An Experimental Analysis and Comparison of Three Rhythms of Movements in Bean (Phaseolus Vulgaris L.)

Three types of rhythmic movements of Phaseolus vulgaris L. (pole beans) were examined collectively and their characteristics compared. Although the ultradian rhythms of shoot circumnutation and leaf movement, as well as the circadian rhythm of leaf movement, occurred simultaneously, each rhythm could be expressed independently of the other two. Shoot circumnutation and ultradian leaf movements displayed the same period (80 min at 25°C and Q₁₀⋍2), while the period of the circadian leaf movements was not temperature dependent (Q₁₀⋍1). Interaction into the plant between two ultradian rhythms (shoot circumnutation and ultradian leaf movement) with the same period and coexistence in the pulvinus of an ultradian with a circadian rhythm are discussed.     

Circadian Modulation of Circumnutation Length, Period, and Shape in Helianthus annuus

Modulation of a turgor-growth movement called circumnutation in sunflower (Helianthus annuus L.) was investigated using a picture analysis system. Two photoperiod conditions were applied: light–darkness conditions (LD) 8:8 and LD 20:10. After about 3 weeks of these regimes, the plants were placed under constant light to determine whether circadian regulation of circumnutation existed or not. The rhythms of movement activity with regard to the trajectory length, period, and shape of individual circumnutations were examined. Data were processed by Fourier spectral analysis. All the parameters, trajectory length, period, and shape, revealed the ability to entrain to the administered daily cycles (16 h or 30 h). We observed diurnal fluctuations of the circumnutation parameters with the phase of the highest trajectory length, the shortest period, and the highest shape coefficient (the most circular form) during the dark period. After the LD–LL transition, the parameters revealed periodicity, which was close to 24 h. After several days of a clear circadian free running rhythm, a gradual decrease of the amplitude of the rhythm was observed. However, the rhythm did not disappear completely. The trajectory length manifested the strongest entrainment; the circumnutation period and the circumnutation shape were less modulated by photoperiod. These findings indicate for the first time that different parameters of circumnutation in sunflower are circadian-regulated rhythms, not solely ultradian as had been thought previously.     

An aluminum influence on root circumnutation in dark revealed by a new super-HARP (high-gain avalanche rushing amorphous photoconductor) camera

The circumnutation of a rice root under dark conditions was observed using a highly sensitive camera, a new super-HARP camera. A rice root showed regular rhythmic movement with fixed angle. When treated with Al (5 microM AlCl3), the rotation angle of the root tip was drastically decreased and then the movement was resumed again, whereas the root elongation rate was constant. With the increase of Al concentration, the cycle-fading period became shorter. This is the first report to show that an Al treatment ceased the rotation movement of the root but not elongation.     

Circadian rhythm of circumnutation in inflorescence stems of Arabidopsis

We investigate the modulation of circumnutation in inflorescence stems of Arabidopsis to determine the circadian regulation of circumnutation. Under constant light conditions (LL), circumnutation speed in wild-type plants fluctuates, with the phase of the highest speed at subjective dawn; the period length is close to 24 h. toc1 appears to shorten the period and elf3 causes an arrhythmic phenotype in circumnutation speed in LL, suggesting that a common circadian clock may control both circumnutation speed and other circadian outputs. These results highlight for the first time a role for a circadian clock in the regulation of circumnutation based on genetic analysis of Arabidopsis.     

Circumnutation behavior of an exotic honeysuckle vine and its native congener: influence on clonal mobility

Virtually all plant parts rotate slightly about a central axis, a movement called circumnutation, but vines show exaggerated circumnutation. This study contrasts circumnutation in two congeneric twining vines, specifically focusing on differences in erect and prostrate shoots, and examines the impact of circumnutation on exploitation of available climbing supports and exploration for more distant ones. Elongating shoots of Lonicera japonica and L. sempervirens growing in a common garden were classed as (1) erect but not climbing, (2) climbing on a trellis, or (3) prostrate, and their circumnutation quantified by tracking the compass direction of shoot tips. To quantify the impact of different circumnutation behaviors, the climbing success of erect shoots and the maximum dispersion and rooting success of prostrate shoots were measured. Erect shoots of both species circumnutated at similar rates (averaging 31°/h), and did not differ in their success rate of exploiting trellises (averaging 76.8%). Prostrate shoots differed, with those produced by L. japonica having reduced circumnutation. In contrast, prostrate shoots of L. sempervirens continued to circumnutate as much as erect shoots. The specialized circumnutation behavior of the prostrate shoots of L. japonica results in increased rooting success and maximum dispersion compared to the unspecialized shoots of L. sempervirens.     

