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In Vivo Magnetic Resonance Imaging of Xylem Vessel Contents in Woody Lianas

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In Vivo Magnetic Resonance Imaging of Xylem Vessel Contents in Woody Lianas Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2003? 2003 26?12051214 Original Article Magnetic resonance imaging of xylem contents M. J. Clearwater & C. J. Clark Plant, Cell and Environment (2003) 26, 1205–1214 In vivo magnetic resonance imaging of xylem vessel contents in woody lianas M. J. CLEARWATER1 & C. J. CLARK2 1Horticulture and Food Research Institute of New Zealand, Te Puke Research Center, RD 2 Te Puke, New Zealand and 2Horticulture and Food Research Institute of New Zealand, Ruakura Research Center, East Street, Private Bag 3123, Hamilton, New Zealand ABSTRACT INTRODUCTION Previous reports suggest that in some plant species the Much recent attention has been focused on the possible refilling of embolized xylem vessels can occur while nega- occurrence of daily variation in the proportion of embo- tive pressure exists in the xylem. The aim of this experiment lized vessels in living, transpiring plants (e.g. Salleo & was to use non-destructive nuclear magnetic resonance Logullo 1989; Grace 1993; Canny 1997; Zwieniecki & Hol- imaging (MRI) to study the dynamics of xylem cavitation brook 1998; Holbrook & Zwieniecki 1999; Melcher et al. and embolism repair in-vivo. Serial 1H-MRI was used to 2001). Cavitation and the subsequent formation of emboli monitor the contents of xylem vessels in stems of two dicot- in xylem conduits was previously thought to be irreversible, yledonous (Actinidia deliciosa and Actinidia chinensis, or reversible only over long time scales and when pressure kiwifruit) and one monocotyledonous (Ripogonum scan- in the xylem was close to or above atmospheric pressure dens, supplejack) species of woody liana. The configuration (Sperry et al. 1994; Magnani & Borghetti 1995; Sperry of the horizontal wide bore magnet and probe allowed the 1995). Recent studies using a variety of direct and indirect imaging of woody stems up to 20mm in diameter. Tests techniques, described below, have provided compelling evi- using excised stems confirmed that the image resolution of dence that in some species embolized vessels can refill in 78mm and digital image subtraction could be used to detect minutes or hours, and that refilling may occur during tran- the emptying and refilling of individual vessels. Imaging spiration while the sap in neighbouring vessels is under was conducted on both intact plants and excised shoots significant tension. If the existence of a mechanism for the connected to a water supply. In the case of Ripogonum the refilling of embolized vessels under tension can be demon- excised shoots were long enough to allow the distal end of strated it will have important consequences for our under- the shoot, including all leaves, to be exposed to ambient standing of long-distance transport and water use by plants conditions outside the building while the proximal end was (Holbrook & Zwieniecki 1999; Tyree et al. 1999). However, inside the MRI magnet. In total, six stems were monitored because of the difficulty of accessing the xylem without for 240h while the shoots were subjected to treatments that disrupting its contents, few reports have provided unequiv- included light and dark periods, water stress followed by ocal evidence of refilling under tension in intact plants. re-watering, and the covering of all leaves to prevent tran- Nuclear magnetic resonance imaging (MRI) is one method spiration. The sudden emptying of water-filled vessels that provides the opportunity to non-destructively image occurred frequently while xylem water potential was low the contents of xylem vessels in vivo (Callaghan, Clark, & (below -0.5MPa for Actinidia, -1.0MPa for Ripogonum), Forde 1994; Holbrook et al. 2001). In this study we use MRI and less frequently after xylem water potential approached to non-destructively monitor changes in the contents of zero at the end of water-stress treatments. No refilling of individual xylem vessels in three species of woody liana. empty vessels was observed at any time in any of the species What evidence is there for refilling under tension? examined. It is concluded that embolism repair under neg- Indirect methods are commonly used for estimating the ative pressure does not occur in the species examined here. proportion of embolized xylem conduits. These include Embolism repair may be more likely in species with nar- measurement of variation in hydraulic conductivity (Salleo rower xylem vessels, but further experiments are required et al. 1996; Tyree et al. 1999; Zwieniecki et al. 2000; Melcher with other species before it can be concluded that repair et al. 2001), measuring the volume of gas bubbles in sap during transpiration is a widespread phenomenon. aspirated