Nutation rhythm of growing pine hypocotyl (Pinus silvestris L.) interferred with a phototropic stimulus

The interaction of nutation oscillation and phototropic curvature mechanisms of growing pine hypocotyl(Pinus silvestris L.) was investigated. Nutation parameters of growing hypocotyl are not affected by continuous lateral illumination. Frequency and nutation amplitudes undergo changes which are dependent on plant development and are nearly the same when plants are illuminated from one side or from above. Lateral illumination, however, induces a phase shift. This deviation from a normal nutation rhythm usually disappears after a period of time equal to three nutation revolutions,i.e. after 12 h. The positive phototropio response of nutating hypocotyl is dependent on the phase in which the hypocotyl is exposed to the lateral illumination:(a) nutation perihelium,(b) ahelium and(c) nutation interphase. These response-variants are compared with the expected gradients of plant hormones at the opposite sites of the hypocotyle. Analysis of location of the individual movement reactions(i.e. oscillations as a component of the geocontrol system and phototropic curvature) together with the determination of the zone of maximum elongation indicates the existence of different receptory centres of these two movement systems. In the case of the phototropic response reaction it is possible to consider the presence of different photo- and biochemical mechanisms at least for a part of this system.     

Elongation and circumnutation oscillations of hypocotyl of pine seedlings (Pinus silvestris L.)

The elongation of pine seedlings (Pinus silvestris L.) is associated with nutation movements. Trajectories of these growth oscillations were recorded by film technique in horizontal and vertical projection during a three day period of growth. On the basis of these data the parameters of elongation and nutation oscillations,i.e. rate, amplitudes and frequency of oscillations, were calculated and their changes during plant development compared. Oscillation trajectories are circular or elliptic spirals the amplitudes of which are increasing with the age of hypocotyl from 1.5 mm to 7.5 mm. The frequencies of nutations are decreasing during the growth from 0.5 to 0.2 rev. h^?1. On the other hand, the growth rate of hypocotyl increased from values near to 10^?3 mm h^?1 at the beginning of the experiment to 4×10^?1 mm h^?1 recorded at the end of the third day. The zone of nutation curvature was slightly transferred from the middle of the hypocotyl toward the apex and its location has not been identical with that of elongation. This indicates that the system controlling nutation oscillations need not be identical with that controlling direction of elongation. At a certain stage of development behaviour of the decapitated pine hypocotyl is analogical to that of the root without the centre of georeception. A possibility of analogy of the system controlling direction of hypocotyl growth and of the system proposed for geotropical control of root growth is discussed.     

Interactions of photo- and geotropism with periodical oscillations of growing pea root (Pisum sativum L.)

Oscillation movements of primary roots of pea seedlings were investigated after low- and high-energy irradiation (10^?2 and 10⁶ W m^?2) which was applied continuously and in pulses at intervals of 3 and 30 min. Oscillation amplitudes of control roots grown in darkness were lower (1 mm) than those of irradiated ones recorded in our previous experiments. The elongation rate of roots grown under scattered and low-energy irradiation as well as their mean oscillation amplitude (2.6 mm) and frequency (8 h) correspond to the standard values recorded in previous experiments. The same effects on root growth and oscillations had scattered electronic flash irradiation. Side-irradiation did not influence the oscillation movements of growing roots. Their frequency and oscillation amplitudes were not changed. Their longitudal axis was, however, deflected 2.75° from the vertical one due to the negative phototropic response of the root. The growth oscillations may be, according to present results, interpreted as consequences of tropic growth controlling system. External factors, like irradiation, may influence oscillation parameters,i.e. their amplitudes and after application of side-irradiation also the direction of longitudinal axis of oscillation spirals. The resultant trajectory is composed from movements which resulted from geotropic and phototropic responses of the roots.     