A pleiotropic Arabidopsis thaliana mutant with inverted root chirality

Circumnutation is an oscillating movement of a growing plant organ that is believed to result from an endogenous rhythmic process intrinsic to growth. Circumnutating organs, as they extend, describe a helical trace. In Arabidopsis thaliana (L.) Heynh. circumnutation is particularly evident in primary roots and occurs, as in most plants, in a right-handed direction when viewed from above in the direction of the growing tips. We have discovered a pleiotropic mutant of Arabidopsis with left-handed root circumnutation. Major abnormalities of the mutant are: (i) a reduced size of all organs, mainly due to a defect in cell elongation or expansion; (ii) a zigzagging pattern of stem pith cells, reminiscent of the “erectoides” phenotype of the lk mutant of Pisum; (iii) roots of the mutant are gravitropic but as they grow, they form tight, left-handed coils. Genetically, the mutant depends on the presence of two independent monogenic recessive factors acting additively. The mutant alleles of both factors alter the growth of the aerial organs in a similar manner but differ at the root level: one mainly produces non-circumnutating roots, the other changes the direction of circumnutation from right to left hand. Received: 18 July 1996 / Accepted: 30 November 1996     

Glutamate induces series of action potentials and a decrease in circumnutation rate in Helianthus annuus

Reports concerning the function of glutamate (Glu) in the electrical and movement phenomena in plants are scarce. Using the method of extracellular measurement, we recorded electrical potential changes in the stem of 3‐week‐old Helianthus annuus L. plants after injection of Glu solution. Simultaneously, circumnutation movements of the stem were measured with the use of time‐lapse images. Injection of Glu solution at millimolar (200, 50, 5 mM) concentrations in the basal part of the stem evoked a series of action potentials (APs). The APs appeared in the site of injection and in different parts of the stem and were propagated acropetally and/or basipetally along the stem. Glu injection also resulted in a transient, approximately 5‐h‐long decrease in the stem circumnutation rate. The APs initiated and propagating in the sunflower stem after Glu injection testify the existence of a Glu perception system in vascular plants and suggest its involvement in electrical, long‐distance signaling. Our experiments also demonstrated that Glu is a factor affecting circumnutation movements.     

Circumnutation as a visible plant action and reaction: Physiological,cellular and molecular basis for circumnutations

Circumnutation is a helical organ movement widespread among plants. It is variable due to a different magnitude of trajectory (amplitude) outlined by the organ tip, duration of one cycle (period), circular, elliptical, pendulum-like or irregular shape and clock- and counterclockwise direction of rotation. Some of those movement parameters are regulated by circadian clock and show daily and infradian rhythms. Circumnutation is influenced by light, temperature, chemicals and can depend on organ morphology. The diversity of this phenomenon is easier to see now that the digital time-lapse video method is developing fast. Whether circumnutation is an endogenous action, a reaction to exogenous stimuli or has a combined character has been discussed for a long time. Similarly, the relationship between growth and circumnutation is still unclear. In the mechanism of circumnutation, epidermal and endodermal cells as well as plasmodesmata, plasma membrane, ions (Ca²⁺, K⁺ and Cl⁻), ion channels and the proton pump (H⁺ATPase) are engaged. Based on these data, the hypothetical electrophysiological model of the circumnutation mechanism has been proposed here. In the recent circumnutation studies, gravitropic, auxin, clock and phytochrome mutants are used and new functions of circumnutation in plants'' life have been investigated and described.Key words: circumnutation, Helianthus annuus, plant movement, elongation, growth, ultradian rhythm, circadian rhythm, time-lapse video, ion channels     

Circumnutation and distribution of phytohormones in <Emphasis Type="Italic">Vigna angularis</Emphasis> epicotyls

