Advertisement

Annals of Forest Science

, 75:88 | Cite as

An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L.

  • Laurent J. Lamarque
  • Déborah Corso
  • José M. Torres-Ruiz
  • Eric Badel
  • Timothy J. Brodribb
  • Régis Burlett
  • Guillaume Charrier
  • Brendan Choat
  • Hervé Cochard
  • Gregory A. Gambetta
  • Steven Jansen
  • Andrew King
  • Nicolas Lenoir
  • Nicolas Martin-StPaul
  • Kathy Steppe
  • Jan Van den Bulcke
  • Ya Zhang
  • Sylvain Delzon
Research Paper

Abstract

Key message

Direct, non-invasive X-ray microtomography and optical technique observations applied in stems and leaves of intact seedlings revealed that laurel is highly resistant to drought-induced xylem embolism. Contrary to what has been brought forward, daily cycles of embolism formation and refilling are unlikely to occur in this species and to explain how it copes with drought.

Context

There has been considerable controversy regarding xylem embolism resistance for long-vesselled angiosperm species and particularly for the model species for refilling (Laurus nobilis L.).

Aims

The purpose of this study was to resolve the hydraulic properties of this species by documenting vulnerability curves of different organs in intact plants.

Methods

Here, we applied a direct, non-invasive method to visualize xylem embolism in stems and leaves of intact laurel seedlings up to 2-m tall using X-ray microtomography (microCT) observations and the optical vulnerability technique. These approaches were coupled with complementary centrifugation measurements performed on 1-m long branches sampled from adult trees and compared with additional microCT analyses carried out on 80-cm cut branches.

Results

Direct observations of embolism spread during desiccation of intact laurels revealed that 50% loss of xylem conductivity (Ψ50) was reached at − 7.9 ± 0.5 and − 8.4 ± 0.3 MPa in stems and leaves, respectively, while the minimum xylem water potentials measured in the field were − 4.2 MPa during a moderate drought season. Those findings reveal that embolism formation is not routine in Laurus nobilis contrary to what has been previously reported. These Ψ50 values were close to those based on the flow-centrifuge technique (− 9.2 ± 0.2 MPa), but at odds with microCT observations of cut branches (− 4.0 ± 0.5 MPa).

Conclusion

In summary, independent methods converge toward the same conclusion that laurel is highly resistant to xylem embolism regardless its development stage. Under typical growth conditions without extreme drought events, this species maintains positive hydraulic safety margin, while daily cycles of embolism formation and refilling are unlikely to occur in this species.

Keywords

Xylem embolism Drought resistance Laurel Refilling Hydraulics Desiccation 

Notes

Acknowledgements

We thank the PSICHE beamline (SOLEIL synchrotron facility, project 20150954) as well as the Experimental Unit of Pierroton (UE 0570, INRA, 69 route d’Arcachon, 33612 CESTAS, France) for providing the plant material.

Funding information

L.J.L. was granted a fellowship (UB101 CR1024-R s/CR1024-6M) from the IdEx Bordeaux International Post-doctoral Program. This work was supported by the program “Investments for the Future” (ANR-10-EQPX-16, XYLOFOREST) from the 49 French National Agency for Research and the T4F grant n° 284181 “Trees4Future” (“Non-invasive measurements of drought stress in trees”), which made microtomography at UGCT possible. B.C. was supported by an Australian Research Council Future Fellowship (FT130101115) and travel funding from the International Synchrotron Access Program (ISAP) managed by the Australian Synchrotron.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

13595_2018_768_MOESM1_ESM.docx (2.9 mb)
ESM 1 (DOCX 2932 kb)

