Journal of Experimental Botany, Vol. 54, No. 389, pp. 1909-1918,
August 1, 2003
© 2003 Oxford University Press
Chiral and non-chiral nutations in Arabidopsis roots grown on the random positioning machine
Received 17 December 2002; Accepted 2 May 2003
1 Institute of Agroenvironmental Biology and Forestry, Consiglio Nazionale delle Ricerche, Via Salaria Km 29.300, 00016 Monterotondo, Rome, Italy
2 Department of Biology, University of Sassari, Italy
* To whom correspondence should be sent. Fax: +39 06 9064492. E-mail: fernando.migliaccio{at}ibaf.cnr.it 
The direction toward which the Arabidopsis roots slant during elongation in the wild type is considered to be the right-hand because, when the plant is seen from above the shoot apex, the root appears to move forward making loops in the clockwise sense. This movement, as is known in Physics, is considered right-handed, and this definition is applied to the whole universe (Gardner, 1990). However, it needs to be remembered that Linnaeus and others scientists (Hart, 1990) considered the above movement left-handed, because they imagined seeing the helix from its interior, in which case the view, logically, is reversed. 
Recently, the Hashimoto group produced some significant papers (Furutani et al., 2000; Hashimoto, 2002) about two mutants called spir1 and spir2, which are studied mainly for the strong right-handed torsion seen in their shoots, but also for the right-handed torsion seen in the roots. The roots of these mutants, however, as seen from the pictures in their papers, appear to wave as they normally do in the wild type, where the torsion is alternatively to the left and to the right (Okada and Shimura, 1990). This effect is surely present also in the spir mutants or at least a reduction of the right-handed torsion should be seen when the wave is moving toward the side that is considered the right-hand (in which case the torsion is left-handed in the wild type). However, if just the roots are considered, spir1 and spir2 are left-handed mutants, like 1-6C, because they slant to the side that is considered the left-hand (as explained in ).
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Arabidopsis thaliana roots grown on a vertically set plate do not elongate straight down the gravitational vector, but by making waves and coils, and by conspicuously slanting towards the right-hand. This behaviour, in a previous paper, was ascribed to the simultaneous effect of three processes: circumnutation, positive gravitropism and negative thigmotropism. However, when the plants are grown on the Random Positioning Machine (RPM), in conditions that are believed to simulate space microgravitational conditions closely, the roots do not show the usual pattern. In the wild type, the roots make large loops to the right-hand side, whereas in the gravitropic and auxinic mutants aux1, eir1, rha1, they just move randomly around the initial direction. Therefore, if the movements made on the RPM are those produced by the exclusion of gravitropism and negative thigmotropism, as is apparent, the conclusion is that Arabidopsis roots are animated by a form of chiral circumnutation, that is lacking in the auxinic and gravitropic mutants aux1, eir1 and rha1. In addition, the 1 g condition appears to reduce the scatter among the circumnutating tracks produced by the roots of the wild types, but not among those of the mutants. Because there is a scarcity of literature regarding circumnutation in roots, it is not known how widely root chiral circumnutation is spread, but it is known that, in some previously studied species, just random nutations are observed. Two kinds of nutating movements seem to exist in plant roots and, whereas the random process does not seem to be connected with auxin physiology and transport, the chiral process appears to be connected in the same way as gravitropism is.
Key words: Arabidopsis, auxin, circumnutation, gravitropism, microgravity, roots.
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As is known, plant organs do not grow straight, but by making movements around the direction of elongation. These movements, that can follow various trajectories, from elliptical to irregular, and that were generically known to ancient plant scientists (Baillaud, 1962), have been more precisely described by Charles and Francis Darwin (Darwin and Darwin, 1880) as circumnutating movements and the general process as circumnutation. The processes do not include the tropic processes which are induced by evident external factors such as gravity or light. Circumnutation, however, could be the basic mechanism from which, as the Darwins believed, all the other movements originated through the process of evolution.
