Growth distribution during first positive phototropic curvature of maize coleoptiles*

Abastract Measurements of growth increments on the shaded and the irradiated sides of phototropically stimulated maize (Zea mays L.) coleoptiles, obtained over the entire fluence range of the first positive curvature, indicate that the curvature is induced by growth stimulation on the shaded side and compensating inhibition on the irradiated side (length increments on the coleoptile flanks were determined 100 min after 30 s phototropic induction with blue light). At high fluences of blue light, overall stimulation of growth takes place, but this tendency is largely eliminated when only the tip of the coleoptile is irradiated. Time courses for growth increments obtained for the maximum first positive response show that the growth stimulation on the shaded side and the growth inhibition on the irradiated side commence almost simultaneously 20-30 min after the phototropic induction. The growth on the irradiated side almost ceases, but the growth rate on the shaded side is doubled, relative to the control rate. The onset of differential growth migrates basipetally from the tip at a velocity similar to that for polar auxin transport. The first positive phototropic response of the coleoptile is concluded to be the consequence of lateral redistribution of growth, which is not necessarily accompanied by changes in the net growth. The results are consonant with the Cholodny-Went theory of tropisms, in which lateral redistribution of auxin is considered to be the cause of tropic responses.     

The role of the apex in the phototropic curvature of Avena coleoptiles: positive curvature under conditions of continuous illumination

The differential growth causing second positive phototropic curvature in intact, black-capped and decapitated Avena coleoptiles has been measured. In all cases the curvature is brought about by a cessation in growth of the illuminated side. The fact that shading the apex does not significantly alter the initial steps of differential growth means that the subapical zones can perceive and respond to unilateral illumination. Decapitation significantly reduces coleoptile growth, especially in the most apical zone. However, the fact that differential growth is still evident in the other zones of decapitated coleoptiles within 30 min of unilateral illumination requires one to conclude that the apex cannot be controlling the differential growth in those basal zones.     

Transport of Indole-3-Acetic Acid during Gravitropism in Intact Maize Coleoptiles

We have investigated the transport of tritiated indole-3-acetic acid (IAA) in intact, red light-grown maize (Zea mays) coleoptiles during gravitropic induction and the subsequent development of curvature. This auxin is transported down the length of gravistimulated coleoptiles at a rate comparable to that in normal, upright plants. Transport is initially symmetrical across the coleoptile, but between 30 and 40 minutes after plants are turned horizontal a lateral redistribution of the IAA already present in the transport stream occurs. By 60 minutes after the beginning of the gravitropic stimulus, the ratio of tritiated tracer auxin in the lower half with respect to the upper half is approximately 2:1. The redistribution of growth that causes gravitropic curvature follows the IAA redistribution by 5 or 10 minutes at the minimum in most regions of the coleoptile. Immobilization of tracer auxin from the transport stream during gravitropism was not detectable in the most apical 10 millimeters. Previous reports have shown that in intact, red light-grown maize coleoptiles, endogenous auxin is limiting for growth, the tissue is linearly responsive to linearly increasing concentrations of small amounts of added auxin, and the lag time for the stimulation of straight growth by added IAA is approximately 8 or 9 minutes (TI Baskin, M Iino, PB Green, WR Briggs [1985] Plant Cell Environ 8: 595-603; TI Baskin, WR Briggs, M Iino [1986] Plant Physiol 81: 306-309). We conclude that redistribution of IAA in the transport stream occurs in maize coleoptiles during gravitropism, and is sufficient in degree and timing to be the immediate cause of gravitropic curvature.     

Gravitropic Responses of Partially Decapitated Corn Coleoptiles with and without Applied [C]Indoleacetic Acid

The curvature of corn seedling (Zea mays L. Mo17 × B73) coleoptiles which had been half-decapitated and supplied with [¹⁴C]indoleacetic acid (IAA) (3.2 micromolar, 51 milliCuries per millimole) was determined during a 3-hour period of gravitational stimulation. Curvature of such half-decapitated coleoptiles was found to be similar in rate and extent to that of intact coleoptiles responding to gravity. Gravitational stimulation was accomplished by reorienting seedlings to a horizontal position, either up or down with respect to the removed half of the coleoptile tips.