References

  1. Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301.  https://doi.org/10.1007/BF00328731 CrossRefPubMedGoogle Scholar
  2. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684.  https://doi.org/10.1016/j.foreco.2009.09.001 CrossRefGoogle Scholar
  3. Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:art129.  https://doi.org/10.1890/es15-00203.1 CrossRefGoogle Scholar
  4. Anderegg WRL, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak M, Ogle K, Shaw JD, Shevliakova E, Williams AP, Wolf A, Ziaco E, Pacala S (2015) Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349:528–532.  https://doi.org/10.1126/science.aab1833 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Anderegg WRL, Martinez-Vilalta J, Cailleret M, Camarero JJ, Ewers BE, Galbraith D, Gessler A, Grote R, C-y H, Levick SR, Powell TL, Rowland L, Sánchez-Salguero R, Trotsiuk V (2016) When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems 19:1133–1147.  https://doi.org/10.1007/s10021-016-9982-1 CrossRefGoogle Scholar
  6. Arroyo-Garcia R, Martinez-Zapater JM, Fernandez Prieto JA, Alvarez-Arbesu R (2001) AFLP evaluation of genetic similarity among laurel populations (Laurus L.). Euphytica 122:155–164.  https://doi.org/10.1023/A:1012654514381 CrossRefGoogle Scholar
  7. Barigah TS, Charrier O, Douris M, Bonhomme M, Herbette S, Ameglio T, Fichot R, Brignolas F, Cochard H (2013) Water stress-induced xylem hydraulic failure is a causal factor of tree mortality in beech and poplar. Ann Bot 112:1431–1437.  https://doi.org/10.1093/aob/mct204 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Benito Garzón M, Gonzalez Munoz N, Wigneron J-P, Moisy C, Fernandez-Manjarres J, Delzon S (2018) The legacy of water deficit on populations having experienced negative hydraulic safety margin. Glob Ecol Biogeogr 27:346–356.  https://doi.org/10.1111/geb.12701 CrossRefGoogle Scholar
  9. Bouche PS, Delzon S, Choat B, Badel E, Brodribb TJ, Burlett R, Cochard H, Charra-Vaskou K, Lavigne B, Li S, Mayr S, Morris H, Torres-Ruiz JM, Zufferey V, Jansen S (2016a) Are needles of Pinus pinaster more vulnerable to xylem embolism than branches? New insights from X-ray computed tomography. Plant Cell Environ 39:860–870.  https://doi.org/10.1111/pce.12680 CrossRefPubMedGoogle Scholar
  10. Bouche PS, Jansen S, Sabalera JC, Cochard H, Burlett R, Delzon S (2016b) Low intra-tree variability in resistance to embolism in four Pinaceae species. Ann For Sci 73:681–689.  https://doi.org/10.1007/s13595-016-0553-6 CrossRefGoogle Scholar
  11. Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol 154:1088–1095.  https://doi.org/10.1104/pp.110.162396 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584.  https://doi.org/10.1104/pp.108.129783 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brodribb TJ, Bowman DJ, Nichols S, Delzon S, Burlett R (2010) Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol 188:533–542.  https://doi.org/10.1111/j.1469-8137.2010.03393.x CrossRefPubMedGoogle Scholar
  14. Brodribb TJ, Bowman DMJS, Grierson PF, Murphy BP, Nichols S, Prior LD (2013) Conservative water management in the widespread conifer genus Callitris. AoB Plants 5:plt052.  https://doi.org/10.1093/aobpla/plt052 CrossRefPubMedCentralGoogle Scholar
  15. Brodribb TJ, Bienaime D, Marmottant P (2016a) Revealing catastrophic failure of leaf networks under stress. Proc Natl Acad Sci U S A 113:4865–4869.  https://doi.org/10.1073/pnas.1522569113 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Brodribb TJ, Skelton RP, McAdam SA, Bienaime D, Lucani CJ, Marmottant P (2016b) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol 209:1403–1409.  https://doi.org/10.1111/nph.13846 CrossRefPubMedGoogle Scholar