Obviously, circumnutating movements can also be seen in the model plant Arabidopsis, both in shoots and in roots. Whereas in the shoots the movement has been reported to be irregular (Orbovic and Poff, 1997; Schuster, 1979), and indifferent to both hands, in roots, at least of the most commonly studied ecotypes, the movement is helical and right-handed (Simmons et al., 1995). When, in fact, Arabidopsis seedlings are grown on the flat surface of a hard-agar dish, that was vertically set or somehow inclined on the horizontal plane, its primary roots do not grow straight down the gravitational vector, but by making waves, and coils, and by slanting consistently toward a side of the plate that has been considered to be the right-hand on the basis of the general spatial movement of the root.
The first report on Arabidopsis root patterns was from Okada and Shimura (1990, 1992), who advanced the hypothesis that the root waves were due to an oscillatory movement of the root tip to the right or to the left of the gravitational vector, as a consequence of the root tip hitting the agar surface, in turn as a consequence of gravitropism. Subsequently, Simmons et al. (1995) suggested that the observed root pattern was mainly due to right-handed circumnutational helical movement of the growing roots, which, when flattened on the two-dimensional agar surface produce waves, coils, slanting and torsions. This circumnutational movement has since been clearly demonstrated by Mullen et al. (1998) by a continuous recording of root growth through a CCD camera connected to a computerized program. More recently, however, the Arabidopsis root movements were reinterpreted as the combined effect of essentially three processes, circumnuation, gravitropism and negative thigmotropism (Migliaccio and Piconese, 2001).
In the last few years, much help in understanding root growth patterns has come from some recently isolated Arabidopsis root mutants disturbed in auxin physiology, gravitropism, and circumnutation. These mutants, whose number is steadily increasing each year, can be divided into different groups. However, those of interest for the present research are essentially three: gravitropism and auxin transport mutants, such as aux1, agr1/AtPin2/eir1/Wav6-52, AtPin1, AtPin3 (Bennet et al., 1997; Palme and Galweiter, 1999); gravitropism and auxin physiology mutants, such as axr1, axr2, axr 3, rgr1/axr4, rha1, clg1, sku5, arg1 (Estelle and Somerville, 1987; Simmons et al., 1995; Sedbrook et al., 1999; Firn et al., 2000; Ferrari et al., 2000; Piconese et al., 2001; Sedbrook et al., 2002); handedness mutants, such as 1-6C, spir1 and spir2 (Marinelli et al., 1997; Furutani et al., 2000). The first group of mutants, on a vertically set agar plate, showed an absence of gravitropism and irregular or random root pattern, the second group showed reduced gravitropism and/or resistance to auxins and ethylene, and the third group showed a circumnutation symmetry opposite to that of the wild type, which is right-handed.
Apart from the mutants, there is now an additional tool used to study the Arabidopsis root growth pattern and its origin and there is the possibility of performing the experiments in the absence of one of the factors which control the root pattern, that is of gravitropism through the exclusion of the force of gravity. In the absence of this force, the root pattern will depend only on the circumnutating movement, since the negative thigmotropic reaction, dependent on gravitropism, will also be excluded. Nowadays, this absence of gravity condition can be achieved on the International Space Station (ISS) and other space vehicles or, waiting for availability of the ISS, it can be simulated through a modern clinostat, that is, through the Random Positioning Machine (RPM). This apparatus, instead of running the biological samples on a single axis, as classic clinostats do, makes continuous random movements on two axes, supposedly subjecting the material set at its centre to a general multilateral gravistimulation. The condition is not exactly that which exists in space, but, as concerns nutational movements, it should represent a good approximation.