Red light enhancement of the phototropic response of etiolated pea stems

In the subapical third internode of 7-day-old etiolated pea seedlings, the magnitude of phototropic curvature in response to continuous unilateral blue illumination is increased when seedlings are pre-exposed to brief red light. The effect of red light on blue light-induced phototropism becomes manifest maximally 4 or more hours after red illumination, and closely parallels the promotive action of red light on the elongation of the subapical cells. Ethylene inhibits phototropic curvature by an inhibitory action on cell elongation without affecting the lateral transport of auxin. Pretreatment of seedlings with gibberellic acid causes increased phototropic curvature, but experiments using ¹⁴C-gibberellic acid indicate that gibberellic acid itself is not laterally transported under phototropic stimuli. Neither red light nor gibberellic acid treatment has any promotive effect on blue light-induced lateral transport of ³H-indoleacetic acid. Under conditions where phototropic curvature is increased by red light treatment, low concentrations of indoleacetic acid applied in lanolin paste to the apical cut end of the seedling cause an increased elongation response in subapical tissue. This could explain increased phototropic curvature caused by red light treatment.     

Diurnal oscillatory movements of growing leaves of tobacco

The analysis of diurnal oscillatory movements of tobacco leaves was used in the diagnosis of viral infection of plants. The oscillatory helices circumscribed by a growing leaf of a healthy plant were regular, but some deviations, particularly in the transition points, were recorded. In order to make clear the cause of these irregularities of trajectory, the course of elongation of leaf petiole and blade in relation to localization and shift of zones of elongation during ontogenesis was analysed. The present analysis is similar to that described by the author's earlier experiments with pea roots. Oscillatory curves circumscribed by petiole, projected on a horizontal plane, were compared with curves circumscribed by the blade tip. The analysis of the leaves of different ages enabled us to study this process in dependence on growth rate. It was confirmed that oscillations are a result of elongation; the extent of oscillations is quantitatively dependent on the growth rate. An analysis of the zones of growth showed that in petiole the active meristems are localized near to its base while in the leaf lamina they move gradually during the ontogenesis from the apical to the basal part of the leaf blade. Active meristems of young rapidly growing leaves are localized approximately in the middle of the blade while those of old leaves were found in close proximity to the base of the lamina. The growth rate of petiole can be expressed in hundreds of mm per hour (4.8×10^?2 mm h^?1); half of this value was recorded for its apical part. The growth rate of leaf blade was found approximately ten times higher (3.2×10^?1 mm h^?1). The oscillatory movements of growing leaf consists of two integrate components: of oscillations originating in the base of the petiole and of oscillations of leaf blade the centrum of which is localized in the basal third of the blade. The arrangement of the experiments did not enable us to determine to what extent the phototropic response of leaf blade participates in leaf movements. The movements of leaves of an intact plant are evidently affected by rhythmic stem oscillations. Stem is an integral part of a system which participates in the transfer of information in plants.     

Growth and nutation parameters of primary root of pedunculated oak (Quercus robur L.)

The elongation of primary roots of pedunculated oak (Quercus robur L.), which is associated with nutation oscillations, was registered by a time lapse cinematography. The following characteristics were expressed graphically: relative growth rate [mm h-¹], frequency [rev. h-¹] and amplitudes [mm] of nutation oscillations, their direction and location of nutation curvatures. The growth-oscillation mechanism is interpreted as a part of the geocontrol system of the root and was evaluated on the basis of its physiological efficiency. Comparison of nutation periods showed that the control system of pedunculated oak is three times more and two times less efficient than that of pea and maize, respectively. Comparison of the oscillation amplitudes of growing roots gives similar results.     

Synchronization of oscillatory rhythms of stems and leaves

A previous report on the mechanism of diurnal oscillations is supplemented here by data concerning causes of irregularities in their oscillation trajectories. Cinematographic records showed that the final trajectory is significantly influenced by the circumnutation oscillations of the stem. Amplitudes of these oscillations which are small(ca 0.7 mm as compared with 5 X larger amplitudes of leaves when measured at the leaf tip) can be enlarged up to 10 times the value at the apical tip of the leaf. These nutations are responsible for side-deviations of space spirals of growing leaves in the direction of their shorter half axis. This explanation is based on the occurrence of side-deviations of leaf trajectories which correlate with the actual position of the nutation phase of the stem. Concurrent frequencies of the two oscillations (= diurnal rhythm) indicate that nyctinastic oscillations of the leaves are controlled by the same mechanism as is the circumnutation of the stem.     