  17. Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez-Castillo M, Rockwell FA, Manna LL, Guerra P, Bernal PL, Troncoso O, Enricci J, Holbrook MN, Goldstein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiol 32:880–893.  https://doi.org/10.1093/treephys/tps054 CrossRefPubMedGoogle Scholar
  18. Cailleret M, Jansen S, Robert EM, Desoto L, Aakala T, Antos JA, Beikircher B, Bigler C, Bugmann H, Caccianiga M, Cada V, Camarero JJ, Cherubini P, Cochard H, Coyea MR, Cufar K, Das AJ, Davi H, Delzon S, Dorman M, Gea-Izquierdo G, Gillner S, Haavik LJ, Hartmann H, Heres AM, Hultine KR, Janda P, Kane JM, Kharuk VI, Kitzberger T, Klein T, Kramer K, Lens F, Levanic T, Linares Calderon JC, Lloret F, Lobo-Do-Vale R, Lombardi F, Lopez Rodriguez R, Makinen H, Mayr S, Meszaros I, Metsaranta JM, Minunno F, Oberhuber W, Papadopoulos A, Peltoniemi M, Petritan AM, Rohner B, Sanguesa-Barreda G, Sarris D, Smith JM, Stan AB, Sterck F, Stojanovic DB, Suarez ML, Svoboda M, Tognetti R, Torres-Ruiz JM, Trotsiuk V, Villalba R, Vodde F, Westwood AR, Wyckoff PH, Zafirov N, Martinez-Vilalta J (2017) A synthesis of radial growth patterns preceding tree mortality. Glob Chang Biol 23:1675–1690.  https://doi.org/10.1111/gcb.13535 CrossRefPubMedGoogle Scholar
  19. Charrier G, Torres-Ruiz JM, Badel E, Burlett R, Choat B, Cochard H, Delmas CE, Domec JC, Jansen S, King A, Lenoir N, Martin-StPaul N, Gambetta GA, Delzon S (2016) Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiol 172:1657–1668.  https://doi.org/10.1104/pp.16.01079 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Charrier G, Delzon S, Domec J-C, Zhang L, Delmas CEL, Merlin I, Corso D, King A, Ojeda H, Ollat N, Prieto J, Scholach T, Skinner P, van Leeuwen C, Gambetta GA (2018) Leaf mortality and a dynamic hydraulic safety margin prevent significant stem embolism in the world’s top wine regions during drought. Sci. Adv. 4:eaao6969.  https://doi.org/10.1126/sciadv.aao6969 CrossRefGoogle Scholar
  21. Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089.  https://doi.org/10.1111/j.1365-3040.2005.01336.x CrossRefGoogle Scholar
  22. Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant Cell Environ 33:1502–1512.  https://doi.org/10.1111/j.1365-3040.2010.02160.x CrossRefPubMedGoogle Scholar
  23. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755.  https://doi.org/10.1038/nature11688 CrossRefPubMedGoogle Scholar
  24. Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S (2016) Noninvasive measurement of vulnerability to drought-induced embolism by X-ray microtomography. Plant Physiol 170:273–282.  https://doi.org/10.1104/pp.15.00732 CrossRefPubMedGoogle Scholar
  25. Clearwater M, Goldstein G (2005) Embolism repair and long distance transport. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier, Amsterdam, pp 201–220Google Scholar
  26. Cochard H (2002) A technique for measuring xylem hydraulic conductance under high negative pressures. Plant Cell Environ 25:815–819.  https://doi.org/10.1046/j.1365-3040.2002.00863.x CrossRefGoogle Scholar
  27. Cochard H, Delzon S (2013) Hydraulic failure and repair are not routine in trees. Ann For Sci 70:659–661.  https://doi.org/10.1007/s13595-013-0317-5 CrossRefGoogle Scholar
  28. Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Améglio T (2005) Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiol Plant 124:410–418.  https://doi.org/10.1111/j.1399-3054.2005.00526.x CrossRefGoogle Scholar
  29. Cochard H, Tete Barigah S, Kleinhentz M, Eshel A (2008) Is xylem cavitation resistance a relevant criterion for screening drought resistance among Prunus species? J Plant Physiol 165:976–982.  https://doi.org/10.1016/j.jplph.2007.07.020 CrossRefPubMedGoogle Scholar