The present paper is concerned with these kind of experiments. The root growth patterns of two wild-type Arabidopsis ecotypes, of a handedness mutant, and of three agravitropic mutants, were studied through the RPM. This is the first report of its kind, because, although other reports were concerned with the tropic movement of plant roots in weightlessness, they were especially concerned with the random movements that are produced in the roots of plants such as cress, maize, and sunflower (Brown, 1993; Antonsen et al., 1995; Johnsson et al., 1996; Legue et al., 1996; Johnsson, 1997; Antonsen and Johnsson, 1998). In Arabidopsis, however, the case seems different, because in the wild types the root movements are not random at all, but show a clear right-handedness, that is they appear to be animated by a process that could be named chiral-circumnutation.
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All the reported experiments were conducted on Arabidopsis seedlings belonging to the ecotypes Wassilewskjia (Ws) and Columbia, the agravitropic and auxinic mutants eir1 (allele with agr1,wav6-52, AtPin2), aux1, rha1 and the left-handed mutant 1-6C. The wild-type seeds, as well as those from the mutants eir1 and aux1, were obtained from the Nottingham Arabidopsis Stock Centre. The rha1 mutant was recently isolated in the laboratory of one of the authors (Piconese et al., 2001), and the 1-6C mutant (Marinelli et al., 1997) was a gift from Professor Soave of the University of Milan (Italy).
Before plating, the seeds were sterilized for 10 min by treatment with a solution made up of 50% commercial bleach (brand name Clorex) and 0.01 % (w/v) SDS, followed by four washes with distilled water. The seeds were then plated in horizontal rows, in petri dishes, on a medium made up of 1.5% agar, 1% sucrose, and 0.5 MS basal medium enriched with Gamborg’s vitamins (from SIGMA number M0404), adjusted to pH 5.7 with KCl. To synchronize germination, the dishes were left in a cold room (4 °C) for 48 h before moving them to the growth room.
Seedlings were then grown on dishes for 7 d at about 23 °C, in white florescent light (200 µmol m–2 s–1 photon flux density), by keeping the dishes vertical, so as to have the primary root growing down the gravitational vector. The vertical was in all cases marked on the bottom of the dishes, because it was later taken as a reference direction.
After this period of growth, half of the dishes were mounted on the Randon Positioning Machine (RPM), and run for an additional 5 d, at 23 °C, and about 150 µmol m–2 s–1 photon flux density. At the same time the remaining half of the dishes were kept vertical in the same room where the RPM was set to furnish a control of plants grown in 1 g conditions. The RPM used was located at the Department of Biology of the University of Sassari, Italy, in Dr P Pippia’s laboratory. RPM was set at 60° s--1.
Two experiments were conducted: in the first the root growth pattern of the wild-type Ws, wild-type Columbia and of the mutant aux1 was studied and, in the second, the root growth pattern of the mutants eir1, rha1 and 1-6C. For each wild-type ecotype or mutant, three Petri dishes were set on the RPM, placing them one above the other at the centre of the apparatus, and three were kept as controls. Each dish carried about 20 seedlings. At the moment of the setting of the dishes on the RPM, the point attained by the root tip was marked on the bottom of the dishes, so as to have a record of the beginning of the experiments. Not all the seeds set in the dishes germinated, so that the number of seedlings analysed is different in the different cases. After 5 d both the dishes running on the RPM and the controls were collected and Xerox images were taken of them from the bottom, so as to have an immediate record of the root pattern produced during the RPM experiments. In addition, pictures were taken of the dishes with a Nikon camera to record the root patterns in a different way.
The Xerox images were then scanned and transferred to a computer program and, on these images, the analysis of the growth pattern was conducted. To analyse the angular deviation of root segments, the technique reported in Antonsen and Johnsson (1998) was applied, not subtracting, however, the first basal segment as they did, but by making reference directly to the vertical marked on the dishes. This analysis consisted in measuring the angle made by the roots with the vertical for each 1 mm of root, starting from the tip, to the moment in which the roots were set on the clinostat. The angular deviation from the vertical was measured by means of a program called Scion-Image, produced by the homonymous Firm, as an adaptation of the original program written for Macintosh by NIH (USA).
