Non-invasive measurement of vulnerability to drought induced

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Running head: Non-invasive measurement of vulnerability to embolism 1 2 3 4 Corresponding author: 5 Brendan Choat 6 University of Western Sydney 7 Hawkesbury Institute for the Environment 8 Building L3.G.08 9 Hawkesbury Campus 10 Bourke St, Richmond 11 2753, NSW, Australia 12 Tel: +61 2 4570 1901 13 email: [email protected] 14 15 Research Area: Ecophysiology and Sustainability 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

Plant Physiology Preview. Published on November 2, 2015, as DOI:10.1104/pp.15.00732

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Title: Non-invasive measurement of vulnerability to drought induced embolism by X-35 ray microtomography. 36 37 Authors: 38 Brendan Choat 39 Eric Badel 40 Regis Burlett 41 Sylvain Delzon 42 Herve Cochard 43 Steven Jansen 44 45 Institutional addresses: 46 University of Western Sydney, Hawkesbury Institute for the Environment, Richmond 47 NSW 2753, Australia (B.C.); INRA, UMR 547 PIAF, F-63100 Clermont-Ferrand, 48 France Clermont and Université (E.B. and H.C.); Université Blaise-Pascal, UMR 547 49 PIAF, 63000 Clermont-Ferrand, France (E.B. and H.C.); INRA, University of 50 Bordeaux, UMR BIOGECO, F-33450 Talence, France. (R.B. and S.D.); Ulm 51 University, Institute for Systematic Botany and Ecology, Albert-Einstein-Allee 11, 52 89081 Ulm, Germany (S.J.). 53 54 55 Summary: X-ray computed microtomography provides a high resolution, non-56 invasive method to evaluate vulnerability to drought induced embolism in living, 57 intact plants. 58 59 60 61 62 63 64 65 66 67 68



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Footnotes: 69 1This research was supported by the European Research Council (ERC) under 70 Advanced Grant project TREEPEACE (grant agreement FP7-339728) and by the 71 ‘Investments for the Future’ programme (ANR-10-EQPX-16, XYLOFOREST) from 72 the French National Agency for Research. HC and EB thank French ANR-10-BLAN-73 1710 Pitbulles for travel funding for visits to the SLS. BC was supported by an 74 Australian Research Council Future Fellowship (FT130101115) and travel funding 75 provided by the International Synchrotron Access Program (ISAP) managed by the 76 Australian Synchrotron. 77 78 *Author for correspondence: Brendan Choat; email: [email protected] 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101



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Abstract 102 Hydraulic failure induced by xylem embolism is one of the primary mechanisms of 103 plant dieback during drought. However, many of the methods used to evaluate the 104 vulnerability of different species to drought induced embolism are indirect and 105 invasive, increasing the possibility that measurement artefacts may occur. Here we 106 utilize X-ray computed microtomography (microCT) to directly visualize embolism 107 formation in the xylem of living, intact plants with contrasting wood anatomy 108 (Quercus robur, Populus tremula x alba and Pinus pinaster). These observations 109 were compared with widely used centrifuge techniques that require destructive 110 sampling. MicroCT imaging provided detailed spatial information regarding the 111 dimensions and functional status of xylem conduits during dehydrated. Vulnerability 112 curves based on microCT observations of intact plants closely matched curves based 113 on the centrifuge technique for species with short vessels (P. tremula x alba) or 114 tracheids (P. pinaster). For ring porous Q. robur, the centrifuge technique 115 significantly overestimated vulnerability to embolism, indicating that caution should 116 be used when applying this technique to species with long vessels. These findings 117 confirm that microCT can be used to assess vulnerability to embolism on intact plants 118 by direct visualization. 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134



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INTRODUCTION 135 Theory describing the physiological mechanism that allows plants to extract water 136 from the soil and transport it many tens of metres in height has often been the subject 137 of intense debate (Tyree, 2003). Plants have evolved a water transport system that 138 relies on water sustaining a tensile force; as a result, xylem sap is at negative absolute 139 pressures (Dixon and Joly, 1895; Melcher et al., 1998; Wei et al., 1999). However, 140 this transport mechanism comes with its own set of problems. Most notably, water 141 under tension is prone to cavitation, which results in the formation of gas bubbles 142 (emboli) that block xylem conduits. Embolism reduces the capacity of the xylem 143 tissue to deliver water to the canopy, where it is required to maintain adequate levels 144 of cellular hydration (Tyree and Sperry, 1989). The probability of embolism occurring 145 in the xylem increases during drought with increasing tension in the xylem sap. 146 During prolonged and severe droughts, xylem embolism can reach lethal levels, 147 causing branch die back and ultimately plant death (Davis et al., 2002; Brodribb and 148 Cochard, 2009; Hoffmann et al., 2011; Choat, 2013; Urli et al., 2013). Water stress 149 induced embolism is now recognised as one of the principal causes of plant mortality 150 in response to extreme drought events (Anderegg, 2014). In the face of increasingly 151 severe droughts expected with rising global temperatures, hydraulic failure due to 152 embolism has the potential to cause widespread dieback of trees across all major 153 forest biomes (Choat et al., 2012). 154

The majority of techniques used to estimate cavitation resistance are indirect 155 and/or invasive, increasing the possibility of artefacts occurring during measurement 156 (Cochard et al., 2013). Artefacts relating to invasive techniques are particularly 157 relevant in this case since xylem sap under tension is in a metastable state and may 158 easily vaporize as a result of disturbance. Non-invasive imaging techniques offer the 159 potential to make direct observations of xylem function in intact plants at high 160 resolution and in real time. Non-invasive techniques include Magnetic Resonance 161 Imaging (MRI) (Holbrook et al., 2001; Kaufmann et al., 2009; Choat et al., 2010) and, 162 more recently, X-ray computed micro tomography (microCT) (Brodersen et al., 2010; 163 Charra-Vaskou et al., 2012; McElrone et al., 2012). MicroCT provides superior 164 spatial resolutions to MRI, with resolutions below 2 μm attainable for a plant stem of 165 4-5 mm in diameter. This allows for detailed analysis of embolism formation and 166 repair in the xylem, including spatial patterns of embolism spread between conduits 167 (Brodersen et al., 2013; Dalla-Salda et al., 2014). 168



