Journal of Experimental Botany, Vol. 53, No. 369, pp. 689-698,
April 1, 2002
© 2002 Oxford University Press
Original Papers |
Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing
1 Biosphere 2 Center, Columbia University, Oracle, AZ 85623, USA
2 Interdisciplinary Centre for Scientific Computing, University of Heidelberg, Im Neuenheimer Feld 368, 69120 Heidelberg, Germany
3 Institute of Plant Sciences, University of Heidelberg, Im Neuenheimer Feld 360, 69120 Heidelberg, Germany
4 ICG-III (Phytosphere), Research Center Jülich GmbH, 52425 Jülich, Germany
Received 28 February 2001; Accepted 15 November 2001
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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A newly developed technique based on image sequence analysis allows automatic and precise quantification of the dynamics of the growth velocity of the root tip, the distribution of expansion growth rates along the entire growth zone and the oscillation frequencies of the root tip during growth without the need of artificial landmarks. These three major parameters characterizing expansion growth of primary roots can be analysed over several days with high spatial (20 µm) and temporal resolution (several minutes) as the camera follows the growing root by an image-controlled root tracking device. In combination with a rhizotron set up for hydroponic plant cultivation the impact of rapid changes of environmental factors can be assessed. First applications of this new system proved the absence of diurnal variation of root growth in Zea mays under constant temperature conditions. The distribution profile of relative elemental growth rate (REGR) showed two maxima under constant and varying growth conditions. Lateral oscillatory movements of growing root tips were present even under constant environmental conditions. Dynamic changes in velocity- and REGR-distribution within 1 h could be quantified after a step change in temperature from 21 °C to 26 °C. Most prominent growth responses were found in the zone of maximal root elongation.
Key words: Diurnal course, kinematics, oscillation, root growth, temperature, Zea mays.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Root growth is based on the linear arrangement of cell division, expansion growth and differentiation along the root tip (Silk, 1992
; Schurr, 1997). Mechanistic understanding of expansion growth requires analysis of the spatial distribution of expansion growth, which accelerates and decelerates within a zone of only a few millimetres in length. The distribution of expansion growth in primary roots has been investigated for a long time (Sachs, 1887; Goodwin and Stepka, 1945). From the early days scientists have used photographic methods (Erickson and Sax, 1956) to visualize and quantify the growth rates of root tip segments. Maize roots became a model system for the relatively large size of their growth zone, their fast growth and easy cultivation. Profiles of distributions of velocity and the relative elemental growth rate (REGR) provide the basis for the analogy between plant growth and fluid dynamics established in the 1970s and 1980s. Deposition processes within the root tip (and the similarly growing monocotyledonous leaf) could be calculated by this approach using the continuity equation (Erickson, 1976; Silk, 1984). The classical techniques to analyse the distribution of expansion growth at the root usually require artificial landmarks on the rhizodermis. Analysis reveals their movement relative to each other. These methods are laborious and take a lot of time. Thus an analysis with high spatial and temporal resolution would require enormous effort, limiting the general application of these techniques. Therefore, progress in the analysis of expansion growth was slow due to the lack of an efficient method with high spatial and temporal resolution. In particular, linking mechanisms of expansion growth and its control to the molecular and biochemical level is hampered as these processes work in time scales of hours or less and on microscopic scales, while classical techniques for root expansion analysis allow hourly resolution.
Digital image analysis has become widely available in recent years with cameras and computers fulfilling the basic needs for automatic analysis. Processing of single digital images has thus become widely used in the field (Beemster et al., 1996; Sacks et al., 1997; Beemster and Baskin, 1998). The next step technology is image sequence analysis, which intrinsically can provide spatial and temporal resolution. Recently developed general algorithms to analyse motion in image sequences (Haußecker and Spies, 1999) have already given dense fields of expansion growth from time lapse sequences of growing dicot leaves (Schmundt et al., 1998; Schmundt and Schurr, 1999) without the need of artificial landmarks. The adaptation of this approach for the analysis of spatio-temporal dynamics of expansion growth of root tips is reported and this new technique is applied to a set of basic problems of root expansion growth analysis.