Circumnutation is a plant growth movement in which the tips of axial organs draw a circular orbit. Although it has been studied since the nineteenth century, its mechanism and significance are still unclear. Greened adzuki bean (Vigna angularis) epicotyls exhibited a clockwise circumnutation in the top view with a constant period of 60 min under continuous white light. The bending zone of circumnutation on the epicotyls was always located in the region 1–3 cm below the tip, and its basal end was almost identical to the apical end of the region where the epicotyl had completely elongated. Therefore, epidermal cells that construct the bending zone are constantly turning over with their elongation growth. Since exogenously applied auxin transport inhibitors and indole-3-acetic acid (IAA) impaired circumnutation without any effect on the elongation rate of epicotyls, we attempted to identify the distribution pattern of endogenous auxin. Taking advantage of its large size, we separated the bending zone of epicotyls into two halves along the longitudinal axis, either convex/concave pairs in the plane of curvature of circumnutation or pre-convex/pre-concave pairs perpendicular to the plane. By liquid chromatography–mass spectrometry, we found, for the first time, that IAA and gibberellin A₁ were asymmetrically distributed in the pre-convex part in the region 1–2 cm below the tip. This region of epicotyl sections exhibited the highest responsiveness to exogenously applied hormones, and the latent period between the hormone application and the detection of a significant enhancement in elongation was 15 min. Our results suggest that circumnutation in adzuki bean epicotyls with a 60 min period is maintained by differential growth in the bending zone, which reflects the hormonal status 15 min before and which is shifting sequentially in a circumferential direction. Cortical microtubules do not seem to be involved in this regulation.     

Daily and infradian rhythms of circumnutation intensity in Helianthus annuus

Circumnutation in Helianthus annuus L. was investigated by measurements lasting 4–7 weeks using a picture analysis system. The rhythmicity of circumnutation vigour (intensity) with regard to the trajectory length and period of individual circumnutations were examined. Three photoperiod conditions were applied [light/dark (LD), continuous light (LL) and LD followed by LL]. Data were processed by the Fourier analysis. Statistical analysis included the examination of circumnutation mean frequencies and correlation tests. Both parameters, trajectory length and period, revealed a daily (24 h) modulation in LD with a weak correlation between them, whereas in LL no daily modulation of the parameters was observed. After LD–LL transition, the parameters were gradually losing their daily modulation. Despite a very strong modulation of the trajectory length in LD, the period was quite stable in all groups tested, but only in LD were there no statistical differences in the number of circumnutations per 24 h among the plants studied. LD was concluded to be the strong synchronizer, making the plants circumnutate regularly. Regardless of the presence or absence of daily modulation, the infradian (several and more days long) harmonics of the trajectory length were the same in each group. These findings strongly support the view that circumnutation in sunflower, widely known as an ultradian rhythm, also possesses daily and infradian modulations of its intensity. To the authors' knowledge, this is the first report of circumnutation that was obtained by a picture analysis system in such a large timescale.     

Glutamatergic elements in an excitability and circumnutation mechanism

In plants, an electrical potential and circumnutation disturbances are a part of a response to environmental and internal stimuli. Precise relations between electrical potential changes and circumnutation mechanisms are unclear. We have found recently that glutamate (Glu) injection into Helianthus annuus stem induced a series of action potentials (APs) and a transient decrease in circumnutation activity. A theoretical explanation for this finding is discussed here taking into considerations data about the ion mechanism of AP and circumnutation as well as about the metabolic and signaling pathways of glutamate and their possible interactions.Key words: action potential, circumnutation, elongation, glutamate, Helianthus annuus, plant movement     

Lazy rice in space: gravity regulates helical movement in plants

Circumnutation, the helical movement of organs, has been observed in diverse species of land plants. Whether circumnutation arises purely from internal growth oscillations or as a response to exogenous forces such as gravity is a subject of active debate. By observing rice seedlings grown under microgravity at the International Space Station (ISS) and analyzing the agravitropic lazy1 mutant, Kobayashi et al. (2019) propose gravity as the causal force that regulates circumnutation of rice coleoptiles.     