  30. Cochard H, Herbette S, Barigah T, Badel E, Ennajeh M, Vilagrosa A (2010) Does sample length influence the shape of xylem embolism vulnerability curves? A test with the Cavitron spinning technique. Plant Cell Environ 33:1543–1552.  https://doi.org/10.1111/j.1365-3040.2010.02163.x CrossRefPubMedGoogle Scholar
  31. Cochard H, Delzon S, Badel E (2015) X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. Plant Cell Environ 38:201–206.  https://doi.org/10.1111/pce.12391 CrossRefPubMedGoogle Scholar
  32. Cohen S, Bennink J, Tyree M (2003) Air method measurements of apple vessel length distributions with improved apparatus and theory. J Exp Bot 54:1889–1897.  https://doi.org/10.1093/jxb/erg202 CrossRefPubMedGoogle Scholar
  33. Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Chang 3:52–58.  https://doi.org/10.1038/nclimate1633 CrossRefGoogle Scholar
  34. David-Schwartz R, Paudel I, Mizrachi M, Delzon S, Cochard H, Lukyanov V, Badel E, Capdeville G, Shklar G, Cohen S (2016) Indirect evidence for genetic differentiation in vulnerability to embolism in Pinus halepensis. Front Plant Sci 7:768.  https://doi.org/10.3389/fpls.2016.00768 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Delzon S, Cochard H (2014) Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytol 203:355–358.  https://doi.org/10.1111/nph.12798 CrossRefPubMedGoogle Scholar
  36. Dierick M, Masschaele B, Van Hoorebeke L (2004) Octopus, a fast and user-friendly tomographic reconstruction package developed in LabView®. Meas Sci Technol 15:1366–1370.  https://doi.org/10.1088/0957-0233/15/7/020 CrossRefGoogle Scholar
  37. Diffenbaugh NS, Swain DL, Touma D (2015) Anthropogenic warming has increased drought risk in California. Proc Natl Acad Sci U S A 112:3931–3936.  https://doi.org/10.1073/pnas.1422385112 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fields CB, Barros V, Stocker TF, Qin D, Dokken DJ, Ebi KL, Mastrandrea MD, Mach KJ, Plattner GK, Allen SK, Tignor M, Midgley PM (2012) Managing the risks of extreme events and disasters to advance climate change adaptation. In: A special report of working groups I and II of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  39. Gonzalez-Munoz N, Sterck F, Torres-Ruiz JM, Petit G, Cochard H, von Arx G, Lintunen A, Caldeira MC, Capdeville G, Copini P, Gebauer R, Gronlund L, Holtta T, Lobo-do-Vale R, Peltoniemi M, Stritih A, Urban J, Delzon S (2018) Quantifying in situ phenotypic variability in the hydraulic properties of four tree species across their distribution range in Europe. PLoS One 13:e0196075.  https://doi.org/10.1371/journal.pone.0196075 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311.  https://doi.org/10.1046/j.1365-3040.2003.00962.x CrossRefGoogle Scholar
  41. Hacke UG, Venturas MD, MacKinnon ED, Jacobsen AL, Sperry JS, Pratt RB (2015) The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems. New Phytol 205:116–127.  https://doi.org/10.1111/nph.13017 CrossRefPubMedGoogle Scholar
  42. Hillabrand RM, Hacke UG, Lieffers VJ (2016) Drought-induced xylem pit membrane damage in aspen and balsam poplar. Plant Cell Environ 39:2210–2220.  https://doi.org/10.1111/pce.12782 CrossRefPubMedGoogle Scholar
  43. Hochberg U, Albuquerque C, Rachmilevitch S, Cochard H, David-Schwartz R, Brodersen CR, McElrone A, Windt CW (2016) Grapevine petioles are more sensitive to drought induced embolism than stems: evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation. Plant Cell Environ 39:1886–1894.  https://doi.org/10.1111/pce.12688 CrossRefPubMedGoogle Scholar