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However, non-invasive imaging techniques have seldom been used to validate 169 indirect or invasive techniques used to estimate cavitation resistance. At this stage 170 only a handful of studies have utilized imaging technology to measure cavitation 171 resistance in trees (Cochard et al., 2014; Torres-Ruiz et al., 2014a) and these studies 172 employed a destructive mode of the technique in which small branches were cut off 173 the plant before scanning took place. Thus far, non-invasive imaging on intact plants 174 has only been used to measure cavitation resistance in two species, Vitis vinifera 175 (Choat et al., 2010; Brodersen et al., 2013) and Sequoia sempervirens (Choat et al., 176 2015). Further measurement of cavitation resistance using non-invasive imaging on 177 intact plants across a range of species is therefore a high priority. 178

These comparisons are particularly important because of the current debate 179 surrounding the invasive techniques (Cochard et al., 2013). Specifically, evidence 180 from a variety of experiments suggests that centrifuge and air injection techniques 181 underestimate cavitation resistance in species with long xylem vessels (Choat et al., 182 2010; Cochard et al., 2010; Ennajeh et al., 2011; Martin-StPaul et al., 2014; Torres-183 Ruiz et al., 2014a; Wang et al., 2014). This artefact occurs when samples placed into 184 centrifuge rotors or air injection collars have a large proportion of vessels that are cut 185 open at both ends of the segment. A number of studies have disputed this ‘open 186 vessel’ hypothesis and suggested that some versions of the centrifuge and air injection 187 techniques provide reliable estimates of cavitation resistance (Jacobsen and Pratt, 188 2012; Sperry et al., 2012; Tobin et al., 2013). Because there will always be 189 uncertainties associated with indirect measurements, non-invasive imaging using 190 intact plants provides the best option for resolving these methodological issues. 191

In this study synchrotron based microCT was utilized to investigate the 192 formation of drought induced embolism in the xylem of intact, potted plants. Three 193 species were selected to provide a range of contrasting xylem structures including 194 Quercus robur (ring-porous), Populus tremula x alba (diffuse porous) and Pinus 195 pinaster (tracheid bearing). Visualizations of xylem embolism in the stems of these 196 species during a sequence of natural dehydration were used to construct embolism 197 vulnerability curves. We hypothesised that (a) vulnerability curves based on microCT 198 observations would match vulnerability curves based on the centrifuge technique for 199 species with short vessels (Populus tremula x alba) or tracheid based xylem (Pinus 200 pinaster), and (b) the centrifuge technique would over estimate vulnerability to 201



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embolism in the long vesseled species (Quercus robur) due to the open vessel 202 artefact. 203 204 RESULTS 205 Vulnerability curves generated with the centrifuge method were in close agreement 206 with curves generated from microCT observations for P. tremula x alba and P. 207 pinaster (Fig. 1; Table 1). For these two species P50 was not significantly different (P 208 > 0.05) between curves generated by the microCT and Cavitron techniques. The 209 estimates of P50 obtained for Q. robur by the Cavitron method (-1.38 MPa) and static 210 centrifuge (-0.47 MPa) were significantly higher (P < 0.05) than P50 obtained from 211 microCT observation (-4.1 MPa) (Table 1). This difference was due to variation in 212 curve shape; the centrifuge curves for Q. robur exhibited a characteristic exponential 213 shape curve in which PLC increased rapidly at high water potentials. Although both 214 centrifuge curves for Q. robur were exponential in form, the P50 derived from the 215 static centrifuge method was significantly (P < 0.05) higher than that derived from the 216 Cavitron (Table 1). All other curves were sigmoidal, with PLC remaining close to 217 zero until a critical threshold was reached. Vessel length analysis revealed that 19% 218 (± 5% SE) of vessels were cut open at both ends of a 0.275 m long segment of Q. 219 robur. For P. tremula x alba, no vessels were cut open at both ends of 0.275 m long 220 segment. 221 Two and three dimensional analyses of microCT scan volumes provided 222 detailed information on the propagation of xylem embolism during dehydration. In 223 each of the three xylem types, ring-porous, diffuse porous and conifer, a very small 224 percentage of secondary xylem conduits were embolised at high water status in the 225 initial scans (Fig. 2). These embolised conduits often appeared to be isolated from 226 other embolised conduits within the scan volume, although this could only be 227 confirmed for P. pinaster (Fig. 3) because vessels in Q. robur and P. tremula x alba 228 extended out of the scan volume. In P. pinaster xylem, embolism appeared first in the 229 primary xylem adjacent to the pith and then in the inner ring of latewood tracheids. 230 Embolised tracheids were also frequently located adjacent to resin ducts (Fig. 2). In 231 both angiosperm and gymnosperm species, the majority of primary xylem conduits 232 were usually embolised at high water status and prior to the first scan (Supplemental 233 Fig. 1). With dehydration and increasing xylem tension, embolism spread from the 234 initially embolised conduits to create patches of embolised xylem throughout the 235



