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First published online April 20, 2007; 10.1104/pp.106.089250 Plant Physiology 144:1157-1165 (2007) © 2007 American Society of Plant Biologists
Intact Plant Magnetic Resonance Imaging to Study Dynamics in Long-Distance Sap Flow and Flow-Conducting Surface Area1Laboratory of Biophysics and Wageningen Nuclear Magnetic Resonance Centre, Department of Agrotechnology and Food Sciences, Wageningen University, 6703 HA Wageningen, The Netherlands
Due to the fragile pressure gradients present in the xylem and phloem, methods to study sap flow must be minimally invasive. Magnetic resonance imaging (MRI) meets this condition. A dedicated MRI method to study sap flow has been applied to quantify long-distance xylem flow and hydraulics in an intact cucumber (Cucumis sativus) plant. The accuracy of this MRI method to quantify sap flow and effective flow-conducting area is demonstrated by measuring the flow characteristics of the water in a virtual slice through the stem and comparing the results with water uptake data and microscopy. The in-plane image resolution of 120 x 120 µm was high enough to distinguish large individual xylem vessels. Cooling the roots of the plant severely inhibited water uptake by the roots and increased the hydraulic resistance of the plant stem. This increase is at least partially due to the formation of embolisms in the xylem vessels. Refilling the larger vessels seems to be a lengthy process. Refilling started in the night after root cooling and continued while neighboring vessels at a distance of not more than 0.4 mm transported an equal amount of water as before root cooling. Relative differences in volume flow in different vascular bundles suggest differences in xylem tension for different vascular bundles. The amount of data and detail that are presented for this single plant demonstrates new possibilities for using MRI in studying the dynamics of long-distance transport in plants.
Sap flow and hydraulic conductivity of long-distance xylem and phloem transport provide key information to validate biophysical structure-function plant models based on integrated carbon and water allocation. Such models are currently used to address plant performance and stress-induced effects (e.g. Daudet et al., 2002  ; Tardieu, 2005), as well as to quantify the contribution of plant evapotranspiration and carbon exchange within global atmospheric circulation models (Sellers et al., 1997). In xylem and phloem, the flow-conducting surface area and the resistance within the vessel or tracheid connections determine hydraulic conductivity (Sperry et al., 2003).
Using conventional methods, it is difficult to measure transport within intact plants or to determine the active flow-conducting area. In the phloem, xylem, and tissue surrounding them, complex and fragile gradients in pressure and osmotic potential exist that are easily disturbed by invasive experimentation (Verkman, 2000
For several decades, heat tracer methods have been used to measure mass flow in the xylem, resulting in acceptable results if precautions against potential sources of errors are taken (Smith and Allen, 1996
NMR imaging (or MRI) is a promising and attractive method for providing spatially and temporally resolved quantitative information on water transport at different length scales—transport over membranes, cell to cell, and long distance—in intact plants (Van As, 2007
The phenomenon that various plants show rapid wilting when their roots are cooled and quick recovery after root temperature has returned to normal levels was reported as early as 1860 (Sachs, 1860
Current techniques for studying both embolism formation and the as-yet-unresolved issue of whether and how repair might occur are not fully up to the task because they are invasive and/or destructive. Embolisms in xylem vessels in roots and leaves, frozen while still attached to the plant, have been studied with cryoscanning electron microscopy (e.g. Canny, 1997
Many hypotheses for embolism-refilling mechanisms have been proposed (e.g. see Salleo et al., 2004
Overall Response of the Plant to the Day/Night Cycle and Root Cooling Figure 2 shows the root water uptake rate (mg/s) for the complete period of time that the plant was in the instrumental setup (compare with Fig. 1 ), starting at 8 PM on day 1. During the day (lights on), transpiration of the plant clearly elevated water uptake by the roots. The light intensity on day 2 was low to allow the plant to recover from transportation and insertion in the setup. From day 3 on, illumination was kept constant at about 200 µmol m–2 s–1 (photosynthetically active radiation), depending on the position of the leaves. MRI flow measurements were started on a regular interval to follow the adaptation of the plant. From day 5 on, MRI flow measurements were repeated at shorter time intervals.