  44. Hochberg U, Windt CW, Ponomarenko A, Zhang YJ, Gersony J, Rockwell FE, Holbrook NM (2017) Stomatal closure, basal leaf embolism, and shedding protect the hydraulic integrity of grape stems. Plant Physiol 174:764–775.  https://doi.org/10.1104/pp.16.01816 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hogg E, Brandt J, Michaellian M (2008) Impacts of a regional drought on the productivity, dieback, and biomass of western Canadian aspen forests. Can J For Res 38:1373–1384.  https://doi.org/10.1139/X08-001 CrossRefGoogle Scholar
  46. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419.  https://doi.org/10.3732/ajb.0800248 CrossRefPubMedGoogle Scholar
  47. Jansen S, Schuldt B, Choat B (2015) Current controversies and challenges in applying plant hydraulic techniques. New Phytol 205:961–964.  https://doi.org/10.1111/nph.13229 CrossRefPubMedGoogle Scholar
  48. Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374. https://doi.org/10.1890/1540-9295(2007)5[365:ANGOCE]2.0.CO;2CrossRefGoogle Scholar
  49. King A, Guignot N, Zerbino P, Boulard E, Desjardins K, Bordessoule M, Leclerq N, Le S, Renaud G, Cerato M, Bornert M, Lenoir N, Delzon S, Perrillat J-P, Legodec Y, Itié J-P (2016) Tomography and imaging at the PSICHE beam line of the SOLEIL synchrotron. Rev Sci Instrum 87:093704.  https://doi.org/10.1063/1.4961365 CrossRefPubMedGoogle Scholar
  50. Knipfer T, Cuneo IF, Brodersen CR, McElrone AJ (2016) In situ visualization of the dynamics in xylem embolism formation and removal in the absence of root pressure: a study on excised grapevine stems. Plant Physiol 171:1024–1036.  https://doi.org/10.1104/pp.16.00136 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Knipfer T, Cuneo IF, Earles JM, Reyes C, Brodersen CR, McElrone AJ (2017) Storage compartments for capillary water rarely refill in an intact woody plant. Plant Physiol 175:1649–1660.  https://doi.org/10.1104/pp.17.01133 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lamarque LJ (2018) Data from: an inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L., Dryad Digital Repository. [Dataset].  https://doi.org/10.5061/dryad.r9q30g0
  53. Lamy JB, Bouffier L, Burlett R, Plomion C, Cochard H, Delzon S (2011) Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS One 6:e23476.  https://doi.org/10.1371/journal.pone.0023476 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lamy JB, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C (2014) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol 201:874–886.  https://doi.org/10.1111/nph.12556 CrossRefPubMedGoogle Scholar
  55. Larter M, Brodribb TJ, Pfautsch S, Burlett R, Cochard H, Delzon S (2015) Extreme aridity pushes trees to their physical limits. Plant Physiol 168:804–807.  https://doi.org/10.1104/pp.15.00223 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Larter M, Pfautsch S, Domec JC, Trueba S, Nagalingum N, Delzon S (2017) Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris. New Phytol 215:97–112.  https://doi.org/10.1111/nph.14545 CrossRefPubMedGoogle Scholar
  57. Li S, Klepsch M, Jansen S, Schmitt M, Lens F, Karimi Z, Schuldt B, Espino S, Schenk HJ (2016) Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J 37:152–171.  https://doi.org/10.1163/22941932-20160128 CrossRefGoogle Scholar
  58. Lindenmayer DB, Laurance WF, Franklin JF (2012) Global decline in large old trees. Science 338:1305–1306.  https://doi.org/10.1126/science.1231070 CrossRefPubMedGoogle Scholar
  59. Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199.  https://doi.org/10.1890/02-0538 CrossRefGoogle Scholar
  60. Martin-StPaul N, Longepierre D, Huc R, Delzon S, Burlett R, Joffre R, Rambal S, Cochard H (2014) How reliable are methods to assess xylem vulnerability to cavitation? The issue of ‘open vessel’ artifact in oaks. Tree Physiol 34:894–905.  https://doi.org/10.1093/treephys/tpu059 CrossRefPubMedGoogle Scholar