The first set of experiments involved placing aluminum foil barriers along one of the two cut surfaces to restrict the movement of IAA into tissues. The initiation and extent of curvature of these half-decapitated coleoptiles was dependent upon the orientation of the removed half-tip and the accompanying barrier. The distribution of radioactivity from [¹⁴C] IAA after 3 hours indicated that the specific lateral movement of label was also dependent upon orientation of the removed half-tip of the coleoptile. A specific movement to the lower side of approximately 14% of the total recovered radioactivity was found in coleoptiles in which the [¹⁴C]IAA was supplied across a transverse cut surface. In contrast, specific movement of only 4% was found for application across a longitudinal cut surface.

A second series of experiments was conducted using 1.0 and 3.2 micromolar [¹⁴C]IAA (51 milliCuries per millimole) supplied to half-decapitated coleoptiles without inserted barriers. The 3.2 micromolar concentration adequately replaced the removed coleoptile half-tips in terms of straight growth, but it did not result in as much curvature as shown by coleoptiles of intact seedlings. The 1 micromolar concentration was not adequate to replace the removed half-tip in straight growth, but resulted in gravitropic curvature nearly as great as that produced by the higher concentration.

The data presented here suggest that strong auxin gradients are not produced in response to gravity stimulation based on the recovered radioactivity from [¹⁴C]IAA. However, it is evident that auxin is required for the development of normal gravitropic responses. It is possible, therefore, that an important early role of this movement is not to cause a large stimulation of growth on the lower side but to decrease growth on the upper side of a gravitropically responding coleoptile.

     

The Geoelectric Effect in Plant Shoots:: IV. INTER-RELATIONSHIP BETWEEN GROWTH, AUXIN CONCENTRATION AND ELECTRICAL POTENTIALS IN ZEA COLEOPTILES

Incubation of Zea coleoptiles in 0.5 M mannitol totally inhibitsgrowth and geotropic curvature, but does not affect the developmentof the geoelectric effect. This pre-treatment also inhibitsthe curvature induced by the asymmetrical application of IAAto the apical end of decapitated vertical coleoptiles, but itdoes not prevent the IAA from giving rise to an electropotentialdifference between the two sides of the coleoptile. Neitherthe normal geoelectric effect, nor the auxin-induced potentialdifference in vertical coleoptiles, can therefore arise as theresult of the different rates of cell extension in the two halvesof the organ. They must be the result of the change of IAA concentrationaffecting some other aspect of the cell's physiology or metabolism. The abolition of the electrical responses in coleoptiles whichhave been plasmolysed in 1.0 M mannitol strongly suggests thatboth longitudinal and lateral transport of IAA are severelydepressed by this degree of plasmolysis. Asymmetrical application of 10^-5 M mersalyl and several othersubstances to the apical end of a decapitated vertical coleoptilegave rise to a marked electropotential difference between thetwo sides of the coleoptile, the side beneath the donor beingpositively charged with respect to the other side. Mersalyldoes not promote the growth of Zea coleoptiles. These resultsprovide additional evidence that the electropotentials do notarise from differential growth, and suggest that such substances,especially the diuretics used in clinical medicine, may provideuseful tools in the further study of the induction of surfaceelectropotentials in plant tissues at the cellular level.     

Can Lateral Redistribution of Auxin Account for Phototropism of Maize Coleoptiles?

Elongation growth of intact, red-light grown maize (Zea mays L.) coleoptiles was studied by applying a small spot of an indole acetic acid (IAA)-lanolin mixture to the coleoptile tip. We report that: (a) endogenous auxin is limiting for growth, (b) an approximately linear relation holds between auxin concentration and growth rate over a range which spans those rates occurring in phototropism, and (c) an auxin gradient established at the coleoptile tip is well sustained during its basipetal transport. We argue that the growth differential underlying coleoptile phototropism (first-positive curvature) can be explained by redistribution of auxin at the coleoptile tip.     