Circumnutation oscillations of the hypocotyl and hypocotyl hook formation: A comparison of Norway spruce (Picea abies (L.)Karst.) and Scots pine (Pinus silvestris L.) seedlings

Circumnutation oscillations of hypocotyls were studied in Norway spruce and Scots pine using time-lapse cinematography. It was found that the circumnutations were specific in species. The analysis of hypocotyl ontogeny (100 h) revealed a different duration of the phases I, II and III of nutation oscillations in the first and second taxon. From the quantitative point of view it can be stated that during the phase I of nutation oscillations the Norway spruce hypocotyls exhibited higher frequency activity (corrections in direction of the hypocotyl by an elongation-controlling system corrected by a feedback mechanism), while in the phase III of nutation oscillations higher growth rate and larger amplitudes were observed in the Scots pine hypocotyl when compared with those of Norway spruce. The hypocotyl hook appeared only in Norway spruce.     

Role of the Cotyledons in the Phototropic Response of Lavatera cretica Seedlings

Young seedlings of Lavatera cretica L. exhibit positive phototropism. The hypocotyl perceives unilateral illumination with blue light and curves towards the light source by unequal growth. In addition, the cotyledonary laminas perceive the vectorial component of unilateral illumination with blue light and reorient normal to the beam by creating a turgor differential in their pulvini. Excision of one cotyledon resulted in negative organotropic curvature of the hypocotyl, away from the remaining cotyledon. Illumination of the cotyledonary lamina did not participate in the phototropic curvature of the hypocotyl, so long as the lamina was free to reorient to face the beam. When the lamina was continuously exposed to vectorial photoexcitation, elongation of the hypocotyl on the side carrying the cotyledon could be enhanced, or inhibited, depending on the direction of the beam striking its lamina.     

Relationships between xanthoxin,phototropism, and elongation growth in the sunflower seedling Helianthus annuus L.

For phototropic curvature of a green sunflower seedling, only the hypocotyl has to be illuminated; the tip and cotyledons are not involved in stimulus perception. The etiolated seedling is phototropically insensitive, illumination of only the hypocotyl renders it sensitive. It is concluded that the photoreceptor is located within the responding organ. In curving seedlings, the endogenous indoleacetic acid (IAA) remains evenly distributed. However, the inhibitor, xanthoxin (Xa), accumulates on the illuminated side. The degree of phototropic response is generally related to the concentration of Xa. The amount of phototropic curvature is independent of the rate of elongation growth, the former can be changed without affecting the latter, and vice versa. The data conflict with the Cholodny-Went theory, whereas they support the hypothesis of Blaauw that the phototropic reaction is caused by the local accumulation of a growth-inhibiting substance on the irradiated side.Abbreviations CCC chlormequat, (2-chloroethyl)trimethylammonium chloride - GA₃ gibberellic acid - IAA indole-3-acetic acid - Xa xanthoxin     

Phytochrome-mediated phototropism in de-etiolated seedlings : occurrence and ecological significance

Phototropic responses to broadband far red (FR) radiation were investigated in fully de-etiolated seedlings of a long-hypocotyl mutant (lh) of cucumber (Cucumis sativus L.), which is deficient in phytochrome-B, and its near isogenic wild type (WT). Continuous unilateral FR light provided against a background of white light induced negative curvatures (i.e. bending away from the FR light source) in hypocotyls of WT seedlings. This response was fluence-rate dependent and was absent in the lh mutant, even at very high fluence rates of FR. The phototropic effect of FR light on WT seedlings was triggered in the hypocotyls and occurred over a range of fluence rates in which FR was very effective in promoting hypocotyl elongation. FR light had no effect on elongation of lh-mutant hypocotyls. Seedlings grown in the field showed negative phototropic responses to the proximity of neighboring plants that absorbed blue (B) and red light and back-reflected FR radiation. The bending response was significantly larger in WT than in lh seedlings. Responses of WT and lh seedlings to lateral B light were very similar; however, elimination of the lateral B light gradients created by the proximity of plant neighbors abolished the negative curvature only in the case of lh seedlings. More than 40% of the total hypocotyl curvature induced in WT seedlings by the presence of neighboring plants was present after equilibrating the fluence rates of B light received by opposite sides of the hypocotyl. These results suggest that: (a) phytochrome functions as a phototropic sensor in de-etiolated plants, and (b) in patchy canopy environments, young seedlings actively project new leaves into light gaps via stem bending responses elicited by the B-absorbing photoreceptor(s) and phytochrome.     