from the xylem (Pate & Canny 1999), and record- ing the proportion of stained vessel walls after stems are Key-words: Ripogonum; Actinidia; cavitation; embolism excised and supplied with dye (Salleo & Logullo 1989; repair; negative pressure; transpiration; water transport. Zwieniecki & Holbrook 1998). In some examples refilling conforms with physical laws governing the dissolution of Correspondence: Michael J. Clearwater. Fax:+64 75733871; e-mail: gas from bubbles within the xylem when tension is very low [email protected] (Borghetti et al. 1991; Tyree & Yang 1992; Yang & Tyree © 2003 Blackwell Publishing Ltd 1205 1206 M. J. Clearwater & C. J. Clark 1992; Sobrado, Grace, & Jarvis 1992). In other cases appar- versus 20mm), but the diameter of stems that could be ent increases in the proportion of water-filled conduits have imaged was larger (20 versus 6mm). The associated higher been observed at xylem tensions much higher than those total leaf area of the plants also meant that xylem pressure that would allow an explanation by any conventional the- potential could be measured more frequently using excised ories concerning xylem water transport (e.g. Salleo & leaves and a pressure chamber without significantly altering Logullo 1989). In most examples measurements are the overall water balance of the plant. Given the lower destructive, within-treatment variability is high, and there image resolution we first needed to confirm that this con- are sometimes other possible explanations for the observed figuration could resolve the contents of individual vessels, variation in hydraulic conductivity, such as changes in sap and we tested the use of digital image subtraction to detect ion concentration or variation in sap viscosity with temper- changes in vessel contents within an image plane that ature (Cochard et al. 2000b; Zwieniecki, Melcher, & Hol- included large numbers of water- and gas-filled vessels. The brook 2001). Refilling may also be observed in experiments system was then used to image vessel contents in stems of that make use of excised and dehydrated shoots that are intact and excised shoots subjected to a variety of treat- then bagged, thus preventing further evaporation and nor- ments. The species used were selected for large vessel diam- mal transpirational flow (Salleo et al. 1996; Tyree et al. eter (>100mm), for a liana growth habit, and for contrasting 1999). monocotyledon and dicotyledon xylem anatomy. Actinidia In addition to indirect measurements there are also two deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var. deli- methods for directly observing the contents of xylem con- ciosa ‘Hayward’ and Actinidia chinensis Planch. var. chin- duits – cryo-scanning electron microscopy (cryo-SEM) and ensis ‘Hort16A’ (Actinidiaceae; green- and yellow-fleshed MRI. Canny and others have provided numerous examples kiwifruit, respectively) are dicotyledonous, deciduous and of daily cycles of vessels emptying and refilling by rapidly have diffuse-porous or semi-ring porous secondary xylem freezing stems and roots of transpiring plants using liquid anatomy with numerous vessels embedded in a matrix of N2 and imaging the xylem using the SEM (Canny 1997; fibre-tracheids and multiseriate rays (Ferguson 1990; Con- Buchard, McCully, & Canny 1999; Melcher et al. 2001; Fac- don 1992; Dichio et al. 1999; Fig.1). Ripogonum scandens ette et al. 2001). However, this method is destructive and Forst. (Smilacaceae; supplejack, kareao), in contrast, is a has been strongly criticized over the possibility that the monocotyledon with subterranean branching rhizomes and emptying of vessels may be an artifact caused by freezing indeterminate, cataphyll-bearing, woody climbing stems up of xylem under tension (McCully et al. 2000; Cochard et al. to 20mm in diameter and 20m or more in length. Vascular 2000a; Canny, McCully, & Huang 2001; Richter 2001). bundles are scattered, smaller at the periphery of the stem While debate over the validity of the cryo-SEM method than in the centre, and usually contain two large collateral continues, MRI provides a non-destructive alternative, meta-xylem elements (Simpson & Philipson 1969; Mac- allowing the serial imaging of xylem in intact, transpiring millan 1972; Fig.1). Collenchyma sheaths associated with plants. MRI has recently been used to measure bulk flow the bundles and confluent around the periphery make the velocities in plant vascular tissue (Kockenberger et al. 1997; stems extremely durable and flexible (Macmillan 1972). Rokitta et al. 1999; Wistuba et al. 2000; Scheenen et al. Ripogonum is an unusual and distinctive feature of native 2002), and to study the refilling kinetics of resurrection New Zealand forest where its abundant, intertwining plants (Wagner et al. 2000). In the first attempt to observe climbing stems often make travel on foot difficult. the refilling
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