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cross section (Fig. 4). As dehydration continued these patches gradually converged 236 until almost all conduits were embolised (Fig. 4). 237 238 DISCUSSION 239 Synchrotron based microCT produced excellent visualization of xylem tissue in plants 240 for three woody plant species of differing xylem structure. Making observations on 241 living, intact plants avoided previously identified artefacts associated with cutting 242 (Wheeler et al., 2013; Torres-Ruiz et al., 2014b) and the presence of open vessels 243 (Cochard et al., 2010). The high quality of signal and contrast allowed for 244 measurement of xylem conduit dimensions to a resolution of 1.62 μm for both air and 245 water filled conduits. This offers a dramatic improvement over MRI, which has 246 previously been used for non-invasive assays of xylem function with spatial 247 resolution resolutions down to 20-40 μm (Holbrook et al., 2001; Kaufmann et al., 248 2009; Choat et al., 2010; Wang et al., 2013). In the context of measuring vulnerability 249 to embolism, one key benefit of achieving resolutions close to one micron is the 250 ability to calculate theoretical hydraulic conductance from conduit dimensions. The 251 impact of xylem embolism on hydraulic capacity can therefore be estimated with a 252 much greater degree of confidence. MicroCT thus provides a direct and unambiguous 253 assay of xylem functional status and serves as an excellent reference technique to 254 assess the reliability and accuracy of destructive techniques used to estimate 255 vulnerability to embolism (Cochard et al., 2014). 256 257 Comparison of methods to assess vulnerability to embolism 258 Vulnerability curves generated by the microCT observations closely matched curves 259 based on the Cavitron technique for P. tremula x alba and P. pinaster. This 260 demonstrates conclusively that the Cavitron technique provides an accurate and 261 precise measure of vulnerability to embolism in these species. In contrast, centrifuge 262 techniques significantly overestimated vulnerability to embolism in Q. robur, 263 particularly in the range of xylem water potentials from -0.25 MPa to -2.5 MPa. 264

The converse argument, that microCT observations underestimated 265 vulnerability in Q. robur, is unlikely but bears further discussion. One possibility is 266 that the X-ray beam may cause cavitation in dehydrating samples, either by heating or 267 X-ray absorption. However, we did not observe any cavitation resulting from repeated 268 scans at the same scan point (Supplemental Fig. S2). Furthermore, this artefact would 269



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be expected to cause differences in vulnerability that were in the opposite direction to 270 those observed, i.e. microCT curves would exhibit greater vulnerability than hydraulic 271 methods. A second possibility is that non-invasive imaging underestimates embolism 272 because many of the cells that appear water filled are still living and therefore non-273 functional (Jacobsen and Pratt, 2012). In this case, all microCT observations were 274 made late in the growing season so undifferentiated and immature conduits would be 275 expected to make up only a very small proportion of the total stem in the juvenile 276 wood of saplings. 277

Excising leaves in air for measurement of bagged leaf water potential has the 278 potential to create embolism in the stem xylem, although the extent was very limited 279 in older section of the stem. Removal of up to seven leaves did not result in new 280 cavitation in the two-year section of the stem close to the base of the plant 281 (Supplemental Fig. S2). This indicates that water potential measurements in our initial 282 experiments would have a very limited effect on PLC calculated from microCT 283 imaging given that all scans were made > 0.20 m below the point where leaves were 284 collected for water potential measurements. However, removal of leaves consistently 285 caused embolism in the xylem of current year stems when cuts were made within 0.05 286 m of the scan point. Overall, these results indicate that care must be taken when scans 287 are made close to the point leaf removal and that the number of leaves collected for 288 water potential measurements should be minimised. They also suggest that alternative 289 techniques for measurement of water potential that do not require damage to the 290 xylem (e.g. stem psychrometry, leaf disk psychrometry) should be considered for 291 these experiments. 292

The results shown here for Q. robur are also consistent with earlier findings that 293 centrifuge techniques overestimate vulnerability to embolism in species with long 294 vessels and provide further support for the ‘open vessel’ artefact hypothesis (Choat et 295 al., 2010; Cochard et al., 2010; McElrone et al., 2012; Martin-StPaul et al., 2014; 296 Torres-Ruiz et al., 2014a). Consistent with this, measurements of Q. robur saplings 297 indicated that over 19% of vessels were cut open at both ends in stem segments used 298 for centrifuge measurements. The most likely cause of this artefact is that 299 microbubbles, which move into the sample either prior to, or during the spinning 300 phase, lead to embolism formation when they reach the centre of the sample where 301 centrifugal forces are highest (Wang et al., 2014). This open vessel artefact has been 302 the subject of intense debate with some researchers suggesting that the artefact only 303



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affects the Cavitron version of the centrifuge technique and not the static centrifuge 304 method (Christman et al., 2012; Jacobsen and Pratt, 2012; Sperry et al., 2012; Tobin 305 et al., 2013; Hacke et al., 2015). Data from the present study demonstrate that static 306 and spin centrifuge techniques produced similarly biased results for Q. robur. This 307 finding agrees with previous work indicating that all centrifuge techniques 308 overestimate vulnerability to embolism in long vesselled species when compared to 309 reference curves generated by dehydration or non-invasive imaging (Torres-Ruiz et 310 al., 2014a). The higher P50 observed with the static centrifuge as compared with the 311 Cavitron is most probably due to variation in vessel length between samples (Wang et 312 al. 2014). 313

Based on these results we reiterate that caution should be used when applying 314 centrifuge based techniques to samples in which a large proportion of vessels are cut 315 open at both ends of the segment. In the case of conifers, there is no possibility that 316 tracheids will exceed the length of the rotor used in centrifuge measurements. 317 Although the microCT vulnerability curve was almost identical to the centrifuge 318 curve for P. tremula x alba, caution is still advised for diffuse porous species since 319 vessel lengths are highly variable (Zimmermann and Jeje, 1981; Sperry et al., 2006) 320 and may exceed rotor diameter in some cases. 321 322 Patterns of embolism spread with dehydration 323 Three dimensional analysis of scan volumes illustrated the fine spatial patterns of 324 embolism spread within each xylem type. These spatial analyses suggest that air 325 seeding through pit membranes was the dominant mechanism of cavitation in all three 326 xylem types. However, a small number of isolated, embolised conduits were observed 327 in both vessel and tracheid bearing species suggesting that other mechanisms of 328 cavitation may also operate in the xylem (Fig. 3 and Supplemental Fig. S1). 329