Diurnal variation of expansion growth of monocot and dicot leaves is strong, even when air temperature is held constant (Watts, 1972; Schmundt et al., 1998; Schurr et al., 2000; Walter and Schurr, 2000). By contrast, previous experiments in roots have shown that the variation of expansion growth between individual seedlings is not due to diurnal variation (Walter et al., 2000). This topic is highly important because the diurnal course of expansion growth defines the background against which short-term changes in response to, for example, environmental stimuli have to be detected. The absence of a diurnal rhythm would be a significant difference between growth control in roots and dicot leaves. The temperature of the root has been shown to alter root growth and the distribution of expansion growth significantly (Pahlavanian and Silk, 1988). These authors compared roots growing under different, but constant temperatures. In this paper, the response of root growth and the distribution of expansion growth during dynamic changes of root temperature is reported for the first time.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Plants and cultivation
Seeds of Zea mays L. (var. Alexander) were germinated in well-watered sand pots. When roots were approximately 2 cm long, 20 seedlings were mounted into holes in a plexiglass bar of a rhizotron (Fig. 1
). This set-up allowed seedling roots to be monitored optically. Roots of mean length and straight habitus were chosen for image sequence acquisition. The black plastic rhizotron base plate was inclined by 68°. Bidistilled water flushed constantly over the growing roots, was collected in a plastic basin (volume 10 l) and pumped up to the top of the base plate again with a submerged pump. The water stream was widened with the plexiglass bar to almost the width of the base plate. A transparent plastic foil covered the base plate and the roots from the plexiglass bar downwards. The rhizotron was placed in a growth room with 12/12 h light/dark cycle, 150 µmol m-2 s-1 PAR, 40% relative humidity and 21 °C air and water temperature during the growth of the seedlings. Variation of water temperature was achieved by a controlled water bath.
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=940 nm) is used for illumination. The camera position is automatically displaced along with growing root tips.
Image acquisition and processing
The procedures of image acquisition and processing including the mathematical calculation of relative growth rates with subpixel accuracy are given in a detailed manuscript concerning the development of this method for leaf growth analysis (Schmundt et al., 1998). This method is deduced from standard image sequence processing procedures, so-called optical flow techniques, which are described in image processing handbooks and textbooks (Haußecker and Spies, 1999; Jähne, 1997).
The following section describes the adaptation of this method to the analysis of root growth. Moreover, the most important principles of the applied image analysis procedures are explained briefly without mathematical stringency.
A CCD-camera (Sony XC75) with attached infrared diode-fields (940 nm, Fig. 1
; Walter and Schurr, 2000) was positioned in front of the rhizotron. The camera was equipped with a lowpass infrared filter (RG9, Schott, Mainz) that blocked visible light. It was mounted in perpendicular orientation to the base plate on an arrangement of two moving stages attached to a vibration free stand. The entire imaging set-up was covered by dark foil to shield the root from light, which could interfere with root growth. Images (640x480 pixels) corresponding to an area of approximately 14x10 mm (approximately 20 µm pixel-1, Fig. 2) were automatically digitized every minute. When the root tip reached a pre-set position of the digitized frame that was implemented (one position in the x- and one in the y-direction), the moving stages shifted the position of the camera for 5 mm in x- and y-directions, respectively, within seconds to keep the root tip within the image frame. This root tracking device allowed image sequences to be acquired over several days. Control of the root tracker and image sequence acquisition as well as analysis of the image sequences was done with algorithms written in a digital image sequence processing (DISP) software (Heurisko, Aeon, Hanau).
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The position of the root was detected within each image by separating root and background via a grey value threshold. Since the calyptra is hardly visible in near infrared light, the apical end of the root corresponds to the outermost pixel found by this segmentation process and thus roughly to the quiescent centre of the meristem. Root tip growth velocity was calculated after calibration from the determined sequence of positions. The segmented images of the root were used for calculation of velocity distribution along the growth zone of the root using the optical flow approach (for details see Schmundt et al., 1998
; Haußecker and Spies, 1999).
In short, any structure showing a suitable grey value contrast within its local spatio-temporal neighbourhood results in an oriented grey value structure in a virtual image stack (Fig. 3). Motion of such grey value structures can be quantified by determination of the ‘vector of constant brightness’. Its orientation in the spatio-temporal neighbourhood around a central pixel is analysed by means of the so-called structure tensor algorithm as previously described in length for leaf growth analysis (Schmundt et al., 1998).
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In the implementation used for expansion growth of roots, spatio-temporal neighbourhoods of 7x7 pixels and five images were chosen. This means that the three-dimensional pixel matrix (x, y, time), which represents an image stack, was analysed blockwise by the structure tensor. The ratio between the value in the x-direction (or the y-direction) and the value in time-direction of the vector of constant brightness rendered the velocity component vx in the x- (or vy in the y-) direction for the motion of the central pixel. After determination of velocities for all suitable pixels in the image stack (20–30% of all pixels within the outline of the root), missing information was filled in by linear interpolation, resulting in a dense ‘displacement vector field’ for the root growth zone.