Distribution of Endogenous Indole-3-acetic Acid and Growth Inhibitor(s) in Phototropically Responding Oat Coleoptiles

The relationship between the flank growth of oat (Avena sativaL. cv. Victory) coleoptiles and the distribution of endogenousindole-3-acetic acid (IAA) and growth inhibitor(s) in the coleoptileswas studied for the second positive phototropic curvature inducedby a continuous unilateral illumination with white light (0.1W.m^–2). The phototropic curvature was caused by growthinhibition at the lighted side and growth promotion at the shadedside. Using electron capture detection gas chromatography, weanalyzed the distribution of endogenous IAA in phototropicallyresponding oat coleoptiles and found that the IAA was evenlydistributed over the lighted and shaded sides during the phototropicresponse; there was also no detectable difference in the amountsof IAA between phototropically stimulated and non-irradiatedcoleoptiles. By contrast, oat coleoptile straight-growth testresults showed that the amount of unknown acidic growth inhibitor(s),different from abscisic acid, increased in the lighted halfof the coleoptiles and decreased in the shaded half, as comparedto the amount in the non-irradiated half. These data suggestthat the phototropic curvature of oat coleoptile is inducedby a difference in lateral flank growth through a lateral gradientof endogenous growth inhibitor(s) rather than of IAA. (Received February 10, 1988; Accepted July 29, 1988)     

Effects of submergence on development and gravitropism in the coleoptile of Oryza sativa L.

Caryopses of rice (Oryza sativa L. cv. Sasanishiki) were germinated in air or under water. In submerged seedlings a twofold increase in coleoptile growth rate and an inhibition of root growth was observed. The amount of starch in the amyloplasts of submerged coleoptiles was substantially reduced compared to the air-grown control plants and plastids had a proplastidic character. During the rapid elongation of coleoptiles under water, the osmotic concentration of the press sap remained constant, whereas in air-grown coleoptiles a decrease was measured. Determination of curvature of gravistimulated air-grown and submerged shoots was carried out by placing the coleoptiles horizontally in air of 98% relative humidity. Air-grown coleoptiles reached a vertical orientation within 5 h after onset of gravistimulation. In coleoptiles germinated under water the first signs of consistent negative gravitropic bending occurred after 4–5 h and curvature was complete after 24 h. During the first 5 h of gravistimulation the water-grown coleoptiles grew at an average rate of 0.39 mm·h^–1, whereas in air-grown coleoptiles a rate of 0.27 mm·h^–1 was measured. Concomitant with the delayed onset of gravitropic bending of the water-grown coleoptiles, a change in plastid ultrastructure and an increase in starch content was observed. We conclude that the gravitropic responsiveness of the rice coleoptile depends on the presence of starch-filled amyloplasts.We wish to thank H.-J. Ensikat for technical assistance with the scanning electron microscopy. Supported by the Bundesminister für Forschung und Technologie and the Deutsche Forschungsgemeinschaft.     

Uridine and the Control of Phototropism in Oat (Avena sativa L.) Coleoptiles

The short-term growth response of oat (Avena sativa L.) coleoptiles to exogenously applied uridine was studied both in excised apical segments and in the intact seedlings. In both cases growth of coleoptile tissue was inhibited by uridine. The inhibition of coleoptile growth consistently occurred 20–30 min after uridine treatment, which is within the lag period of their phototropic response. Asymmetric application of uridine to coleoptiles in the intact seedlings resulted in their bending toward the direction to which uridine was applied in the absence of light stimulus. These findings suggest that uridine or its metabolites, plays an important role in the phototropism of oat coleoptiles and provide support to the Bruinsma–Hasegawa theory as an alternative to the Cholodny–Went theory for explaining phototropism.     