The majority of primary xylem conduits were embolised at high water status in 330 each of the three species (Supplemental Fig. S1). This is similar to the pattern 331 observed in intact grapevines using MRI (Choat et al., 2010) and microCT (Brodersen 332 et al., 2013) and extends this earlier finding across a range of xylem types. Single 333 vessel measurements indicate that protoxylem conduits are more vulnerable to air 334 seeding because they possess only partial secondary wall thickening and may suffer 335 damage during extension growth, which can cause stretching and rupture of the 336 primary cell walls (Choat et al., 2005). The secondary xylem of all species also 337



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contained a number of embolised conduits at the initial scan point. These embolised 338 conduits often appeared to be isolated from other air filled spaces within the scan 339 volume. However, in the vessel bearing species (Q. robur and P. tremula x alba), 340 vessels were always longer than the length of the scan volume (~5 mm). It was 341 therefore not possible to verify whether apparently isolated embolised conduits were 342 actually connected to other embolised conduits outside the scan volume. There were 343 also numerous embolised tracheids visible in the initial scans of P. pinaster stems that 344 were isolated from other air filled tracheids (Supplemental Fig S1). In this case we 345 were able to verify that these embolised tracheids were completely isolated from other 346 air spaces because tracheid lengths were less than the scan volume (Fig. 3). This 347 suggests that these tracheids may have become embolised by a mechanism other than 348 air seeding, e.g. defects in wall structure during initial formation, nucleation from 349 hydrophobic surface or vapour embryos (Pickard, 1981; Tyree et al., 1994; Schenk et 350 al., 2015). This is consistent with results of microCT observations on intact saplings 351 of Sequoia sempervirens, which also indicated the presence of isolated, embolised 352 tracheids (Choat et al., 2015). 353

With dehydration and increasing xylem tension, embolism spread from the 354 initially embolised vessels and tracheids. This pattern is consistent with air seeding 355 through pit membranes as the primary mechanism of cavitation in the xylem 356 (Zimmermann, 1983; Sperry and Tyree, 1988; Cochard et al., 1992; Choat et al., 357 2008). Although embolism was more frequent in the inner portions of the stem during 358 the early stages of dehydration, this pattern was not as distinct as the radial spread of 359 embolism observed in grapevine stems (Brodersen et al., 2013). In Q. robur, dendritic 360 bands of tracheids surrounding vessels and ray cells remained hydrated for the 361 duration of the experiment. In contrast, fibre cells were always observed to be air 362 filled. In the xylem of P. tremula x alba, fibres surrounding the vessels were also 363 embolised with the exception of a band close to the cambium (Fig. 4). This is similar 364 to the distribution of water observed by cryoSEM in the xylem of diffuse porous 365 species growing under well watered conditions (Utsumi et al., 1998). As P. tremula x 366 alba stems dehydrated, the water filled fibres close to the cambium gradually 367 embolised. 368 In P. pinaster xylem, embolism appeared first in the primary xylem adjacent 369 to the pith and then in the inner ring of latewood tracheids (Fig. 2). This is consistent 370 with observations of xylem from mature Douglas fir trees, which also demonstrates 371



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much higher vulnerability of latewood tracheids compared with earlywood (Dalla-372 Salda et al., 2014). Latewood tracheids may be more vulnerable to embolism because 373 of their pit structure. Anatomical work has shown that the margo in latewood 374 tracheids of many conifer species are inflexible and do not readily allow the torus to 375 seal the pit aperture in the event of air entry (Domec et al., 2006). This is also 376 apparent from the work of wood technologists, who have shown that latewood 377 remains unaspirated in dried wood samples (Petty, 1970). Embolism spread primarily 378 in the lateral direction, presumably because inter-tracheid pits are located almost 379 exclusively on the radial walls of tracheids. It is likely that much of this embolism 380 spread from the initially isolated embolised tracheid and small patches of tracheids 381 adjacent to resin ducts. Embolism then spread in a non-contiguous fashion between 382 rings, with some earlywood tracheids in the outer rings becoming embolised. This 383 pattern of embolism spread suggests differential resistance to cavitation along files of 384 tracheids in the growth ring, most probably related to variation in pit level traits 385 (Pittermann et al., 2010; Dalla-Salda et al., 2014). Embolism then spread outwards to 386 the cambium and back towards the pith until the majority of tracheids were 387 embolised. 388 389 Conclusions 390 The results of microCT observations confirm that this technique is an excellent non-391 invasive method for measurement of vulnerability to embolism with the principal 392 advantage that measurements can be made on intact plants. The high resolution of 393 images allowed for calculation of theoretical hydraulic conductivity based on xylem 394 conduit dimensions. We were therefore able to estimate the impact of embolised 395 vessels and tracheid on the hydraulic capacity of each sample. The fine spatial 396 patterns of embolism spread within the xylem could also be followed, providing 397 insight into the way cavitation is nucleated within the xylem. The results indicated 398 that centrifuge techniques overestimated vulnerability to embolism in ring porous Q. 399 robur, consistent with previous reports suggesting the centrifuge suffers from an open 400 vessel artefact when applied to long vesselled species (Choat et al., 2010; Cochard et 401 al., 2010; Torres-Ruiz et al., 2014a). However, the centrifuge produced curves that 402 were in excellent agreement with microCT observations for diffuse porous P. tremula 403 x alba and the conifer P. pinaster. These results provide further evidence that the 404 centrifuge technique is rapid and reliable method of assessing vulnerability to 405