The values for total volume flow (compare with Fig. 2 ), calculated from the MRI measurements (see next section), are indicated as diamonds and white crosses. Diamonds represent values from conventional measurements in which motion-encoding gradients are stepped equidistantly before Fourier transformation into a propagator (Scheenen et al., 2000a ). These values turned out to be systematically too small for higher flow velocities because, at the actual experimental settings, displacements up to a maximum of 150 µm during the labeling time (corresponding to a maximum velocity of 16 mm/s) were covered. This explains the observed results on days 5 and 6, which are about constant, independent of the increase in flow and thus velocity. At reduced velocities (during day 5 after cooling and days 6 and 7 at night), these conventional MRI flow results fit the actual root water uptake rate. This limitation was circumvented by stepping the motion-encoding gradients nonlinearly, thereby probing higher velocities more accurately (up to a maximum displacement of 400 µm, corresponding to a maximum velocity of about 40 mm/s; Scheenen, 2001). The calculated volume flow values of the latter measurements, indicated with the white crosses in Figure 2, clearly fit the rate of root water uptake as measured with the balance. From days 3 to 6, the plant grew about 20 cm in length, which is noticeable by a steady increase in water uptake values of the plant during this period. Therefore, the intensity of light for the young upper leaves was certainly higher than 200 µmol m–2 s–1 during days 5, 6, and 7. The roots of the plant were cooled on day 6 from 12:20 PM to 4:20 PM. Water uptake decreased during this period to values below those measured the night before root cooling. Also, uptake the night following cooling reduced to approximately the values as observed during day 1, while the plant was recovering from transportation and insertion in the setup.
During root cooling, transpiration turned out to exceed water uptake, resulting in a net water loss that caused severe wilting of all leaves and the top of the stem (visual inspection; data not shown). After warming the roots to room temperature, water uptake recovered only partially (Fig. 2), but the plant restored turgor completely (visual estimation) within 2.5 h (except for the upper three small leaves that got damaged by the light in the absence of transpiration). This observation points to rapid, at least partial, recovery of the radial conductance of the roots upon rewarming (Berndt et al., 1999
Results from four MRI measurements are shown in Figure 3
, together with light microscopic images of a thin, hand-cut slice of the stem through the imaging plane (made after the MRI study). The different tissues indicated in the microscopic image of a part of the plant stem (Fig. 3A) can be recognized in both an image of the NMR spin-spin relaxation time T2 (Fig. 3B) and an image of the water content of the virtual MRI slice (Fig. 3C). The NMR single-parameter maps in Figure 3, B and C, are a result of the analysis of a multiecho imaging experiment (Edzes et al., 1998
Although only one thin transverse slice of the stem (at 35 cm from the roots) with a thickness of 3 mm was visualized in the NMR images, the cause of increased hydraulic resistance could immediately be found. Figure 3, C to E, represents the water content at different points in time, revealing cavitated vessels due to root cooling. The signal intensity of the lower right reference tube in these images is slightly attenuated due to saturation of the NMR signal in this tube. The red arrows in Figure 3D indicate four vessels (two embolizing vessels at arrow I) that were filled with water before root cooling (t = 130 h; Fig. 3B), empty 3.7 h after the period of root cooling (t = 140 h; Fig. 3C), and refilled again in the last night of the experiment (t = 170 h; Fig. 3D). Figure 3F is an enlarged view (light microscopy) of the embolized vessel indicated with arrow II in Figure 3D. The time course of embolism formation and refilling of these vessels will be examined in detail later. Figure 3, G to J, summarizes the results of one flow-imaging experiment: total amount of water per pixel (Fig. 3G), amount of stationary water per pixel (Fig. 3H), volume flow per pixel (Fig. 3I), and an overlay image of the volume flow (Fig. 3I) and the amount of stationary water (3 h; Fig. 3J). In addition, images representing the amount of flowing water and the linear flow velocity of the flowing water are available (data not shown). It is clear from Figure 3I that only a few large xylem vessels are responsible for most of the total volume flow through the slice. The sum of the volume flow of all pixels with flowing water represents the total volumetric water uptake through the slice, which corresponds with water uptake by the roots, measured with the precision balance, as presented in Figure 2 and discussed before. Instead of presenting the total sum of the volume flows of the flow-containing pixels, MRI flow imaging allows detailed study of the flow behavior in individual pixels or vessels. In the next section, we present detailed flow characteristics in time of some selected, small clusters of pixels in the images containing individual vessels or a small number of vessels. These pixels have been selected to demonstrate the quite diverse response to root cooling: about unaffected or slightly increased flow, embolized and refilling (but not yet functional), and nonflowing (filled) starting to flow. The flow characteristics in these pixels were very comparable in both the conventional and the optimized flow measurements (Fig. 2, diamonds and crosses).