Accumulation of 14C from exogenous labelled auxin in lateral root primordia of intact pea seedlings (Pisum sativum L.)

When [¹⁴C]indol-3yl-acetic acid was applied to the apical bud of 5-day old dwarf pea seedlings which possessed unbranched primary roots, a small amount of ¹⁴C was transported into the root system at a velocity of 11–14 mm h^-1. Most of the ¹⁴C which entered the primary root accumulated in the young lateral root primordia, including the smallest detectable (20–30 mm from the primary root tip). In older (8-d old) seedlings in which the primary root bore well-developed lateral roots, ¹⁴C also accumulated in the tertiary root primordia. In contrast, little ¹⁴C was detected in the apical region of the primary root or, in older plants, in the apices of the lateral roots.Abbreviations IAA indol-3yl-acetic acid     

Phototropic bending of non-elongating and radially growing woody stems results from asymmetrical xylem formation

Active phototropic bending of non-elongating and radially growing portion of stems (woody stems) has not been previously documented, whereas negative gravitropic bending is well known. We found phototropic bending in woody stems and searched for the underlying mechanism. We inclined 1-year-old Quercus crispula Blume seedlings and unilaterally illuminated them from a horizontal direction perpendicular to ('normal' illumination) or parallel to ('parallel' illumination) the inclination azimuth. With normal illumination, active phototropic bending and xylem formation could be evaluated separately from the negative gravitropic response and vertical deflection resulting from the weight of the seedlings. One-year-old stems with normal illumination bent significantly, with asymmetrical xylem formation towards the illuminated upper surface and side of the stem, whereas those with parallel illumination showed non-significant lateral bending, with asymmetrical xylem formation only on the upper side. A mechanical model was built on the assumption that a bending moment resulted from the asymmetrical xylem formation during phototropic bending of the woody stems. The model fitted the relationship between the observed spatial distributions of the xylem and the observed lateral bending, and thus supported the hypothesis that phototropic bending of woody stems results from asymmetrical xylem formation, as such occurs during gravitropism.     

Physiology of Movements in Stems of Seedling Pisum sativum L. cv. Alaska : I. Experimental Separation of Nutation from Gravitropism

Gravitropism and nutation in the stems of dark-grown, seedling peas (Pisum sativum L. cv. Alaska) were recorded on time-lapse photographs made with photomorphogenetically inactive light. Although gravitropism and nutation have been connected by several different theories in the past, our experiments indicate that the two processes are in fact dissociable. The evidence is as follows: (a) Nutational patterns are asymmetric. There is much greater amplitude of oscillation in the plane parallel () to the plane of the apical hook than in the plane perpendicular (), yet the average gravitropic response is equal in these two planes. (b) Brief red light irradiation given 16 to 24 hours before observation greatly increases the amplitude of nutation in the -plane, but has no influence on the kinetics of gravitropic response. (c) An inhibitor of auxin transport, α-naphthylphthalamic acid, strongly inhibits nutation at 5 micromolar but affects gravitropism only at higher concentrations. (d) Nutation is also strongly inhibited by removal of the apical bud, but gravitropism is unaffected. (e) The period of nutation does not exhibit a constant relationship to the response time of gravitropism. The above evidence is inconsistent with theories that gravitropism is an asymmetrically modified nutation or, alternatively, that nutational oscillations result in a simple fashion from gravitropic overshoots. The evidence is consistent with, although not proof of, autonomous factors such as an endogenous rhythm of growth as the cause of nutation in pea stems. However, gravity and nutation do interact. Nutation in a population of seedlings can be synchronized and brought into phase by a single gravitropic induction. Furthermore, the response time and initial rate of gravitropic curvature depend to some extent on the phase of nutational curvature at which gravitropic induction is begun.     