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embolism in species with short vessels or tracheids, but is prone to errors when a high 406 proportion of vessels are cut open in the measurement sample. Caution is advised 407 when applying this technique to species with vessel lengths that exceed the diameter 408 of the rotor used in centrifuge methods. 409 410 MATERIALS AND METHODS 411 Plant material 412 Ten two-years-old oak (Quercus robur) and five one-year-old poplar (Populus 413 tremula x alba, clone INRA 717-1B4) saplings were grown at the laboratories in 414 INRA Bordeaux (44°44′N, 00°46′W) and Clermont-Ferrand (45.76° N, 3.14° E), 415 respectively. Oak seeds were collected in a natural population in Southern France, 416 while poplars were multiplied clonally by in-vitro micropropagation. After potting, 417 the plants were gradually acclimatized in a greenhouse under well watered conditions 418 (irrigated twice daily, ambient light and temperature). At the time of measurement, 419 sapling stems ranged between 0.4 to 0.8 m high with an average diameter of 4.5 mm 420 at the base. Plants were moved to the SLS (Swiss Light Source, Paul Scherrer 421 Institute, Switzerland) and scanned in September of 2012. 422

In July of 2013, fifty Pinus pinaster saplings were ordered from PlanFor nursery 423 (Mont de Marsan, France). All plants were two years old at the time of purchase. 424 Plants were repotted into 0.7 L pots and grown for one month under well watered 425 conditions (irrigated twice daily, ambient light and temperature) at the Ulm University 426 Botanical Gardens (48.4222° N, 9.9539° E). Plants were moved to the SLS and 427 scanned in September of 2013. Two weeks prior to the microCT imaging, drought 428 stress was induced in 20 plants by cessation of irrigation. In order to facilitate 429 dehydration vulnerability curves, plants were dried for varying periods to produce a 430 range of stem water potentials. At the time of measurement plants were 0.2-0.3 m in 431 height and 3-5 mm diameter at the stem base. Measurements using the static 432 centrifuge technique were applied to another set of 2-year old Q. robur saplings in 433 March of 2015. These saplings were grown in the greenhouse under identical 434 conditions to the first cohort of Q. robur seedlings. A third cohort of Q. robur 435 saplings, which had been raised outside of the greenhouse, was used for evaluation of 436 leaf removal in microCT experiments. 437 438 439



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X-ray computed microtomography 440 Synchrotron based computed microtomography (microCT) was used to visualize 441 embolised and water filled conduits in the main stem axes for each of the three 442 species. Potted plants were transported to the SLS tomography beamline (TOMCAT-443 X02DA). Tomographic scans were recorded during two allocations of beamtime. 444 Quercus robur and P. tremula x alba plants were visualized in September 2012, while 445 observations of P. pinaster were recorded in September 2013. 446

The measurement protocol used to scan living plants is described in detail in 447 McElrone et al. (2013). Potted plants were placed in a custom-built aluminium holder 448 that immobilized the stem and mounted on the TOMCAT sample stage. For each 449 plant, a 5 mm section of the main stem axis was scanned approximately 0.03 m above 450 the soil surface. Stems were positioned 30 mm from the 2D detector and secured to 451 bamboo or birch wood skewers (3 mm diameter) in order to minimize sample 452 movement during rotation of the stage. Plants were scanned at 20 keV in the 453 synchrotron X-ray beam while being rotated through 0 to 180 degrees using 454 continuous rotation mode. X-ray projections were collected at 0.12° steps with 150 455 ms exposure time during rotation with projection images magnified through a series 456 of lenses and relayed onto a sCMOS camera (pco.edge 5.5, PCO, Kelheim, Germany). 457 The scan time was less than four minutes for each sample. Samples were removed 458 between scans and placed under LED lighting to facilitate more rapid drying of plants. 459

Scans yielded 1500, 2D projections per sample. Raw 2D tomographic 460 projections were reconstructed into a single 3D volume that was then split into 461 approximately 2000 TIF image slices using software developed at the TOMCAT 462 beamline. The resulting images yielded images with a 1.625 µm voxel resolution. 463 These images were analyzed in imageJ (Rasband, 2014) and Avizo 8.1.1 software 464 (VSG, Inc., Burlington, MA) to determine the location and dimensions of embolised 465 vessels or the cross sectional area of embolised tracheids within each sample. 466

For Q. robur and P. tremula x alba, scans were made on five plants per species, 467 with plants scanned every three hours during dehydration. Plants were dried down in 468 pots under laboratory condition at the SLS facility. A red-blue LED light source was 469 secured 1 m above the potted plants. A fan was also used to increase the rate of 470 dehydration in Q. robur plants. P. pinaster plants were dehydrated at the Ulm 471 University Botanical Gardens prior to arrival at the SLS. In August 2013, plants were 472 moved to a rainout-shelter and divided into four groups. Water was withheld for one, 473



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two or three weeks prior to scanning, respectively for three of the groups. The fourth 474 group was maintained in well watered conditions. Each plant was scanned once at the 475 SLS. 476

