatially separate during all phases of gravitropism in maize roots.

Gravitropism↗
PubMed1996

Patterns of auxin and abscisic acid movement in the tips of gravistimulated primary roots of maize.

Because both abscisic acid (ABA) and auxin (IAA) have been suggested as possible chemical mediators of differential growth during root gravitropism, we compared with redistribution of label from applied 3H-IAA and 3H-ABA during maize root gravitropism and examined the relative basipetal movement of 3H-IAA and 3H-ABA applied to the caps of vertical roots. Lateral movement of 3H-ABA across the tips of vertical roots was non-polar and about 2-fold greater than lateral movement of 3H-IAA (also non-polar). The greater movement of ABA was not due to enhanced uptake since the uptake of 3H-IAA was greater than that of 3H-ABA. Basipetal movement of label from 3H-IAA or 3H-ABA applied to the root cap was determined by measuring radioactivity in successive 1 mm sections behind the tip 90 minutes after application. ABA remained largely in the first mm (point of application) whereas IAA was concentrated in the region 2-4 mm from the tip with substantial levels found 7-8 mm from the tip. Pretreatment with inhibitors of polar auxin transport decreased both gravicurvature and the basipetal movement of IAA. When roots were placed horizontally, the movement of 3H-IAA from top to bottom across the cap was enhanced relative to movement from bottom to top whereas the pattern of movement of label from 3H-ABA was unaffected. These results are consistent with the hypothesis that IAA plays a role in root gravitropism but contrary to the idea that gravi-induced asymmetric distribution of ABA contributes to the response.

Abscisic Acid↗
PubMed1988

Effects of cations on hormone transport in primary roots of Zea mays.

We examined the influence of aluminum and calcium (and certain other cations) on hormone transport in corn roots. When aluminum was applied unilaterally to the caps of 15 mm apical root sections the roots curved strongly away from the aluminum. When aluminum was applied unilaterally to the cap and 3H-indole-3-acetic acid was applied to the basal cut surface twice as much radioactivity (assumed to be IAA) accumulated on the concave side of the curved root as on the convex side. Auxin transport in the apical region of intact roots was preferentially basipetal, with a polarity (basipetal transport divided by acropetal transport) of 6.3. In decapped 5 mm apical root segments, auxin transport was acropetally polar (polarity = 0.63). Application of aluminum to the root cap strongly promoted acropetal transport of auxin reducing polarity from 6.3 to 2.1. Application of calcium to the root cap enhanced basipetal movement of auxin, increasing polarity from 6.3 to 7.6. Application of the calcium chelator, ethylene-glycol-bis-(beta-aminoethylether)-N,N,N',N'-tetraacetic acid, greatly decreased basipetal auxin movement, reducing polarity from 6.3 to 3.7. Transport of label after application of tritiated abscisic acid showed no polarity and was not affected by calcium or aluminum. The results indicate that the root cap is particularly important in maintaining basipetal polarity of auxin transport in primary roots of corn. The induction of root curvature by unilateral application of aluminum or calcium to root caps is likely to result from localized effects of these ions on auxin transport. The findings are discussed relative to the possible role of calcium redistribution in the gravitropic curvature of roots and the possibility of calmodulin involvement in the action of calcium and aluminum on auxin transport.

Abscisic Acid↗
PubMed1985

Inhibition of gravitropism in primary roots of Zea mays by chloramphenicol.

Primary roots of Zea mays seedlings germinated and grown in 0.1 mM chloramphenicol (CMP) were significantly less graviresponsive than primary roots of seedlings germinated and grown in distilled water. Elongation rates of roots treated with CMP were significantly greater than those grown in distilled water. Caps of control and CMP-treated roots possessed extensive columella tissues comprised of cells containing numerous sedimented amyloplasts. These results indicate that the reduced graviresponsiveness of CMP-treated roots is not due to reduced rates of elongation, the absence of the presumed gravireceptors (i.e., amyloplasts in columella cells), or reduced amounts of columella tissue. These results are consistent with CMP altering the production and/or transport of effectors that mediate gravitropism.

Chloramphenicol↗
PubMed2001

Functional analysis of salt-inducible proline transporter of barley roots.