Influence of cobalt on soybean hypocotyl growth and its ethylene evolution

Development of dark-grown “Clark” soybean (Glycine max [L.] Merr.) seedlings is abnormal at 25 C but normal at 20 and 30 C. At 25 C, hypocotyls swell and fail to elongate normally; lateral root formation and seedling ethylene evolution are enhanced.

Co²⁺ promoted hypocotyl elongation of etiolated “Clark” soybean seedlings by 28% when grown at 25 C. The same growth-promoting concentration reduced hypocotyl thickness and primary root elongation by 28 and 43%, respectively. Co²⁺ inhibited ethylene production both of intact seedlings and of apical 1-centimeter hypocotyl segments with attached epicotyls and cotyledons by 65 and 60%, respectively. These results suggest that Co²⁺ exerts its effects on the hypocotyl growth by inhibiting ethylene production, and also confirm our previous conclusion that abnormal ethylene production at 25 C is responsible for the inhibition of hypocotyl elongation and for its swelling.

     

Physiology of Movements in the Stems of Seedling Pisum sativum L. cv Alaska : III. Phototropism in Relation to Gravitropism, Nutation, and Growth

Phototropic response in etiolated pea (Pisum sativum L. cv Alaska) seedlings is poor. However, the curvature induced by unilateral blue light can be hastened and increased in magnitude by a previously administered red light pulse followed by several hours of darkness. Phytochrome is involved in the red light effect. Phototropic response was almost completely inhibited by removal of the apical bud and hook, but it was restored if exogenous indole-3-acetic acid was applied apically to the cut stump. Therefore, the stem contains both the phototropic photoreceptor and response mechanism. Perception of gravity and gravitropic response were also localized in the stem, but gravitropism was scarcely inhibited by decapitation. It was also observed that the kinetics and curvature pattern of gravitropism differed greatly from those of phototropism. Like phototropism, stem nutation required auxin and was promoted by red light. Unlike phototropism, photoenhanced nutational curvature required the apical hook and was propagated as a wave down the stem. Naphthylphthalamic acid inhibited, in order of decreasing effect, nutation, phototropism/gravitropism, and growth. Phototropism, gravitropism, and nutation appear to represent distinct forms of stem movement with fundamental differences in the mechanisms of curvature development.     

Immunological estimation of growth regulator distribution in phototropically reacting sunflower seedlings

The distribution of immunoassayable xanthoxin (XA), abscisic acid (ABA) and indole-3-acetic acid (IAA) in all parts of sunflower ( Helianthus annuus L.) seedlings was determined. During the course of phototropic curvature, including the lag phase (5 min), the distribution of these growth regulators was analyzed in the illuminated and shaded side of the hypocotyl, as well as in the peripheral and central tissues. All three growth regulators showed no detectable asymmetries between the illuminated and shaded hypocotyl halves during the lag phase and early phototropic curvature. Also, no indication for an exchange of XA, ABA or IAA between the peripheral and central tissues was observed. Partial removal of the peripheral cell layers revealed that changes in the growth properties of this tissue, preferentially at the illuminated side of the hypocotyl, are required for the phototropic reaction. Complete removal of the peripheral cell layers abolishes the phototropic response. In dark-incubated, green sunflower seedlings, the loss of sensitivity to phototropic stimulation is correlated with decreasing levels of IAA immunoreactivity, whereas no changes in the levels of ABA- and XA immunoreactivity were recorded. The findings are discussed with respect to the involvement of ABA, XA and IAA in phototropic reactions of green dicotyledonous shoots.     

Diurnal and ultradiurnal oscillations of growing organs within the framework of the information system of the plant