Covered leaf water potential was measured on leaves or leafy twigs just prior to 477 scans using a Scholander Pressure Chamber (Plant Moisture Stress Model 600, 478 Albany, Oregon, USA). Leaves were covered with plastic bags and aluminium foil for 479 at least 30 min prior to each measurement of water potential. Due to concerns 480 regarding the impact of leaf removal for water potential measurements on cavitation 481 in the stem xylem, another set of observations were undertaken in April 2015 at the 482 SOLEIL microCT beamline (PSICHÉ). These measurements were conducted on 2-483 year old Q. robur plants grown at the laboratories in INRA Bordeaux (44°44′N, 484 00°46′W). Plants were first scanned close in the two-year old section of the stem 485 before any leaves were removed. After 15 minutes, plants were scanned again at the 486 same point to test whether the X-ray beam itself was causing cavitation. A leaf was 487 then removed from the apex of the plant, between 0.20-0.25 m above the scan point 488 and the plant was scanned for a third time after a further 15 minutes. The plant holder 489 was then moved down and the procedure was repeated at a scan point on the current 490 year shoot within 0.03-0.05 m of where leaves would be removed for water potential 491 measurements. This protocol was applied to two replicate plants. These measurements 492 indicated that (a) the X-ray beam did not induce cavitation in the stem during scans, 493 and (b) that removal of leaves for water potential measurements had the potential to 494 induce air entry and embolism in xylem vessels, although only in the current year 495 growth zone within 6 cm of where the leaf was removed (Supplemental Fig. S2). 496 497 Vulnerability curves based on microCT observations 498 Vulnerability curves were generated from microCT by estimating the theoretical 499 hydraulic conductance of each sample based on the conduit dimensions of embolised 500 and functional conduits. Measurements were made on transverse slices taken from the 501 centre of the scan volume. For angiosperm species, vessel diameters were measured 502 manually. To increase the accuracy of vessel diameter measurements, a final scan was 503 carried out on each stem after it had been cut in air. This ensured that all vessels were 504 air filled at the time of scanning, increasing the contrast with surrounding tissue. For 505 P. pinaster samples, a binary image was created for each transverse slice and the 506 dimensions of tracheids were automatically measured using the “analyze particles” 507



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function. A separate run was required to separate embolised from functional tracheids. 508 The “watershed” function was used to assist in separating tracheids that were 509 connected after the initial thresholding (Choat et al., 2007). 510

The maximum theoretical hydraulic conductance (kmax) of each stem was then 511 calculated as: 512 513

kmax = πD4/128η (1) 514 515

The current hydraulic conductance (kh) for each sample was then calculated by 516 subtracting the summed hydraulic conductance of embolised vessels from the kmax of 517 that sample. This calculation of hydraulic conductance does not include the hydraulic 518 resistance due to pits. Assuming that pit resistance scales with lumen resistance 519 (Choat et al. 2008), impairment of flow calculated with equation 1 should be 520 comparable with flow rates measured directly on the plant. The theoretical percent 521 loss of hydraulic conductance (PLCth) of the sample was therefore given by: 522 523

PLCth = 100 x (1 − kh / kmax) (2) 524 525 In all cases, measurements included all secondary xylem visible in the cross section of 526 a given sample. Primary xylem was excluded from calculations on the basis it had 527 become previously embolised in the majority of cases. Curve fitting and analysis of 528 curve parameters is described below. 529 530 Vulnerability curves based on hydraulic measurements 531 Vulnerability to xylem cavitation was assessed using two versions of the centrifuge 532 technique; the static centrifuge method described by Alder et al. (1997) and the in situ 533 flow technique (Cavitron) developed by Cochard (2002) and Cochard et al. (2005). 534 Both techniques employ centrifugal force to generate tension in the xylem of spinning 535 stem samples. In the Cavitron technique, the loss of hydraulic conductance is 536 measured while the sample is spinning (under tension) in the centrifuge. In the static 537 centrifuge technique, the sample is removed between spins to measure hydraulic 538 conductance on the bench top. The in situ flow and static versions of the centrifuge 539 technique have been shown to produce similar results (Li et al., 2008; Torres-Ruiz et 540



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al., 2014a). All hydraulic measurements were made with 10 mM KCl solution filtered 541 to 0.2 μm. 542

Cavitron measurements were carried out on all three species while static 543 centrifuge measurements were only conducted on Q. robur. Cavitron measurements 544 were conducted on the same population of two year old Q. robur plants as used for 545 microCT observations directly after the 2012 SLS beamtime allocation. Four-year old 546 P. pinaster plants were measured with the Cavitron in May of 2010. Three to five 547 replicates were measured per species at a high-throughput phenotyping platform for 548 hydraulic traits (Cavit_Place, University of Bordeaux, Talence, France). 549 Measurements were made using a custom-built honeycomb rotor (SamPrecis 2000, 550 Bordeaux, France) mounted on a Sorvall RC5 superspeed centrifuge (Thermo Fisher 551 Scientific, Munich, Germany). Cavitron vulnerability curves shown for P. tremula x 552 alba 717 1B4 are based on data from Awad et al. (2010). Samples of Q. robur and P. 553 pinaster were cut under water to a length of 0.27 m to fit into the static Cavitron rotor. 554 For Quercus, samples were flushed at ca. 0.15 MPa to remove any embolism until a 555 stable maximum kh value was reached prior to measurements. 556

Xylem pressure was first set to a reference pressure (-0.4 to -0.6 MPa) and the 557 maximal conductance (kmax) of the sample was determined once a stable value had 558 been reached. The xylem pressure was then set to a more negative value for 3 min and 559 the hydraulic conductance (kh) of the sample was again determined. The PLC at each 560 pressure step was calculated as per Eq. 2. The procedure was repeated for more 561 negative pressures (with 0.5 to 1.0 MPa increments) until PLC reached at least 90%. 562