The flow characteristics in time of one of four embolisms that were visible in the measured slice are examined in more detail here. The signals from five pixels, containing the embolizing vessel, indicated with the bottom red arrow (arrow II) in Figure 3, D and F, were added and reanalyzed as described by Scheenen et al. (2000b)
The flow characteristics of nine pixels immediately adjoining the refilling vessel (with vessels v1 and v2; Fig. 3F) were hardly affected by the formation and refilling of the embolism. According to the Hagen-Poiseuille law for laminar flow (Bird et al., 1960 ), the volume flow through a circular tube or vessel is related to the radius by the power of 4. This relation clarifies why the volume flow of the unaffected nine-pixel area was smaller than the volume flow of the embolizing vessel (Fig. 4A), whereas the amount of flowing water of v1 and v2 was larger (compare Fig. 4, B and C). The cross-sectional area of flow for v1 and v2, calculated from light microscopy, was 2.2 x 10–2 mm2 and 1.4 x 10–2 mm2. Although the vessels are not perfectly circular, the Hagen-Poiseuille law can be used to estimate the xylem pressure difference  Px over the vessels, which was assumed to be equal for v1, v2, and the embolizing vessel. Px of the embolizing vessel (Fig. 3, v2), before root cooling, needed to drive 0.49 mg water per second through a 0.2-mm-diameter vessel (estimated from a cross-sectional area of flow of 3.0 x 10–2 mm2), is 14 Pa/mm. Table I summarizes the kinetics of refilling for all vessels indicated with the red arrows in Figure 3D. The flow characteristics of the embolizing vessel in Figure 4, which were calculated from the alternative flow measurements (Fig. 2, white crosses), corresponded with those calculated from the conventional flow measurements (Fig. 2, squares), so the values from both measurements could be considered here (compare the ordinary symbols in Fig. 4 with the symbols in which a cross is drawn).
Apart from embolizing vessels, a vessel in which flow started after root cooling could also be found (Fig. 3D, blue arrow). Figure 5
reveals the flow characteristics of a selected area containing this vessel (five pixels) and of a neighboring area (six pixels), transporting water throughout the complete experiment. Even on day 3, around t = 67, there is no water transport in the selected area (data not shown). At t = 152 (2 h after the lights had been turned on; compare with Fig. 5, A and C) water transport in the vessel started and increased to 0.2 mg/s in 6 h. The total amount of water in the relevant area remains constant throughout the experiment: Before t = 152, all water was stationary; then about one-third of the water starts flowing (Fig. 5C). The cross-sectional area of flow of this vessel was 2.7 x 10–2 mm2, calculated from the NMR measurements, and 3.0 x 10–2 mm2, calculated from Figure 3F, corresponding with a circular vessel diameter of 0.2 mm. To obtain a volume flow of 0.2 mg/s, a
The amount of stationary and flowing water of the area next to the restoring vessel (at a distance of 0.5–0.6 mm) was not influenced by the restoration of flow or root cooling (Fig. 5B). However, the volume flow of this area on the day after root cooling was larger compared to the transpiring period before root cooling and the hours just after root cooling on day 6.