Velocity distributions vx(x)im in the image coordinates were calculated by columnwise summation (across the root) of vx-values inside the borders of the root mask (image section that corresponds to the root after segmentation from background—see above):
 | (001) |
The first value of this distribution corresponded to the velocity of the root tip vx,tip and represented the maximal velocity of the distribution. Velocity distribution relative to the growing root tip vx(x)root was calculated by taking the difference between the maximal velocity at the tip and the local velocity at each position along the root:
 | (002) |
Statistical analysis was applied to calculate the averaged velocity distributions: after selecting a time interval in the image sequence (typically 30 min), the mean and the standard deviation for each value of vx within the velocity distribution in the coordinate system of the root were calculated. Distributions with outliers of vx-values deviating by more than five standard deviations from the mean were eliminated from the selected set of distributions and the mean and standard deviation were calculated again. The procedure was iteratively repeated three times. By this procedure, velocity distributions from images taken directly before or after the camera was shifted by the moving stages and from otherwise disturbed images were excluded from the analysis.
Values for vy were retrieved in an analogous procedure.
Distribution of REGR was calculated as the derivative of the velocity distribution for single images as well as for averaged sequence intervals:
 | (003) |
Colour-coded maps of REGR- and velocity-distribution were produced by the use of ‘look-up-tables’ that assigned specific colours to classes of REGR and velocity, respectively. Original images were overlaid by transparent colour maps. On demand, video animations or sequential maps of those four-dimensional velocity- or REGR-distributions can be produced and displayed by the software.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Steady-state root expansion growth
Up to now, 12 different maize roots were investigated with the described methods for their expansion growth distribution over a period of several hours (up to 3 d) in the conditions of the present study. In each of the roots, maximal growth activity repeatedly showed two peaks in the zone of maximal elongation (Fig. 4
). The intensity and the location of the peaks differed strongly between individual roots and fluctuated with time. The distributions show average values over 30 min. REGR standard deviations are typically in the range of 0–10% h-1. Taking average values over several different roots or over longer time intervals leads to a loss of information concerning the structure of the double peak. The existence of the double-peaked REGR-maximum is strengthened by results from roots of Solanum tuberosum and from Nicotiana tabacum (data not shown here).
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The temporal stability of the distribution is shown by eight consecutive, momentary REGR-distributions of a single typical root under stable environmental conditions (Fig. 5
).
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Root tip growth velocity (vx,tip) showed no diurnal course (Fig. 6
) at a constant root temperature. Although the velocity of the root tip fluctuated in each experiment, no significant maximum or minimum of the diurnal course was detected during the day/night cycle. This implies that whole root expansion growth is not regulated diurnally. This result eases experiments on the impact of environmental stimuli on root expansion growth, as they can be conducted at any time of the day without the need to account for a dynamic underlying diurnal variation of root expansion growth. Measurements of vx,tip of about 120 control plants in the same setup by marking the root tip position manually in 4 h intervals (data not shown here) support this result.
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The maximal change of vx,tip throughout the experiments was from 1.1 mm h-1 to 1.5 mm h-1 within 4.5 h corresponding to a change in velocity of about 7% h-1 or a mean acceleration of about 0.1 mm h-2. Standard deviations of whole root expansion growth within 30 min intervals are in the same range as the differences between maximal and minimal vx,tip. A considerable variability of whole root expansion growth between equally treated seedlings is also clearly demonstrated by this experiment: at identical growing conditions, the average vx,tip for the four roots shown in Fig. 6
varies between 0.8 mm h-1 and 1.3 mm h-1. It has previously been shown that this variation is not linked to differences in the seed weight (Walter et al., 2000).
Visualization of REGR-distribution can also be done by an overlay of colour-coded REGR-maps (Fig. 7, left) to match the original image with local REGRs. These data can also be displayed as movie clips: Under constant conditions the REGR-profile of the root tip is time-invariant in the root coordinate system and moves along with the root tip through the image stack.