The analysis of growth and movements of seedling organs of kidney bean (Phaseolus vulgaris L.) provides a pattern of periodic phases of activity and relaxation. The existence of a central organ which would control the phase relationships, is not anticipated in the integrity of the plant. The cyclic activity of individual organs shows itself by growth associated with oscillation movements. One and the same organ may simultaneously accomplish oscillatory movements with a diurnal and ultradiurnal frequency. These rhythms originate during the organ development; the first pair of kidney bean leaves at first executes oscillation movements with a diurnal frequency and only after it is fully developed it exhibits a diurnal cycle with the photophil phase upwards and the scotophil downwards, the oscillations with an ultradiurnal oycle being maintained. The movements of the two leaves are synchronous, but there occur short sections with a desynchronous cycle. Simultaneously with these oscillations, in which the leaf petiole takes part, the adult leaf performs oscillatory movements perpendicular to the longitudinal leaf axis, the so-called side swings, controlled by periodical changes of the joint attaching the leaf blade. Their frequency is practically identical with that of the ultradiurnal cycle. Thus the periodic growth activity of the kidney bean results in growth oscillations passing in the diurnal cycle with a frequency of 0.043 rev.h^-1, their ascending and descending phases consisting of periodical ultradiurnal oscillations in cycles of 0.73–0.59 rev.h^-1. The epicotyl growth shows a similar pattern: into the basic diurnal nutation cycle with a frequency of 0.042 rev.h^-1 ultradiurnal oscillation cycles are incorporated having a similar frequency to that revealed in leaves (0.69–0.64 rev.h^-1). The diurnal oscillatory cycles belong to a system established on the basis of periodicity of day and night and other geophysical cycles. The ultradiurnal rhythmic oscillations are presumed to be an expression of the geocontrol system of root and shoot growth direction and orientation of the organ in space. The shape of their trajectories in bean leaves is contradictory to this; they are not spatial helices, as the kybernetic model would presuppose, but have a vertical, upwards and downwards course in one plane. Since these oscillatory movements with an ultradiurnal cycle cease after petiole excision from the stem and after shoot apex amputation, one may presume that they are coupled with the low-frequency oscillatory system of the epicotyl.     

Genetic control of stem form in Pinus pinaster Ait. seedlings exposed to lateral light

 In order to compare family differences in stem form determination, seedlings of eight half-sib progenies of Pinus pinaster were exposed to three different light treatments: fixed lateral light (T1), alternate lateral light (T2), and direct sunlight (T3). From spatial coordinates of several points along the stem we computed four variables: global leaning (GL), apical leaning (APL), flexuosity index (FL) and length of the stem (LEN). Based on comparisons of the four variables, the phototropic stimulus caused different responses in stem form at the familial level. Treatment had an important effect on stem form, although the familial response to treatments was quite variable. Heritability values (h²) of the four analyzed variables showed a different pattern of variation for the three treatments, being very stable for LEN and FL, whereas h² of APL was much greater based on T1 and T2 compared to T3, and h² of GL based on T2 was much greater compared to T3 and T1. Differences in stem form were due not only to photomorphogenetic response to different light stimuli, but also to the straightening processes such as compression wood formation. The results suggest that lateral light treatments may be useful in revealing differences in efficiency of the mechanisms involved in stem form determination. Received: 1 June 1995 / Accepted: 1 April 1997     

GROWTH PATTERNS IN NUTATING AND NONNUTATING SUNFLOWER (HELIANTHUS ANNUUS) HYPOCOTYLS

Dark-grown sunflower (Helianthus annuus L.) seedling hypocotyls (15–30 mm) were marked with two rows of lanolin-coated resin beads, and the events of the following 24 hr, in physiological darkness, were recorded on time-lapse video. Nutational movement of the hypocotyl, followed for 20–24 hr for each of 21 seedlings, was found to have a mean period of 153 ± 26 min (ca. 24 C). Displacement of each bead, with time, was measured with a microcomputer-controlled video analyzer, and relative elemental elongation rate and relative growth rate analyses were carried out to determine the spatial and temporal distribution of growth. Relative elemental elongation rates were plotted against distance and time to produce “growth landscapes.” A strongly nutating seedling showed periodic fluctuations in local growth rates that alternated between values of 0.0 hr^−-1 and >0.12 hr^−-1 near the hypocotyl hook. Nearer the base, maximum growth rates were lower but local periodic changes still were evident. Seedlings, in which nutation appeared during the time period analyzed, showed non-synchronous pulses of growth along the axis. With nutational development, these local growth fluctuations became synchronized along each side and phased (usually 180° out of phase) with the coordinated growth fluctuations along the opposite side. In some seedlings the changes from low to high local growth rates occur nearly simultaneously over two-thirds of the active region. In others, basipetally traveling waves of growth are suggested by the growth landscapes.