On each root picture, a set of 1 mm long segments was drawn and, on these, the angular deviations were measured. The angles were determined at the point of intersection of each 1 mm segment with the following, starting from the interception of the first and the second, down towards the base of the roots. Only seven 1 mm segments were reported on the graphs (see Results), because many roots did not grow over this distance by the 5 d period. The data were then averaged, all the measurements relative to the same segment for the different roots were combined, starting from the tip, and, from the data, graphs were produced by means of the Sigma-Plot (Spw5) program. Subsequently the points on the graphs, marking the average angular deviations for each segment, were subjected to regression analysis, representing their path through a linear regression in all the samples kept in gravitational conditions, with the exception of aux1, and, for those run on the RPM, in the mutants aux1, eir1, and rha. Instead, in the case of the roots from wtWs, wt Columbia and 1-6C run on the RPM, a polynomial 2 grade regression curve was adopted to interpolate at best the average points.
The RPM from Fokker, Netherlands, is basically a clinostat, which produces a multilateral gravitational stimulation in an object set at its centre by slowly rotating it on two axes or by random movements induced on both axes by a computerized program. Although this machine only simulates microgravitational conditions through multilateral stimulation of the studied material on all sides, in the case of tropism, it should reproduce with sufficient fidelity space microgravitational conditions. As would be shown, in fact, it was quite possible to distinguish the behaviour of the wild-type seedlings roots from that of the mutants.
Gravitropism was measured on 7-d-old seedlings grown on petri dishes set vertically square and grown between two agar layers to avoid interference from circumnutation movements. After 7 d of growth, at the beginning of the experiments, the dishes were turned counter-clockwise by 90 degrees (as is known, the direction of the 90 degrees reorientation is important as a consequence of the interference of the slanting in the circumnutating roots) and left for 24 h in the dark at 23 °C. The other conditions were 65% humidity and about 200 µmol m–2 s–1 photon flux density, when in the light. The movement of the primary root tip was marked on the reverse of the dishes at the beginning of the experiments, and at time lapses of 4, 8, and 24 h. The dishes were then xerographed and the xeroxes scanned and made available for computer analysis. To measure the angles, the above-mentioned Scion program was used, measuring, in the case of root responding to gravity, the angle of the root tip from the initial mark and a line decurring through the previously grown root (line set horizontal at the beginning of the experiments). In the case of roots not responding to gravity (aux1 and eir1), the deviation of the root tip was measured by making reference to a straight line decurring through the shoot and the base of the root. In this case, the angles made towards the same direction of the graviresponding roots were considered positive and the movements towards the opposite direction were considered negative.
Root elongation was determined by measuring the extension of the root growth, both in the RPM and in control plants, during the 5 d run on the RPM. Before measuring the root length, the roots were stretched, so as to eliminate their shortening due to the various waves and turns produced on an agar plate.
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Results |
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Figure 1 shows pictures, taken from the dishes after the experiments, of two Arabidopsis wild-type ecotypes, Ws and Columbia, and of the mutants eir1, aux1, 1-6C, after 5 d of growth on the RPM or in 1 g conditions. On the xeroxes taken from the dishes, as reported in the previous section, the angular deviations, shown in Figs 2 and 3, of root segments from the vertical, were measured. Both the pictures and, more clearly, the graphs, show that the roots from the wild-type ecotypes, Ws and Columbia, made on the agar plates on the RPM, large clockwise loops (right-handed), of which the angular deviation average points were interpolated at best through a second grade regression equation. The auxinic mutants aux1 and eir1 instead produced random movements to the right and to the left of the vertical, whose average angular deviation points were best interpolated through linear regression. As expected, the left-handed mutant 1-6C produced a pattern similar to that of the ecotypes, although left-handed (anticlockwise as seen from above) and less deeply circular. The auxinic mutant rha1, which is only partially agravitropic, produced no loops, but its roots moved randomly to the right and to the left of the vertical, as in the case of aux1 and eir1. On the other hand, the curvature of the wtWs was clearly larger than that of wt Columbia, showing, as was already known (Rutherford and Masson, 1996) the strongest right handedness of the former ecotype.