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Lateral oscillations of the growing root at constant external conditions
Small movements perpendicular to the main root axis were observed within the expansion zone, resulting in a wavy motion of the growing root tip (Fig. 7, right). During these movements the anticlinal axis through the root tip deviated by up to 10° from the mean root growth direction. These movements could be quantified as velocities in the y-direction of the image frame (vy). The colour-coded images of the vy-distribution show the periodic movement of the root tip. This movement is not restricted to the very tip, but extends throughout the entire growth zone. The periodical waves of lateral velocities show clearly (Fig. 7, right) that the maximum of the lateral movement starts at the root tip and is pushed through to the end of the expansion zone. In some cases root tip and parts of the expansion zone moved actually in opposite directions. Fourier analysis of the y-movement of the root tip gave a main frequency component of 0.0185 min-1 corresponding to a period of 54 min. In parallel experiments (n
20), periods between 40 min and 70 min were observed (data not shown here). vy can reach maximal values of 0.7 mm h-1; mean values of 0.3 mm h-1 were observed in this experiment. Lateral movements were not coupled to clearly observable rotational distortions of the growth zone.
The lateral movement is a major source of the short-term variation in vx,tip (Fig. 6). A lateral velocity of 0.7 mm h-1 perpendicular to a vx,tip of 2 mm h-1 diminishes vx,tip by 6.3% with the assumption of a maximal velocity of linear root elongation of 2 mm h-1 (vx=(22-0.72)x1/2).
Dynamic changes in expansion growth and its distribution during a temperature shift
Previous quantitative analyses of the profile of root expansion growth were limited to steady-state conditions. With this method it is possible to study dynamic changes in response to, for example, environmental stimuli. In this section, the significance of the spatial aspects of the results is enhanced by presenting average values over 30 min. A temperature increase by 5 °C caused an acceleration of vx,tip within 0.5 h (Fig. 8). One hour after increasing the temperature from 21 °C to 26 °C, vx,tip had increased from 1.4 mm h-1 to 1.9 mm h-1 and this velocity was maintained throughout the rest of the experiment (11 h). During the temperature change, strong fluctuations of expansion growth obscured the temperature-shift response and for this reason were smoothed out by averaging over 30 min. During the first hour after the temperature shift, the root tip was accelerated by 0.5 mm h-2, thus significantly more than the maximal acceleration during constant conditions (see above). Additional experiments gave the same results, but because of the inter-individual variability of absolute growth velocity, the graphical representation of several experiments would not add to the clarity of the results shown for one individual root. It is a further advantage of this non-invasive technique that individual roots can be monitored in their response, thus limiting the impact of inter-individual plant variation.
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Concerning the reaction of the REGR-distribution towards the temperature step, the most distinct effect was observed in the first maximum of REGR-distribution in the centre of the root elongation zone (Fig. 9
). During the temperature change, REGR was boosted, particularly at the peak zone closest to the root tip, and reached values of up to 65% h-1, while the second peak did not show such an overshooting response. This might indicate a functional difference between the two peaks of REGR.
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A minor increase of expansion growth was detected in the growth zone from 2–7 mm behind the root tip. The length of the expansion zone tended to enlarge at 26 °C relative to 21 °C. This result is partly in contrast to previous analyses with classical techniques, which did not have a comparable spatial resolution.
The principal pattern of distributions of REGR along the growth zone was not changed by the step increase in root temperature. After the root expansion zone had settled to the new steady-state temperature regime, higher REGR were detected from 1.5 mm behind the root tip to the end of the expansion zone. Maximal REGR was increased from 30% h-1 to peak values of 45% h-1. The two maxima of REGR were still present, but moved slightly further away from the root tip (2.5 and 5 mm, respectively).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Growth in plants is a process characterized (and controlled) by spatio-temporal patterns. It is therefore a crucial requirement to analyse growth processes in time and space simultaneously in order to understand the impact of environmental stimuli as well as basic mechanistic control. As the underlying biochemical and molecular mechanisms act within minutes rather than hours, it is necessary to use high resolution methods to link growth distributions with the controlling processes. This has been difficult with classical approaches (for an overview see Schurr, 1997
). This paper combines the description of a new method for the analysis of root expansion growth at high spatio-temporal resolution with the first applications that analyse the pattern of root expansion rate and lateral movements of the root tip under constant conditions as well as the dynamic responses to variation of root temperature.
The root tip is commonly chosen as the origin of a linear coordinate system running along the centre of the growing root tip (Silk, 1992). The transformation of velocities from the displacement vector field (in the rectangular coordinate system of the image) to the growth field of the root is done automatically by the algorithms finding the root tip. More sophisticated, curvilinear coordinate systems at even higher resolution need to take into account the arrangement of cell walls along the principal directions of growth within the root apical meristem (Hejnowicz and Karczewski, 1993).