The accuracy of MRI to quantify sap flow and effective flow-conducting area is deduced from the comparison of the flow characteristics of the water by MRI with the results obtained for root water uptake and optical microscopy of the vessel dimensions. When proper MRI settings are used, the MRI flow results are in close agreement with the results obtained by monitoring the root water uptake (Fig. 2). Care has to be taken to cover the full dynamic range of the sap velocity. This can easily be reached either by adjusting the MRI settings (Windt et al., 2006 ) or by stepping the motion-encoding gradients nonlinearly, as applied here (Scheenen, 2001). Successful discrimination of stationary and flowing water in a single pixel is demonstrated by the agreement between the calculated cross-sectional area of some large vessels based on the MRI results and microscopic inspection (Table I): Parameters obtained by MRI range within 10% of those from microscopy. To the best of our knowledge, no other method is at present available to obtain this type of data in intact plants.
The development of the overall water uptake by the cucumber plant in the instrumental setup before root cooling indicates that the plant is healthy and growing (Fig. 2). The difference in water uptake between just before and 1 d after root cooling suggests a reduction in the rate-limiting hydraulic conductance of the plant. The decrease in radial conductance of the roots and increase in viscosity of the water (accounting for a decrease in flow by about 40%) by cooling is, at least partially, rapidly reversed on rewarming (Berndt et al., 1999 Investigating the temporal dynamics of embolizing vessels in more detail in Figure 4 revealed a few interesting phenomena. First, embolism formation, as observed on the basis of the drop in amount of flowing water (Fig. 4B) took about 3 h. This is unexpectedly long. Second, large embolized xylem vessels in the stem of the plant were refilled and the time scale of refilling is long; it took 5, 13, and 14 h to refill a length of only 3 mm (the observed slice) of the embolized vessels. Third, refilling occurred while nearby tissue and vessels were under tension, or at least functioned normally under the applied conditions.
The speed of refilling was on the order of 0.6 x 10–2 mm3/h. Having comparable refilling speeds, the smaller embolized vessel refilled faster (in the observed slice). Extrapolated linearly, it would take 17 to 47 h for every centimeter of a vessel to be refilled with water. Although it is not possible to resolve whether the speed of refilling is constant over a complete vessel from the presented data, it is clear that refilling of an embolized vessel in the stem of a cucumber plant under the applied environmental conditions is a slow process. This is contrary to what has been concluded for petioles of sunflower (Helianthus annuus; Canny, 1997
Refilling occurred while nearby tissue and vessels functioned normally under the applied conditions. The area adjoining an embolizing vessel at a distance no more than 0.4 mm was unaffected by embolism formation and refilling of the neighboring vessel (Fig. 4B). One explanation for this observation could be that water in the refilling vessel is completely isolated from water in surrounding vessels, as was hypothesized and investigated before (Holbrook and Zwieniecki, 1999
The volume flow of vessels v1 and v2 (Fig. 3F) was constant in the hours with lights on before root cooling on day 6, throughout days 7 and 8 (Fig. 4A). However, the volume flow of vessels near the vessel in which flow was restored was around 50% larger on days 7 and 8 compared to day 6 before root cooling (lights-on periods; Fig. 5A). These relative differences in volume flow (and therefore also in
Although we report observations of only one plant in this study, the amount of data and detail that is presented clearly demonstrates the new possibilities of the used MRI method in plant science. In future work, the combination of MRI and physiological measurements (e.g. a xylem or tissue pressure probe providing absolute values of xylem pressure during embolism formation and refilling, root pressure, transpiration normalized on leaf area, etc.) is needed to further clarify the mechanism of refilling. Changing the osmotic pressure in the root medium might induce a response in the rate of refilling, which could indicate the possible role of root pressure. The effect of cold girdling of part of the stem (Peuke et al., 2006 Here, we have shown a substantial leap forward in studying dynamics in long-distance sap flow transport and flow-conducting area. The accuracy, amount of data, and detail that are presented, in combination with the suggestions of additional MRI experiments, of this single plant in response to changes in environmental conditions stress new possibilities of the use of MRI methods for intact plant studies. It demonstrates the potential to further unravel the mystery of embolism formation and repair during normal and stress conditions.