Measurements using the static centrifuge technique were applied to another set 563 of 2-year old Q. robur saplings in March of 2015. Samples were spun to five xylem 564 tensions ranging between -0.3 MPa to -3.5 MPa. Foam pads saturated with perfusing 565 solution were added to reservoirs in the centrifuge rotor in order to ensure that the cut 566 ends of samples remained immersed in water during spinning (Hacke et al. 2015). 567 Measurements of hydraulic conductance between spins were made using a Sartorious 568 Practum analytical balance (0.01 mg resolution) connected to a computer with a 569 custom program recording flow and computing conductance (Graviflow, Univ 570 Bordeaux). Hydraulic conductance was calculated from the slope of three pressure 571 heads (0.13, 0.17 and 0.20 m) following the protocol described in Torres-Ruiz et al. 572 (2012). Pressure heads were kept low (< 0.0021 MPa) to avoid removal of embolism 573



18

from open vessels during flow measurements. All measurements were made on the 574 whole sample (0.27 m length) after at least two minutes of stable flow. 575

To facilitate comparison of Cavitron and static centrifuge vulnerability curves 576 for Q. robur, kmax of Cavitron measurements was calculated by extrapolating from the 577 first three measurements in the pressure series to the y-intercept. This provided an 578 estimate of kmax at a pressure of 0 MPa. This was necessary because the first Cavitron 579 measurement of kh was taken at -0.3 MPa, a point at which substantial PLC had 580 already occurred in the static centrifuge measurements. The offset calculated for 581 Cavitron kmax allowed for both curves to be scaled to kmax at Ψ = 0 MPa. A plot of 582 sapwood specific hydraulic conductivity (Ks) vs. xylem pressure is provided in 583 Supplemental Fig. S3. 584

585 Curve Fitting 586 All vulnerability curves were fitted using a Weibull function as reparameterized by 587 Ogle et al. (2009): 588

−−=

=

−=

1001ln)100(

1001

XXV

PPp

Xkk

VSP

x

p

sat

Xx (3) 589 590 where k is the relative hydraulic conductivity at X% loss of conductivity, ksat is the 591 saturated hydraulic conductivity (i.e. k at 0 MPa), P is the positive-valued xylem 592 water potential (P = -Ψ), Px is the Ψ at X% loss of conductivity, and Sx is the slope of 593 the vulnerability curve at P = Px. P50 was defined as Ψ at 50% loss of conductivity, 594 respectively. Eq. 3 was fit using non-linear least squares (function nls in R 3.0.1, R 595 Core Team (2013). A bootstrap resampling technique was employed to calculate 596 confidence intervals for the fitted parameters, by fitting the curve to resampled data 597 (999 replicates). The fitting routines were implemented as an R package (fitplc, 598 available from Duursma, 2014). Curves were fitted separately for each sample run in 599 centrifuge data with P50 and slope parameters then calculated as the means of three to 600 five replicates. In the Cavitron centrifuge data Q. robur exhibited a double curve. 601



19

Weibull curves were therefore fitted for separately for each half of the curve in order 602 to improve estimation of P50 (Cai et al., 2014). 603 604 Vessel lengths 605 The number of vessels open at both ends of a 0.275 m segment was measured by 606 injection of silicone elastomer (Rhodorsil RTV 141, Rhodia, Cranbury, NJ, USA) 607 with a fluorescent optical brightener (Ciba Uvitex OB; Ciba Specialty Chemicals, 608 Tarrytown, NY, USA) was mixed with chloroform (1% w/w) and added to the 609 silicone (Lens et al. 2011). Measurements were made on three stems of Q. robur and 610 P. tremula x alba. Stems were sealed in a pressure manifold with one cut end 611 submerged in elastomer. Samples were infiltrated at a pressure of 0.10 MPa for 24 612 hours and then oven dried at 70 °C overnight. Vessels were counted at both ends of 613 the stem with the difference between the proximal and distal end representing the 614 proportion of vessels cut open at both ends of the sample. 615 616 Supplemental Data 617 Supplemental Figure S1. Transverse slices from microCT scans show embolised and 618 functional xylem conduits for in well hydrated samples of (A) Quercus robur, (B) 619 Populus tremula x alba, and (C) Pinus pinaster. 620 621 Supplemental Figure S2. Sequential images from microCT scans showing the effects 622 of repeated scans and removal of leaves for water potential measurements. 623 624 Supplemental Figure S3. Vulnerability to drought induced embolism in Quercus 625 robur saplings using two centrifuge techniques. 626 627 ACKNOWLEDGMENTS 628 We gratefully acknowledge the Paul Scherrer Institut, Villigen, Switzerland for 629 provision of synchrotron radiation beamtime at the TOMCAT beamline. Sarah Irvine 630 and Kevin Mader are thanked for assistance with measurements at the TOMCAT 631 beamline. We also thank the SOLEIL synchrotron, France, for provision of beamtime 632 at the PSYCHE beamline. Andrew King is thanked for assistance with measurements 633 at the PSYCHE beamline. Andrew McElrone is thanked for supplying a specialized 634 plant holder for measurements at the SLS. Craig Brodersen is thanked for advice on 635



20

image analysis and 3D rendering. We thank Gaëlle Capdeville for assistance with 636 static centrifuge measurements made in 2015. 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669



21

Table 1. Xylem pressure at 50% loss of hydraulic conductance (P50) for three woody 670 species as determined by two centrifuge techniques and X-ray computed 671 microtomography (microCT). Within each row, different letters indicate significant 672 differences (P < 0.05) across techniques. Mean ± standard error (n= 3-5 for Cavitron 673 and static centrifuge measurements). 674 P50 (-MPa)

Species Cavitron Static centrifuge microCT

Quercus robur 1.38 (±0.10) a 0.47 (±0.09) b 4.16 (±0.16) c

Populus tremula x alba 1.83 (±0.05) a 1.81 (±0.02) a

Pinus pinaster 3.50 (±0.06) a 3.27 (±0.23) a

675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697



22

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Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Anderegg WRL (2014) Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts onvegetation. New Phytologist: doi: 10.1111/nph.12907


Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soilconditions. Physiologia Plantarum 139: 280-288


Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA (2013) In vivo visualizations of drought-inducedembolism spread in Vitis vinifera. Plant Physiology 161: 1820-1829


Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: In vivovisualizations using high resolution computed tomography. Plant Physiology 154: 1088-1095


Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. PlantPhysiology 149: 575-584


Cai J, Li S, Zhang HX, Zhang SX, Tyree MT (2014) Recalcitrant vulnerability curves: methods of analysis and the concept of fibrebridges for enhanced cavitation resistance. Plant Cell and Environment 37: 35-44


Charra-Vaskou K, Badel E, Burlett R, Cochard H, Delzon S, Mayr S (2012) Hydraulic efficiency and safety of vascular and non-vascular components in Pinus pinaster leaves. Tree Physiology 32: 1161-1170


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Choat B, Brodersen CR, McElrone AJ (2015) Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirenssaplings during cycles of drought and recovery. New Phytologist 205: 1095-1105


Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulicfunction. New Phytologist 177: 608-625


Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, Mcelrone AJ (2010) Measurement of vulnerability to waterstress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant Cell andEnvironment 33: 1502-1512


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Choat B, Sack L, Holbrook NM (2007) Diversity of hydraulic traits in nine Cordia species growing in tropical forests withcontrasting precipitation. New Phytologist 175: 686-698


Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous treespecies. New Phytologist 193: 713-720


Cochard H (2002) A technique for measuring xylem hydraulic conductance under high negative pressures. Plant Cell andEnvironment 25: 815-819


Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S (2013) Methods for measuring plant vulnerability to cavitation: acritical review. Journal of Experimental Botany 64: 4779-4791


Cochard H, Cruiziat P, Tyree MT (1992) Use of positive pressures to establish vulnerability curves - further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiology 100: 205-209


Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Ameglio T (2005) Evaluation of a new centrifuge technique for rapidgeneration of xylem vulnerability curves. Physiologia Plantarum 124: 410-418


Cochard H, Delzon S, Badel E (2014) X-ray microtomography (micro-CT): a reference technology for high-resolution quantificationof xylem embolism in trees. Plant Cell and Environment 38: 201-206


Cochard H, Herbette S, Barigah T, Badel E, Ennajeh M, Vilagrosa A (2010) Does sample length influence the shape of xylemembolism vulnerability curves? A test with the Cavitron spinning technique. Plant Cell and Environment 33: 1543-1552


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Hacke UG, Venturas MD, MacKinnon ED, Jacobsen AL, Sperry JS, Pratt RB (2015) The standard centrifuge method accuratelymeasures vulnerability curves of long-vesselled olive stems. New Phytologist: 205: 116-127


Hoffmann WA, Marchin RM, Abit P, Lau OL (2011) Hydraulic failure and tree dieback are associated with high wood density in atemperate forest under extreme drought. Global Change Biology 17: 2731-2742


Holbrook NM, Ahrens ET, Burns MJ, Zwieniecki MA (2001) In vivo observation of cavitation and embolism repair using magneticresonance imaging. Plant Physiology 126: 27-31


Jacobsen AL, Pratt RB (2012) No evidence for an open vessel effect in centrifuge-based vulnerability curves of a long-vesselledliana (Vitis vinifera). New Phytologist 194: 982-990


Kaufmann I, Schulze-Till T, Schneider HU, Zimmermann U, Jakob P, Wegner LH (2009) Functional repair of embolized vessels inmaize roots after temporal drought stress, as demonstrated by magnetic resonance imaging. New Phytologist 184: 245-256


Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, & Jansen S (2011). Testing hypotheses that link wood anatomy to cavitationresistance and hydraulic conductivity in the genus Acer. New phytologist 190: 709-723


Li YY, Sperry JS, Taneda H, Bush SE, Hacke UG (2008) Evaluation of centrifugal methods for measuring xylem cavitation inconifers, diffuse- and ring-porous angiosperms. New Phytologist 177: 558-568


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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hacke&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hacke&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hoffmann&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=In vivo observation of cavitation and embolism repair using magnetic resonance imaging&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://scholar.google.com/scholar?as_q=No evidence for an open vessel effect in centrifuge-based vulnerability curves of a long-vesselled liana (Vitis vinifera)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jacobsen&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kaufmann&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lens&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28The issue of %27open vessel%27 artifact in oaks%2E Tree Physiology%5BTitle%5D%29 AND 34%5BVolume%5D AND 894%5BPagination%5D AND Martin%2DStPaul NK%2C Longepierre D%2C Huc R%2C Delzon S%2C Burlett R%2C Joffre R%2C Rambal S%2C Cochard H%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Martin-StPaul&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28New Phytologist%5BTitle%5D%29 AND 196%5BVolume%5D AND 661%5BPagination%5D AND McElrone AJ%2C Brodersen CR%2C Alsina MM%2C Drayton WM%2C Matthews MA%2C Shackel KA%2C Wada H%2C Zufferey V%2C Choat B%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=McElrone&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Centrifuge technique consistently overestimates vulnerability to water stress-induced cavitation in grapevines as confirmed with high-resolution computed tomography&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Centrifuge technique consistently overestimates vulnerability to water stress-induced cavitation in grapevines as confirmed with high-resolution computed tomography&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=McElrone&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature%2E%5BTitle%5D%29 AND McElrone AJ%2C Choat B%2C Parkinson DY%2C MacDowell AA%2C Brodersen CR%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=McElrone&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Journal of Experimental Botany%5BTitle%5D%29 AND 49%5BVolume%5D AND 1757%5BPagination%5D AND Melcher PJ%2C Meinzer FC%2C Yount DE%2C Goldstein G%2C Zimmermann U%5BAuthor%5D&dopt=abstract

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