Root expansion growth does not vary diurnally
For the root, the analysis of the distribution of expansion rates in space and time with an analogous procedure to the one used successfully in leaves (Schurr et al., 2000) was made possible by the development of an additional device that allows the growing root tip to be tracked with a CCD-camera mounted on moving stages. This approach allows continuous observation of the growing root tip at high resolution over several days.
The absence of diurnal changes in expansion growth from roots growing at constant environmental conditions was proven. This result was obtained consistently even when individual roots were tracked over a period of several days and was supported by parallel analysis of root tip growth by following the root tip position with lower temporal resolution and in parallel experiments with roots of Nicotiana tabacum and Arabidopsis thaliana (data not shown). This result confirms measurements on roots of rice and sorghum (Iijima et al., 1998), but is in contrast to the diurnal behaviour of leaves of dicotyledonous species (Schmundt et al., 1998; Walter and Schurr, 2000; Schurr et al., 2000), where it was shown, that diurnal growth variations are present at constant temperatures too. Hence, those two major plant sinks differ significantly in their diurnal behaviour of expansion growth. The reason for this might be the difference in the natural diurnal fluctuation of temperature in the soil (nearly constant) and above ground (strong diurnal variations). It is shown for monocot leaves that even small diurnal changes of the temperature within the growth zone affect leaf expansion (Watts, 1974; Ben-Haj-Salah and Tardieu, 1995). Both systems, leaves and roots, respond to temperature changes, but at constant conditions, their diurnal course of expansion growth differs. It will be important to unravel the biochemical and molecular background of this difference in growth control, the impact on whole plant transport, nutrient and carbon allocation, as well as its evolutionary aspects.
Technically, this result eases analysis of dynamic responses of root expansion growth to changing environmental stimuli, as it is not required to take into account an underlying diurnal variation. However, significant variation between seedlings has been detected, even when treated identically. This cannot be explained from different seed weights as previously reported (Walter et al., 2000). It might thus either be due to genetic variability or, for example, variation of the nutrients stored in the seeds, from which the seedlings are fully dependent in this early stage of development (Walter et al., 2000).
Root expansion profiles have two zones of high expansion activity
The spatial distribution of expansion growth along the root axis showed two major peaks of REGR. Even though the differences in the peak activities were not large, they were consistently found throughout the entire experiments and even at different temperatures. The differential response of the first and second peaks to changing root temperature (Fig. 8, see below) hints at different functional properties of both zones. The presence of a double peak of REGR in the expansion zone contrasts with the results of most previous analyses with classical techniques (Erickson and Sax, 1956; they also described a double peak on a single root). With these techniques the spatial (and temporal) resolution was not sufficient to identify this feature.
Logistic functions are commonly used to fit profiles of REGR along roots (Morris and Silk, 1992; Walter et al., 2000) and monocotyledonous leaves (Beemster et al., 1996). However, such models are only able mathematically to describe a single peak in the REGR profile. Spatial shifts of the single peak activity of REGR as quantified by such approaches (Silk, 1992) have to be interpreted with caution, as they could also be explained by movements of the two peak activities relative to each other. Such effects should be restudied with higher spatial resolution and analysed with new, more function-based models of root expansion growth profiles.
At present there is not a proven explanation, but, as root differentiation occurs at different speeds at the root surface and the root core (Dolan et al., 1993), the two peaks might originate from expansion of the root tip zones driven or hindered by different tissues (e.g. epidermis, core). Correlations between anatomical records and root expansion distribution are required to test this hypothesis. Alternatively, different transport properties of the tissue linked to root differentiation might be involved. Key target tissues that might be involved in this process are protophloem and protoxylem. Both tissues are initiated between the root tip and the zone of maximal growth activity, with the protophloem being formed significantly earlier (more apical) than the protoxylem (Goodwin and Stepka, 1945; Esau, 1965).
Lateral movement of growing root tips
Transversal growth components with a frequency of between 40 and 70 min were quantified as velocities in the y-direction of the image frame (vy). Technically, the transverse component of growth is responsible for the variation in the axial growth rate distribution, a component previously not possible to analyse with classical techniques. These movements are obviously closely related to expansion growth and may originate from local differences in expansion growth between the different faces of the vertically growing root, as previously shown in gravitropical responses of roots (Buff et al., 1987). The lateral movements might originate from a gravitropical feedback signal (Buff et al., 1987) or from an internal oscillation causing circumnutations even without gravitational impact (Johnsson and Heathcote, 1973; Shabala and Newman, 1997).