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In 1 g conditions the general picture was different. The roots of wild-types Ws and Columbia showed no loops, but a clear waving and right-handed slanting, whose average points were at best interpolated through linear regression. The auxinic mutants eir1 and aux1 showed random movements similar to those seen on the RPM, although in aux1 a slight tendency to make right-handed loops is apparent, as observed by Mirza (1987),whereas the 1-6C mutant produced a general slanting to the left. The behaviour of rha1 was also peculiar in 1 g conditions because, whereas its roots on the RPM showed just random movements, at 1 g they grew straight down without slanting or with a moderate skew to the left. This behaviour, however, is not clear from the graphs, but in the pictures (Fig. 1) it is self evident. In any case, there is no doubt about the behaviour of rha1 in 1 g conditions, this mutant being the object of study for a long time in the laboratory (Piconese et al., 2001).
In particular, the final measured average angular deviation of the root tips in the different cases was: in 1 g conditions 31.50° for wt Ws, 21.02 for wtCol, 38.21° for aux1, 20.94° for eir1, –4.01° for rha1, –37.99° for 1-6C. On the RPM: 181.60° for wtWs, 113.75° for wtColumbia, 15.94° for aux1, 5.89° for eir1, –26.24° for rha1, –178.12° for 1-6C.
In Figs 4 and 5, the single angular deviations of seven randomly chosen roots for each of the wild-type ecotypes and of the mutants considered, are shown. These pictures are reported to show that the interpolation, for the most linear, in 1 g wild-type ecotypes, plus 1-6C mutant, and in 1 g and RPM auxinic mutants aux1 and eir1 is the consequence of two different processes. In the first case, in 1 g conditions, a constant slanting to the right-hand (left-hand in 1-6C) is at the origin of the liner regression, shown by the fact that all the average points are in the + area (– in the case of 1-6C). In the second case a random movement is at the basis of the linear interpolation, evident from the average points in general falling both in the + and – area. With rha1 in 1 g conditions, the same considerations reported above apply.
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Another aspect that can be seen in Figs 4 and 5, but not in Figs 2 and 3, is the fact that the presence of 1 g seems to reduce the variability in the root angular deviations of the considered wild-type ecotypes, 1-6C mutant, and rha1 in quantitative values, because the curves are in these cases more grouped than in the cases of the RPM or of the auxinic mutants. This is also evident in Table 1, where the average standard deviations of the data (angular deviations) in Figs 1 and 2 are shown.
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The gravitropic response, that is, the reorientation of the root tips after a turn of 90 degrees in a counter-clockwise sense, of all the wild-type ecotypes and mutants studied is reported in Fig. 6. From this graph it can be seen that the auxinic mutants aux1 and eir1 do not show any gravitropic response over the 24 h considered, whereas gravitropism in rha1 and 1-6C is notably reduced, but not abolished. On the other hand, gravitropism is quite regular in the wild-type ecotypes, Ws and Columbia. The exact average values after 24 h were as follows: wtWs=84.57°, wtColumbia=89.31°, 1-6C=61.82°, rha1=37.86°, eir1=–6.13, and aux1=–10.04°.
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Root elongation over 5 d in RPM or 1 g conditions for the wild-type ecotypes, Ws and Columbia, and the mutant aux1, is reported in Fig. 7. The differences observed are apparently small, an increase is seen in the RPM wtColumbia, and a decrease in the RPM aux1 plants. This is in contrast to the data from Antonsen and Johnsson (1998) regarding cress roots, which show a reduction in elongation in plants flown in space. However, the plant and the experimental conditions used by the above scientists were different.
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The measured elongations values were: wtWs, 1 g=15.37±0.43 (SE), RPM=15.38±0.32; wtColumbia, 1 g=8.89±0.27, RPM=16.61±0.22; aux1, 1 g=16.33±0.45, RPM=15.37±0.38.