Automorphosis of maize shoots under simulated microgravity on a three-dimensional clinostat

Seedlings of maize ( Zea mays L. cv. Golden Cross Bantam T-51) were grown under microgravity conditions simulated by a three-dimensional clinostat. On the clinostat, maize shoots exhibited curvatures in three different portions: (1) the basal transition zone connecting roots and mesocotyls, (2) the coleoptile node located between mesocotyls and coleoptiles, and (3) the elongating region of the coleoptiles. Even non-clinostatted control shoots showed some degree of curvature away from the caryopsis in the transition zone and bending toward the caryopsis in the coleoptile node. Clinostat rotation greatly stimulated these curvatures. Control coleoptiles elongated almost straightly, whereas coleoptiles on the clinostat bent either away from or toward the caryopsis depending on the timing of rotation. The curvature in all three portions became larger with time, both in control and clinostatted seedlings. There was no difference in the osmotic concentration of the cell sap between the convex and the concave halves of any portion. However, in coleoptile nodes and coleoptiles, the faster-expanding convex side exhibited a higher extensibility of the cell wall than the opposite side, and this appears to be a cause of the curvature. Thus, changes in the cell wall metabolism may be involved in automorphosis, which governs the life cycle of plants under a microgravity environment.     

Lateral redistribution of auxin is not the means for gravitropic differential growth of coleoptiles: A new model

Gravicurvature in water- and auxin (IAA)-incubated coleoptiles of rye ( Secale cereale L.) is similar, despite a general strongly enhancing effect of exogenous IAA on the overall (cell) elongation of these organs. Longitudinally split coleoptiles or isolated longitudinally halved coleoptiles (horizontally positioned as upper or lower halves) respond gravitropically in the same way as water-incubated intact coleoptiles, irrespective of whether the halves are incubated in distilled water or IAA. A new model for the principal mechanism of regulation of gravitropic growth is proposed which depends on, yet does not involve, the redistribution of IAA as the means for gravistimulated differential growth, as postulated by the Cholodny-Went hypothesis (CWH). It is based on a gravimediated temporarily restrained infiltration of IAA-induced wall-loosening factors into the growth-limiting outer epidermal walls of the concave organ flank.     

Unequal distribution of osmiophilic particles in the epidermal periplasmic space of upper and lower flanks of gravi-responding rye coleoptiles

In various studies, auxin (IAA)-induced coleoptile growth has been reported to be closely correlated with an increased occurrence of osmiophilic particles (OPs) at the inner surface of the outer, growth-limiting epidermal cell wall, indicating a possible function related to the mechanism of IAA-induced wall loosening. In order to test whether changes in cell elongation rates of upper and lower flanks (UFs, LFs, respectively) during graviresponsive growth are reflected in appropriate changes in the occurrence of OPs, rye (Secale cereale L.) coleoptiles either as segments or as part of intact seedlings, were gravitropically stimulated by positioning them horizontally for 2 h. Ultrastructural analyses within the UFs and LFs of the upward-bending coleoptiles revealed a distinct imbalance in the occurrence of OPs. The number of OPs per transverse epidermal cell section of the elongation-inhibited UF on average amounted to twice the number of OPs counted in epidermal cell sections of the faster-growing LF. As a hypothesis, the results lead us to suggest that OPs are involved in the mechanism of wall loosening and that temporary growth inhibition of epidermal cells of the UF during upward bending is mediated by inhibition of OP entry into the cell walls. Thereby, more OPs accumulate near the inner surface of the outer wall of epidermal cells of the UF compared with the LF.     