Temperature affects root expansion zones differently and dynamically
Analysis of dynamic changes of REGR profiles in response to short-term changes of environmental conditions were previously not possible with the low spatial and temporal resolution of standard techniques. However, short-term responses can elucidate functional differences in sections of the growth zone. Additionally, even in well-buffered environments like the soil, dynamic changes of the conditions are common (e.g. flushes of cold water during heavy rain fall) and can be relevant for the overall performance of the growing root.
Steady-state temperature regimes and their results for the characteristics of elongation zones of growing root tips were analysed in detail several years ago (Pahlavanian and Silk, 1988). In agreement with these results an increase was found in the REGR by up to 50% in response to a temperature increase of 5 °C. The new steady-state was reached within 60 min.
The step change in temperature affected mostly the apical peak of maximal expansion growth activity, but also exerted an effect on the entire expansion zone. The overall pattern of REGR distribution was not altered and exhibited two distinct zones of high REGR before, within and after the temperature change. The extent of the growing zone tended to increase with the rising temperature. This is in contrast to the observations in a range of different, but constant growth temperatures (Pahlavanian and Silk, 1988; Ben-Haj-Salah and Tardieu, 1995). From the present data sets it is, however, not clear if the increase in length of the elongation zone is transient and would diminish after several days or if it has not been detected by the previous techniques. The increased size was still present several hours after the temperature step increase. An important feature of the temperature effect is the differential response of the two zones of REGR peak activity. While the more apical one exhibited a strong overshoot during the first 30 min after the temperature increase, the more basal zone immediately reached its new steady-state REGR. This clearly indicates different functional properties of both zones, which need to be studied in more detail in future experiments.
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Conclusion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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A new technique has been established that allows automatic analysis of REGR distributions in growing root tips on the basis of image sequence analysis. The method significantly enhances the spatial and temporal resolution in comparison to the commonly used techniques. The software application is straightforward and extracts the relevant natural coordinate system directly from the image sequences. The enhanced performance has already given new insights into the spatial and temporal characteristics of expansion zones of growing root tips. Long-term (diurnal over several days by the extension of the root tracker) and short-term (dynamic response to step increase in temperature, lateral oscillations) growth effects have been studied. It has been shown that diurnal variations in root expansion are absent from roots, when the temperature is maintained constant, and that the response to changing temperature affects individual regions of the expansion zone differently. The enhanced spatial resolution provided evidence for two distinct zones of high REGR with different functional characteristics.
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Acknowledgments |
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The authors thank the German Science Foundation (DFG) for funding within the research unit ‘Study of dynamic processes by image sequence analysis’ and the SFB ‘Molecular ecophysiology’. We thank Wendy Silk for helpful discussions during the experiments and Regina Feil for her technical assistance.
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Notes |
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5 To whom correspondence should be addressed. Fax: +492461612492. E-mail: u.schurr{at}fz\|[hyphen]\|juelich.de
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 M. WATT, W. K. SILK, and J. B. PASSIOURA Rates of Root and Organism Growth, Soil Conditions, and Temporal and Spatial Development of the Rhizosphere Ann. Bot., May 1, 2006; 97(5): 839 - 855. [Abstract] [Full Text] [PDF]
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A. G. Bengough, M. F. Bransby, J. Hans, S. J. McKenna, T. J. Roberts, and T. A. Valentine Root responses to soil physical conditions; growth dynamics from field to cell J. Exp. Bot., January 1, 2006; 57(2): 437 - 447. [Abstract] [Full Text] [PDF]
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A. WALTER and U. SCHURR Dynamics of Leaf and Root Growth: Endogenous Control versus Environmental Impact Ann. Bot., May 1, 2005; 95(6): 891 - 900. [Abstract] [Full Text] [PDF]
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L. Fan and P. M. Neumann The Spatially Variable Inhibition by Water Deficit of Maize Root Growth Correlates with Altered Profiles of Proton Flux and Cell Wall pH Plant Physiology, August 1, 2004; 135(4): 2291 - 2300. [Abstract] [Full Text] [PDF]
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C. M. van der Weele, H. S. Jiang, K. K. Palaniappan, V. B. Ivanov, K. Palaniappan, and T. I. Baskin A New Algorithm for Computational Image Analysis of Deformable Motion at High Spatial and Temporal Resolution Applied to Root Growth. Roughly Uniform Elongation in the Meristem and Also, after an Abrupt Acceleration, in the Elongation Zone Plant Physiology, July 1, 2003; 132(3): 1138 - 1148. [Abstract] [Full Text] [PDF]
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