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The reported data show that whereas the primary roots of wtWs, wtColumbia and the mutant 1-6C produce in 1 g conditions a wavy slanting to the right-hand (left-hand in 1-6C), on the RPM they make large loops to the same direction. By contrast, the auxinic and gravitropic mutants aux1 and eir1 show random movements both in 1 g or in RPM conditions. On the other hand, the case of rha1 was peculiar because, whereas these mutant roots produced random movements on the RPM, in 1 g conditions they elongated vertically down, or a little to the left, but not randomly in any case.
Thus if the pattern observed on the RPM is that produced under the effect of the sole circumnutation, without any interference from gravitropism and negative thigmotropism, it can be concluded that the Arabidopsis roots from the wild types make large movements of circumnutation only to the right-hand (to the left hand in 1-6C). These movements, imagined in a three-dimensional condition, should be close to that of a right-handed (or left-handed) helix, which, when flattened on a two-dimensional agar plate appears, as seen from above, to produce clockwise (or anticlockwise) circular loops (Maher and Martindale, 1980; Mirza, 1987). This pattern is similar to that which can be observed on horizontally set agar plates (not shown), although with these conditions the roots make frequently irregular movements and clockwise multiple strict circles, which elsewhere (Simmons et al., 1995) have been named coils. Since on plates run on the RPM no strict multiple coils were seen, it can be concluded that gravity is involved in the making of the coils. They could be produced as a consequence of the continuous thigmo-stimulation affecting the root tips on horizontally set plates. In any case, the data coming from the experiments with wtWs, wtColumbia and 1-6C seem to confirm the model recently advanced by Migliaccio and Piconese (2001), which suggests, in the production of the root patterns seen in 1 g conditions, an interaction among circumnutation, positive gravitropism, and negative thigmotropism.
On the other hand, the absence of loops either large or strict in the auxinic mutants aux1 and eir1, both in RPM or 1 g conditions, and the presence of random movements to the right and to the left of the vertical, indicates that these mutants are lacking a regular chiral circumnutational movement. The auxinic mutants, therefore, are not just disturbed in the gravitropic response (both aux1 and eir1 have been shown to be totally agravitropic, Fig. 6), but also in the chiral circumnutation. Consequently, the process that is destroyed in the mutants seems to control not only gravitropism, but also circumnutation. In other words, gravitropism and chiral circumnutation seem to have common bases at the level of the transduction of the signal. Naturally, this does not mean that all the plant organs (roots and shoots) that show random nutations do not respond to gravity, because they do indeed respond (Baillaud, 1962). Nevertheless, in this specific case, the notable fact seems to be that the totally agravitropic mutants are also random concerning nutations. The case of rha1 and 1-6C, however, was somehow intermediate between the wild-type ecotypes and the auxinic mutants, because both rha1 and 1-6C show clearly reduced gravitropism, but concerning nutations these were random in rha1 on the RPM, and in 1-6C circular and left-handed. 1-6C, nevertheless, is not an auxinic mutant (Marinelli et al., 1997), and this can explain the regularity in circumnutation and also supports the involvement of auxin in the process.
Another interesting observation that can be made on the root growth pattern comparing the data from the 1 g or RPM conditions, is the fact that the data coming from 1 g conditions show, in the case of the wild-type Ws and Columbia, and in the 1-6C mutant, less variability in the angular deviation from the vertical (Figs 4, 5; Table 1). This effect shows that the 1 g stimulation reduces the variability in the responses quantitatively and modulates circumnutation. A similar observation was made by Andersen and Johnsson (1972), and Zacharias et al. (1987) on Helianthus annuus hypocotyls. In particular, they observed a net increase of the amplitude of the circumnutation waves in parallel with an increased gravity force (to 3 g). 1 g, however, had the reverse effect, so that it is possible to imagine that the force of gravity needed for the production of a regular earthbound circumnutation process is 1 g. The effect of 1 g is visible also in the mutant rha1, clearly, because it is a mutant, only moderately auxin resistant and agravitropic.