Changes in ion fluxes during phototropic bending of etiolated oat coleoptiles

BACKGROUND AND AIMS: This work has been conducted to assist theoretical modelling of the different stages of the blue light (BL)-induced phototropic signalling pathway and ion transport activity across plant membranes. Ion fluxes (Ca(2+), H(+), K(+) and Cl(-)) in etiolated oat coleoptiles have been measured continuously before and during unilateral BL exposure. METHODS: Changes in ion fluxes at the illuminated (light) and shadowed (dark) sides of etiolated oat coleoptiles (Avena sativa) were studied using a non-invasive ion-selective microelectrode technique (MIFE). The bending response was also measured continuously, and correlations between the changes in various ion fluxes and bending response have been investigated. For each ion the difference (Delta) between the magnitudes of flux at the light and dark sides of the coleoptile was calculated. KEY RESULTS: Plants that demonstrated a phototropic bending response also demonstrated Ca(2+) influx into the light side approximately 20 min after the start of BL exposure. This is regarded as part of the perception and transduction stages of the BL-induced signal cascade. The first 10 min of bending were associated with substantial influx of H(+), K(+) and Cl(-) into the light (concave) side of the coleoptiles. CONCLUSIONS: The data suggest that Ca(2+) participates in the signalling stage of the BL-induced phototropism, whereas the phototropic bending response is linked to changes in the transport of H(+), K(+) and Cl(-).     

Nuclear magnetic resonance imaging in studies of gravitropism in soil mixtures

Gravitropic responses of oat coleoptiles were measured in different growth media; humid air, natural soil and artificial soil (glass beads). The oat coleoptiles in soil and glass beads were monitored by NMR imaging, while those in humid air were imaged in darkness with an infrared-sensitive charge-coupled device (CCD) camera. The present study shows for the first time that gravitropic experiments can be performed in artificial soil using NMR imaging as a convenient and suitable recording method. Not only was it possible to follow the gravitropic curvatures in natural soil, but the artificial soil allowed plant images of sufficient spatial and temporal resolution to be recorded. The advantages of using artificial soil in magnetic resonance imaging studies are that the iron content of glass beads is very low compared with natural soil, and that the artificial soil matrix can easily be standardized with regard to particle size distribution and nutrient content. Two types of glass beads were used, the diameter of the small and the large beads being 300–400 and 420–840 μm, respectively. The growth rate of the coleoptiles in soil and in big beads was roughly the same and only slightly lower than in humid air, whereas small beads reduced the growth rate by approx. 16%. The bending rate of the coleoptiles during the gravitropic response was reduced by c. 65% in soil and 75% in bead mixtures relative to bending in air. It should be noted, however, that the maximum curvature of the coleoptile tip was of the same order in all cases, about 35°. This value may represent the largest possible curvature of the organ. The potential of NMR imaging to study how plant organs penetrate the soil under the influence of gravitropism, mechanical impedance and thigmotropism is also discussed.     

Distribution of Calcium, Potassium and Phosphorus in Helianthus annuus Hypocotyls and Zea mays Coleoptiles in Relation to Tropic Stimuli and Curvatures

Studies have been made of the distribution of ⁴⁵Ca, ⁴²K, totalK⁺ and ³²P between the concave and convex sides of segmentsof hypocotyl of Helianthus annuus and coleoptiles of Zea maysduring curvatures induced by gravity, unilateral illuminationor unilateral applications of indol-3yl acetic acid (IAA). Theelements were fed to the roots of seedlings for a 3–4h pretreatment period. Distributions in segments in intact seedlingswere compared with those in explanted segments deprived of acontinuing supply of the element concerned in order to separatepossible differential transport of the element from the rootsfrom any real movement across the organ from side to side. Withall three treatments, and in both explants and intact plants,⁴⁵Ca concentrations (on both fwt and dwt bases) were higheron the convex side. There was evidence of differential transportto the two sides and also of a direct movement across the parenchymafrom one side to the other. In organs where curvature was inhibitedby low temperatures (4 °C in geotropic experiments) or bythe antitropistic agent, N-1-naphthylphthalamic acid, no concentrationdifferences arose between the two sides. After the tropic stimulithe onset of the concentration differences preceded the onsetof curvature significantly, indicating that those differenceswere not caused by differential growth of the organ. The diuretic,mersalyl, applied unilaterally produced differences in elementconcentration of the same order and kind as similar treatmentwith IAA, but caused no growth curvatures. It is concluded that the movement of elements in tropicallycurving tissues, although apparently obligately-linked withcurvature, is not the result of that curvature or its cause,but is in some as yet undefined way an outcome of auxin gradientsin the tissue.     