Plant Material and NMR Imaging Setup Twenty-four-day-old, commercially grown cucumber (Cucumis sativus ‘Hurona’) plants were transferred from rock wool to an aerated, one-half Hoagland solution and grown for 5 weeks in a greenhouse at Wageningen University. A cylindrical jacket around the upper 10 cm of the roots maintained horizontal root expansion within a 4.5-cm diameter to facilitate insertion into the gradient probe of the instrumental setup. Flowers were pinched out and occasionally the bottom leaves of the plants were cut to clear the lower 50 cm of stem from leaves. Three days before the start of the measurements, one of the plants (approximately 1.6 m tall) was selected and moved from the greenhouse to the laboratory. A plastic mold was placed around the plant stem (approximately 35 cm from the roots) and a solenoid (15-mm diameter) was wound on this mold. Capacitors for tuning and matching fixed on a plastic support for attachment to the stem were connected to the coil to form a tuned circuit or radiofrequency (RF) probe for detection of the MRI signal. The roots of the plant were put through the 4.5-cm cylindrical bore of a gradient probe (Doty Scientific). Finally, the gradient probe, containing the plant with the RF probe, was positioned in a 0.7-T electromagnet (Bruker; Fig. 5). MRI experiments were performed with an SMIS console (SMIS Ltd). Water uptake by the roots of the plant was measured with a precision balance (LC3201D; Sartorius AG), sampling the average differential weight of the container with growth medium every 30 s. A heat exchanger in the container was able to cool and reheat the roots from 22°C to 3°C or vice versa in 5 min. The temperature in the climate chamber above the magnet was 25°C ± 2°C during the photoperiod (from 6 AM to 9 PM, relative humidity 65% ± 5%, illumination about 200 µmol m–2 s–1 photosynthetically active radiation, depending on position of the leaves) and 22°C ± 2°C at night.
The diameter of the xylem vessels in the vascular bundles of a cucumber plant ranges between 0.02 and 0.35 mm (Reinders, 1987
A crucial step in flow quantification is the discrimination between stationary and flowing water. The fact that the propagator for stationary water is symmetrical around zero displacement due to diffusion and that for flow is unidirectional with respect to zero displacement was used to separate the stationary from the flowing water. The signal in the nonflow direction was mirrored around zero displacement and subtracted from the signal in the flow direction to produce the displacement distribution of the flowing water. The signal amplitude is proportional to the density of the mobile protons, so the integral of the propagator provides a measure for the amount of water. Signal amplitude calibration is based on the signal of pure water present in reference tubes. The average velocity of the flowing water was then calculated using the amplitude weighted average of the velocity distribution. The volume flow rate or flux is calculated by taking the integral of amplitude times displacement of the velocity distribution. Using this approach, the following flow characteristics were extracted from the propagators for every pixel as described by Scheenen et al. (2000b)
We thank Ir. Jaap Nijsse from the laboratory of plant physiology for preparing the light microscopy pictures and an unknown referee for very valuable comments and suggestions. Received September 1, 2006; accepted April 16, 2007; published April 20, 2007.
1 This work was supported by the Dutch Technology Foundation, Applied Science Division of the Netherlands Organization for Scientific Research (project no. WBI 3493). 
2 Present address: Department of Radiology (667), Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands.
3 Present address: Institute of Imaging Science, MCN Vanderbilt University, Nashville, TN 37232. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: T.W.J. Scheenen (henk.vanas{at}wur.nl). www.plantphysiol.org/cgi/doi/10.1104/pp.106.089250 * Corresponding author; e-mail henk.vanas{at}wur.nl; fax 31–317–482725.
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