We cloned a cDNA encoding Hordeum vulgare Proline Transporter (HvProT) from salt-stressed barley roots by differential display. HvProT was 2,161 bp long and had an open reading frame encoding 450 amino acids. The deduced amino acid sequence of HvProT was similar to those of proline transporter proteins of rice (65.7%), Arabidopsis (57.7%) and tomato (42.0%). Northern blot analysis showed that the transcript level of HvProT was induced in roots at 30 min after 200 mM NaCl treatment and its peak was observed at 3 h. However, the transcript level was very low in leaves and did not increase by salt stress. The expression level of Delta(1)-pyrroline-5-carboxylate synthetase (P5CS), encoding a key enzyme of proline synthesis, was induced later than HvProT by salt stress. A transport assay using a yeast with mutation in proline uptake revealed that HvProT was a transporter with high affinity for L-proline (K(m) = 25 microM). HvProT was found to be a unique transporter with high affinity for L-proline. Since its transport activity was dependent on the pH gradient, HvProT was suggested to be a H(+)/amino acid symporter. In situ hybridization analysis showed that the HvProT mRNA was strongly expressed in root cap cells under salt stress. HvProT might play an important role in the transport of proline to root tip region urgently upon salt stress.

1-Pyrroline-5-Carboxylate Dehydrogenase↗
PubMed1985

Abscisic acid, xanthoxin and violaxanthin in the caps of gravistimulated maize roots.

The occurrence and distribution of abscisic acid (ABA), xanthoxin (Xa) and the carotenoid violaxanthin (Va) were investigated in root tips of maize (Zea mays L. cv. Merit). In roots grown in the dark, Va and ABA were present in relatively high amounts in the root cap and in low amounts in the adjacent terminal 1.5 mm of the root. Xanthoxin was present in equal concentrations in both regions. In roots exposed to light, the ABA distribution was reversed, with relatively low levels in the root cap and high levels in the adjacent 1.5-mm segment. Light also caused a decrease in Va in both regions of the root and an increase in Xa, especially in the cap. In the maize cultivar used for this work, light is necessary for gravitropic curving. This response occurs within the same time frame as the light-induced ABA redistribution as well as the changes in the levels of Va and Xa. These data are consistent with a role for ABA in root gravitropism and support the proposal that Xa may arise from the turnover of Va.

Abscisic Acid↗
PubMed2002

Basipetal propagation of gravity-induced surface pH changes along primary roots of Lepidium sativum L.

While there is ample evidence for a role of auxin in root gravitropism, the seeming rapidity of gravi-induced changes in electrical parameters has so far been an argument against auxin being a primary signal in gravitropic signal transmission. To address this problem, we re-investigated the effect of gravistimulation on membrane voltages of Lepidium sativum L. and Vigna mungo L. root cells. In our hands, gravistimulation did not induce changes in membrane voltage in cells of the root cap statenchyma, root meristem or apical elongation zone that can be correlated with the orientation of the cells relative to the gravity vector. While these results challenge a model of rapid electrically based signal transmission, there is evidence for a slower signal propagation along gravistimulated L. sativum roots. Using multiple proton-selective microelectrodes to simultaneously measure surface pH on opposite root flanks at different distances from the root tip, we observed gravi-induced asymmetric pH changes at the surface of all investigated root zones. Upon gravistimulation, the surface pH decreased on the physically upper root flank and increased on the lower flank. The pH asymmetry appeared first [2.1+/-0.4 min (mean +/- SD) after tilting] at the root cap and then - with incrementing lag times - at the meristem (after 2.5+/-0.3 min at 300 micro m from root tip; after 3.7+/-0.4 min at 700 micro m) and apical elongation zone (4.8+/-0.5 min at 1,000 micro m), suggesting a basipetal progression of differential surface acidification at a rate of 250-350 micro m min(-1), consistent with reported auxin transport rates.

Biological Transport↗
PubMed1985

Geoperception in primary and lateral roots of Phaseolus vulgaris (Fabaceae). III. A model to explain the differential georesponsiveness of primary and lateral roots.

Half-tipped primary and lateral roots of Phaseolus vulgaris bend toward the side of the root on which the intact half tip remains. Therefore, tips of lateral and primary roots produce growth effectors capable of inducing gravicurvature. The asymmetrical placement of a tip of a lateral root onto a detipped primary root results in the root bending toward the side of the root onto which the tip was placed. That is, the lesser graviresponsiveness of lateral roots as compared with primary roots is not due to the inability of their caps to produce growth inhibitors. The more pronounced graviresponsiveness of primary roots is positively correlated with the presence of columella tissues that are 3.8 times longer, 1.7 times wider, and 10.5 times more voluminous than the columellas of lateral roots. We propose that the lack of graviresponsiveness exhibited by lateral roots is due to the fact that they (i) produce smaller amounts of the inhibitor than primary (i.e., strongly graviresponsive) roots and (ii) are unable to redistribute the inhibitor so as to be able to create a concentration gradient sufficient to induce a pronounced gravitropic response.