Circumnutational movement in rice coleoptiles involves the gravitropic response: analysis of an agravitropic mutant and space‐grown seedlings

Plants exhibit helical growth movements known as circumnutation in growing organs. Some studies indicate that circumnutation involves the gravitropic response, but this notion is a matter of debate. Here, using the agravitropic rice mutant lazy1 and space‐grown rice seedlings, we found that circumnutation was reduced or lost during agravitropic growth in coleoptiles. Coleoptiles of wild‐type rice exhibited circumnutation in the dark, with vigorous oscillatory movements during their growth. The gravitropic responses in lazy1 coleoptiles differed depending on the growth stage, with gravitropic responses detected during early growth and agravitropism during later growth. The nutation‐like movements observed in lazy1 coleoptiles at the early stage of growth were no longer detected with the disappearance of the gravitropic response. To verify the relationship between circumnutation and gravitropic responses in rice coleoptiles, we conducted spaceflight experiments in plants under microgravity conditions on the International Space Station. Wild‐type rice seeds were germinated, and the resulting seedlings were grown under microgravity or a centrifuge‐generated 1 g environment in space. We began filming the seedlings 2 days after seed imbibition and obtained images of seedling growth every 15 min. The seed germination rate in space was 92–100% under both microgravity and 1 g conditions. LED‐synchronized flashlight photography induced an attenuation of coleoptile growth and circumnutational movement due to cumulative light exposure. Nevertheless, wild‐type rice coleoptiles still showed circumnutational oscillations under 1 g but not microgravity conditions. These results support the idea that the gravitropic response is involved in plant circumnutation.     

Circumnutations under free-fall conditions in space?

Regular growth movement, so-called circumnutation, of plants and plant organs is a very general phenomenon. The origin of circumnutations is, however, unclear. Three different types of model are discussed in relation to some experimental results on circumnutations. It is suggested that an experiment in space, under free-fall conditions, should be done on different species showing circumnutations in order to discriminate between the models.     

An electronic device for continuous, in vivo measurement of forces exerted by twining vines

Contact forces are important in maintaining the twining habit of viny stems. A stem twining around a supporting pole puts itself into tension and uses a helical geometry to generate normal loads that are large relative to stem mass per unit length (Silk and Hubbard, Journal of Biomechanics 24(7):599-606, 1991). An electronic pressure-sensing device has been constructed to provide continuous, in vivo measurements of the forces exerted by twining stems. The pressure-sensing element is based on a thin beam load cell that is sheared by a twining stem ascending a split pole. Preliminary results show that after morning glory stems begin to coil around a supporting pole, the twining force increases in an oscillatory fashion over 3 or 4 d, corresponding to positions at least 200 mm from the apex. The force-measuring device should reveal relationships between twining forces and developmental attributes or environmental factors.     

Residual nutational activity of the sunflower hypocotyl in simulated weightlessness

Does gravity drive circumnutation? One model ascribes hypocotylcircumnutation to a continuing series of geotropic responseseach of which overshoots thereby maintaining a sustained oscillation.However, some features of the observed movements are not easilyreconciled with the model. The critical feature of this modelis the requirement that circumnutation must exhibit an absolutedependence on a g-force. Experiments with Helianthns annum onhorizontal clinostats demonstrated an 80% reduction in the amplitudeof hypocotyl circumnutation (compared with upright plants atone g) although the oscillations continued at simulated "zerog". It is not certain that the clinostat environment adequatelysimulates the weightless environment of space but, if it does,we may expect a space experiment to demonstrate that hypocotylnutation in Helianthus annuus is not fully dependent on gravity. (Received October 13, 1978; )     

The global trend in plant twining direction

Aim  To examine, at a global scale, patterns in the direction in which climbing plants twine. We tested three hypotheses: (1) that twining direction is determined randomly; (2) that twining direction is determined by apices following the apparent movement of the sun across the sky; and (3) that twining direction is determined by the Coriolis effect.
Location  Seventeen sites spanning nine countries, both hemispheres and 65° of latitude.
Methods  Twining direction was recorded for the first c . 100 stems encountered along transects through natural vegetation at each site.
Results  Ninety-two per cent of the 1485 twining stems we recorded grew in right-handed helices, i.e. they twined in an anticlockwise direction. This is significantly ( P < 0.001) different from random. The proportion of stems twining right-handedly (anticlockwise) was independent of both latitude ( P = 0.33) and hemisphere ( P = 0.63). These data are inconsistent with the idea that twining direction is determined by either the relative passage of the sun through the celestial sphere or by the Coriolis effect. Thus, we reject all three of our hypotheses.
Main conclusions  The predominance of right-handed helical growth in climbing plants cannot be explained by hypotheses attempting to link plant growth behaviour and global location. One alternative hypothesis for our findings is that the widespread phenomenon of anticlockwise twining arises as a function of microtubule orientation operating at a subcellular level.     