There have been so few reports in the literature about root circumnutation (Baillaud, 1962; Johnsson, 1979) that it is not known if the root chiral movement is common or restricted to a few plant species. Charles and Francis Darwin (Darwin and Darwin, 1880) described helical movements, for plants different from Arabidopsis, however, as Boltz (1927) did, and also from the analysis of the circumnutation tracks reported in Spurny (1966) one is led to think they are helical movements. But Fritsche (1899, cited in Baillaud, 1962) reported irregular movements. In some plant species studied in space, different from Arabidopsis, such as cress, sunflowers, and lentil (Legue et al. 1996), nutations were shown to be undoubtedly random. In particular, in a recent paper from Antonsen and Johnsson (1998) it is clearly demonstrated, also with the help of mathematical analyses, that in cress roots flown in space the movements follow a random path. These kind of experiments, made mainly on cress roots and sunflower hypocotyls, support the circumnutation hypothesis advanced by Brown (1993), and more recently by Shabala and Newman (1997), which suggests that this process can start in a point of the plant organ by chance, and then be extended to areas close by. The fact that this process can start chiral circumnutational movements is also interesting, although they can easily reverse after a lapse of time and, in any case, start from the beginning indifferent to one of the two hands.
Random processes of nutation, however, are not characteristic of Arabidopsis wild-type primary roots, in which the roots circumnutate only to the right-hand (to the left-hand in the mutant 1-6C), as well as in the twining plants, where the sense of circumnutation is normally genetically fixed (Baillaud, 1962).
The behaviour of the mutant 1-6C roots was in all aspects similar to that seen in the wild types, with the only difference being in the sense of rotation, and in a reduced response to gravitropism (Fig. 6). This mutant, however, does not seem to represent exactly the opposite of the right-handed wild types, because, as reported in Marinelli et al. (1997), it shows significant alterations in the growth and shape of the epidermal root layer, which do not fully elongate as happens in the wild type. It is suggested that 1-6C roots would switch to the right-hand if the epidermal cells had the possibility of further elongation. Similar considerations also seem to apply to the left-handed mutants spir1 and spir2 recently studied by the Hashimoto group (Furutani et al., 2000).
It is not known how the chiral circumnutational process starts nor how it is maintained. Clearly both the structure and physiology of chiral plant organs should be involved. The subject so far has not really been addressed (Baillaud, 1962). On the basis of this research that shows that the auxinic and gravitropic mutants eir1, aux1 and rha1 present both circumnutation and gravitropism defects, it is suggested that auxin is involved as a condition necessary for chiral circumnutaion, as is well known for gravitropism.
In a previous paper Ney and Pilet (1981) concluded that circumnutation and gravitropism had common bases, because when the roots were responding to gravitropism they stopped circumnutating, and resumed the movement at the end of the gravitropic response. Similar results were obtained by the Darwins (Darwin and Darwin, 1880), who, on the basis of these kind of experiment, stated that gravitropism was a form of modified circumnutation, and that all the plant movements have a common origin, evolved from the simple (non-chiral) movement of nutation.
The experiments reported here, however, limited to Arabidopsis roots, cannot fully support the above hypothesis, but they show that chiral circumnutation and gravitropism in Arabidopsis primary roots seem to depend both on auxin transport and/or physiology. This does not mean to say that the processes of circumnutation and gravitropism in plants are solely controlled by auxin, which probably would be wrong (Firn et al., 2000), but simply that this hormone seems particularly involved, primarily or secondarily, in the circumnutating and tropic responses of plants, as suggested from the beginning by the pioneers of auxin research (Went and Thimann, 1937).
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Acknowledgements |
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We wish to thank Dr A Johnsson from the University of Trondheim, Norway, for critical reading of the manuscript and the suggestions given. The research was made possible by a grant from ASI (Italian Space Agency) to FM.
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References |
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