NPH3- and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles

Phototropic curvature results from differential growth on two sides of the elongating shoot, which is explained by asymmetrical indole-3-acetic acid (IAA) distribution. Using 2 cm maize coleoptile segments, 1st positive phototropic curvature was confirmed here after 8 s irradiation with unilateral blue light (0.33 μmol m(-2) s(-1)). IAA was redistributed asymmetrically by approximately 20 min after photo-stimulation. This asymmetric distribution was initiated in the top 0-3 mm region and was then transmitted to lower regions. Application of the IAA transport inhibitor, 1-N-naphthylphthalamic acid (NPA), to the top 2 mm region completely inhibited phototropic curvature, even when auxin was simultaneously applied below the NPA-treated zone. Thus, lateral IAA movement occurred only within the top 0-3 mm region after photo-stimulation. Localized irradiation experiments indicated that the photo-stimulus was perceived in the apical 2 mm region. The results suggest that this region harbours key components responsible for photo-sensing and lateral IAA transport. In the present study, it was found that the NPH3- and PGP-like genes were exclusively expressed in the 0-2 mm region of the tip, whereas PHOT1 and ZmPIN1a, b, and c were expressed relatively evenly along the coleoptile, and ZmAUX1, ZMK1, and ZmSAURE2 were strongly expressed in the elongation zone. These results suggest that the NPH3-like and PGP-like gene products have a key role in photo-signal transduction and regulation of the direction of auxin transport after blue light perception by phot1 at the very tip region of maize coleoptiles.     

Correlation between cell wall extensibility and the content of diferulic and ferulic acids in cell walls of Oryza sativa coleoptiles grown under water and in air

Rice ( Oryza sativa L. cv. Sasanishiki) coleoptiles grown under water achieved greater length than those grown either in air or under water with constant air bubbling. The extensibility of cell walls in coleoptiles grown under water was larger than that in the other treatments. Per unit length of the coleoptile, the content of ferulic and diferulic acids ester-linked to hemicelluloses was higher in air and bubbling type coleoptiles than in water type ones. The extensibility of the coleoptile cell walls correlated with the content of diferulic acids per unit length and per hemicellulose, suggesting that the enhancement of the formation of diferulic acid bridges in hemicelluloses in air or under water with air bubbling makes the cell walls mechanically rigid; thereby inhibiting cell elongation in rice coleoptiles. In addition, the ratio of diferulic acid to ferulic acid was almost constant irrespective of coleoptile age, zone and growth conditions, suggesting that the feruloylation of hemicelluloses is rate-limiting in the formation of diferulic acid bridges in the cell walls of rice coleoptiles.     

The Rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin

We isolated a mutant, named coleoptile phototropism1 (cpt1), from gamma-ray-mutagenized japonica-type rice (Oryza sativa). This mutant showed no coleoptile phototropism and severely reduced root phototropism after continuous stimulation. A map-based cloning strategy and transgenic complementation test were applied to demonstrate that a NPH3-like gene deleted in the mutant corresponds to CPT1. Phylogenetic analysis of putative CPT1 homologs of rice and related proteins indicated that CPT1 has an orthologous relationship with Arabidopsis thaliana NPH3. These results, along with those for Arabidopsis, demonstrate that NPH3/CPT1 is a key signal transduction component of higher plant phototropism. In an extended study with the cpt1 mutant, it was found that phototropic differential growth is accompanied by a CPT1-independent inhibition of net growth. Kinetic investigation further indicated that a small phototropism occurs in cpt1 coleoptiles. This response, induced only transiently, was thought to be caused by the CPT1-independent growth inhibition. The 3H-indole-3-acetic acid applied to the coleoptile tip was asymmetrically distributed between the two sides of phototropically responding coleoptiles. However, no asymmetry was induced in cpt1 coleoptiles, indicating that lateral translocation of auxin occurs downstream of CPT1. It is concluded that the CPT1-dependent major phototropism of coleoptiles is achieved by lateral auxin translocation and subsequent growth redistribution.     

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.