Rhythmic iron stress reactions in sunflower at suboptimal iron supply

Uptake and translocation of labelled iron were studied in sunflower ( Helianthus annuus L. cv. Sobrid) grown in nutrient solution with low FeEDDHA concentrations during preculture. In contrast to conditions for plants adequately supplied with iron, suboptimal iron supply leads to temporary Fe stress with rhythmic rates of uptake and translocation of iron (period 2–4 days). This rhythmic behaviour of iron uptake is associated with corresponding changes in morphology (thickening of root tips) and physiology (increase in reducing capacity) of the roots. Iron stress is alleviated within less than one day if sufficient iron is available. This is indicated by normalisation of root morphology, reducing capacity and rate of iron uptake and translocation. This rhythm in iron uptake stresses the importance of rhythmic patterns of biochemical behaviour in complex biological systems. It is suggested that phytohormones are involved in the transformation of the iron nutritional status of the shoot apex into a "signal" for the uptake sites of iron in the roots. Preliminary experiments with sunflower in calcareous soil indicate an ecological importance of this fine regulation mechanism for plants on soil with a low iron availability, manifested in rhythmic iron stress reactions.     

Complex relationship between growth and circumnutations in Helianthus annuus stem

The growth and circumnutation of the stem of three-week old Helianthus annuus in the 16:8 h light:dark photoperiod were monitored using an angular position-sensing transducer and a time lapse photography system. It was found that the rate of growth and circumnutation reached a high level in the dark stage; in the light stage, however, only the growth rate reached the same high level, whereas the circumnutations were weak. These results showed that in the light stage the stem circumnutation was downregulated more strongly than the growth. Short-term stem responses to darkening and illumination were a further display of the relation between growth and circumnutations. Switching off the light caused an increase in the growth and circumnutation rate. In some cases it was accompanied by changes in the rotation direction. On the other hand, switching the light on caused an immediate transient (several-minute long) decrease in the growth rate resulting in stem contraction, and this was accompanied by an almost complete pause of circumnutation. Additionally, under light, there occurred a subsequent decrease in the magnitude, disturbance of circumnutation trajectory and, in some cases, changes in the direction of rotation. The observed stem contraction and disturbance of circumnutation imply the occurrence of turgor changes in sunflower stem, which may be caused by a non-wounding, darkening or illumination stimulus. Our experiments indicate that the disturbances of the growth rate are accompanied by changes in circumnutation parameters but we have also seen that there is no simple quantitative relation between growth rate and circumnutation rate.Key words: Helianthus annuus, plant movement, circumnutation, elongation, growth, stem contraction     

Gravitropic response plays an important role in the nutational movements of the shoots of Pharbitis nil and Arabidopsis thaliana

The shoots of a Japanese strain of morning glory ( Pharbitis nil  ) called 'Shidare-asagao' display agravitropic and weeping growth. It has been shown that this shoot agravitropism may be due to the defective differentiation of endodermal cells that contain statoliths. Roots of the weeping morning glory show normal responsiveness to gravity and the shoots are positively phototropic. Shoots of the morning glory cultivar Violet used as a wild type exhibited distinct circumnutation with circular movements that increase as the plants grow. In weeping morning glory, however, nutation was limited to slight back and forth or side to side movements. To determine whether endodermal cells participate in circumnutation through a function that is independent of their role in gravitropism, the nutational movements of various gravitropic mutants of Arabidopsis thaliana were compared. The inflorescences of wild-type Arabidopsis showed relatively large circular movements. Inflorescences of the pgm-1 mutant, which is defective in starch synthesis, showed reduced nutation. Even more seriously affected were the sgr1-1 / scr-3 and sgr7-1 / shr-2 mutants, which are defective in endodermal cell differentiation, and the auxin-resistant axr2-1 mutant showed no significant nutational movements at all. 1- N -naphthylphthalamic acid (NPA) could inhibit Violet circumnutation, supporting the notion that auxin participates in circumnutation. Thus, the gravitropic response is an essential component in plant shoot circumnutation. Endodermal cells are involved in such circumnutation possibly because of their role in inducing the gravitropic response.