Fabaceae↗
PubMed1996

Effects of gravitropic stress on the development of the primary root of lentil seedlings grown in space.

Root growth and cell differentiation were analysed in lentil seedlings grown (1) in microgravity (F microg), (2) on the 1 x g centrifuge (F1 x g), (3) in microgravity and placed on the 1 x g centrifuge for 4 h [F(microg + 1 x g)], (4) on the 1 x g centrifuge and placed in microgravity for 4 h [F(1 x g + microg)]. In microgravity, there were strong oscillations of the root tip, even when the seedlings were grown first on the 1 x g centrifuge [F(1 x g + microg)]. In the [F(microg + 1 x g)] sample, the roots grown in microgravity were oblique with respect to the 1 x g acceleration when the seedlings were placed on the centrifuge. They were therefore gravistimulated. However, root length was similar in the 4 samples after 29 h of growth and growth rate of the root was the same between 25 h and 29 h although it appeared to be slightly greater in the [F(microg + 1 x g)] sample. Cell elongation was analysed as a function of the distance from the root cap junction. Cell length was similar in the seedlings grown in microgravity or on the 1 x g centrifuge. The transfer from the 1 x g centrifuge to microgravity [F(1 x g + microg)] did not modify cell elongation in the roots. Cell length in the roots which were grown in microgravity and gravistimulated [F(microg + 1 x g)] was different from that observed in microgravity but this was only due to gravistimulation. Thus, gravity does not have an effect on cell elongation when the roots are strictly oriented in the vertical position but it does as soon as the root tip deviates from this orientation.

Centrifugation↗
PubMed2005

Mechanoreceptors rather than sedimentable amyloplasts perceive the gravity signal in hypergravity-induced inhibition of root growth in azuki bean.

Elongation of primary roots of azuki bean (Vigna angularis Ohwi et Ohashi) was suppressed under hypergravity conditions produced by centrifugation, such that the growth rate decreased in proportion to the logarithm of the magnitude of the gravity. The removal of the root cap did not influence the hypergravity-induced inhibition of root growth, although it completely inhibited the gravitropic root curvature. Lanthanum and gadolinium, blockers of mechanoreceptors, nullified the growth-inhibitory effect of hypergravity. These results suggest that the gravity signal for the hypergravity-induced inhibition of root growth is perceived independently from that of gravitropism, which involves amyloplasts as statoliths. Horizontal and basipetal hypergravity suppressed root growth as did acropetal hypergravity, all of which were nullified by the presence of lanthanum or gadolinium. These findings suggest that mechanoreceptors on the plasma membrane perceive the gravity signal independently of the direction of the stimuli and roots may utilise it to regulate their growth rate.

Centrifugation↗
PubMed1985

Calcium movement, graviresponsiveness and the structure of columella cells and columella tissues in roots of Allium cepa L.

Roots of Allium cepa L. cv. Yellow are differentially responsive to gravity. Long (e.g. 40 mm) roots are strongly graviresponsive, while short (c.g. 4 mm) roots are minimally responsive to gravity. Although columella cells of graviresponsive roots are larger than those of nongraviresponsive roots, they partition their volumes to cellular organelles similarly. The movement of amyloplasts and nuclei in columella cells of horizontally-oriented roots correlates positively with the onset of gravicurvature. Furthermore, there is no significant difference in the rates of organellar redistribution when graviresponsive and nongraviresponsive roots are oriented horizontally. The more pronounced graviresponsiveness of longer roots correlates positively with (1) their caps being 9-6 times more voluminous, (2) their columella tissues being 42 times more voluminous, (3) their caps having 15 times more columella cells, and (4) their columella tissues having relative volumes 4.4 times larger than those of shorter, nongraviresponsive roots. Graviresponsive roots that are oriented horizontally are characterized by a strongly polar movement of 45Ca2+ across the root tip from the upper to the lower side, while similarly oriented nongraviresponsive roots exhibit only a minimal polar transport of 45Ca2+. These results indicate that the differential graviresponsiveness of roots of A. cepa is probably not due to either (1) ultrastructural differences in their columella cells, (2) differences in the rates of organellar redistribution when roots are oriented horizontally. Rather, these results indicate the graviresponsiveness may require an extensive columella tissue, which, in turn, may be necessary for polar movement of 45Ca2+ across the root tip.

Biological Transport↗