  61. Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecol Lett 20:1437–1447.  https://doi.org/10.1111/ele.12851 CrossRefPubMedGoogle Scholar
  62. Masschaele B, Dierick M, Van Loo D, Boone MN, Brabant L, Pauwels E, Cnudde V, Van Hoorebeke L (2013) HECTOR: a 240 kV microCT setup optimized for research. J Phys Conf Ser 463:012012.  https://doi.org/10.1088/1742-6596/463/1/012012 CrossRefGoogle Scholar
  63. McElrone AJ, Choat B, Parkinson D, MacDowell A, Brodersen CR (2013) Utilization of high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature. J Vis Exp 74:50162.  https://doi.org/10.3791/50162
  64. Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997.  https://doi.org/10.1126/science.1098704 CrossRefPubMedGoogle Scholar
  65. Michaelian M, Hogg EH, Hall RJ, Arsenault E (2011) Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob Chang Biol 17:2084–2094.  https://doi.org/10.1111/j.1365-2486.2010.02357.x CrossRefPubMedCentralGoogle Scholar
  66. Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J (2014) The PyHST2 hybrid distributed code for high speed tomographic reconstruction with interaction reconstruction and a priori knowledge capabilities. Nucl Instrum Methods Phys Res B 324:41–48.  https://doi.org/10.1016/j.nimb.2013.09.030 CrossRefGoogle Scholar
  67. Nardini A, Ramani M, Gortan E, Salleo S (2008) Vein recovery from embolism occurs under negative pressure in leaves of sunflower (Helianthus annuus). Physiol Plant 133:755–764.  https://doi.org/10.1111/j.1399-3054.2008.01087.x CrossRefPubMedGoogle Scholar
  68. Nardini A, Savi T, Losso A, Petit G, Pacile S, Tromba G, Mayr S, Trifilò P, Lo Gullo MA, Salleo S (2017) X-ray microtomography observations of xylem embolism in stems of Laurus nobilis are consistent with hydraulic measurements of percentage loss of conductance. New Phytol 213:1068–1075.  https://doi.org/10.1111/nph.14245 CrossRefPubMedGoogle Scholar
  69. Nolf M, Lopez R, Peters JM, Flavel RJ, Koloadin LS, Young IM, Choat B (2017) Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements. New Phytol 214:890–898.  https://doi.org/10.1111/nph.14462 CrossRefPubMedGoogle Scholar
  70. Paganin D, Mayon SC, Gureyev TE, Miller PR, Wilkins SW (2002) Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206:33–40.  https://doi.org/10.1046/j.1365-2818.2002.01010.x CrossRefPubMedGoogle Scholar
  71. Pammenter NW, Van der Willigen C (1998) A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol 18:589–593.  https://doi.org/10.1093/treephys/18.8-9.589 CrossRefPubMedGoogle Scholar
  72. Rhizopoulou S, Mitrakos K (1990) Water relations of evergreen sclerophylls. I. Seasonal changes in the water relations of eleven species from the same environment. Ann Bot 65:171–178.  https://doi.org/10.1093/oxfordjournals.aob.a087921 CrossRefGoogle Scholar
  73. Rockwell FE, Wheeler JK, Holbrook NM (2014) Cavitation and its discontents: opportunities for resolving current controversies. Plant Physiol 164:1649–1660.  https://doi.org/10.1104/pp.113.233817 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rodríguez-Sánchez F, Guzmán B, Valido A, Vargas P, Arroyo J (2009) Late Neogene history of the laurel tree (Laurus L., Lauraceae) based on phylogeographical analyses of Mediterranean and Macaronesian populations. J Biogeogr 36:1270–1281.  https://doi.org/10.1111/j.1365-2699.2009.02091.x CrossRefGoogle Scholar
  75. Salleo S, Lo Gullo MA (1993) Drought resistance strategies and vulnerability to cavitation of some Mediterranean sclerophyllous trees. In: Borghetti M, Grace J, Raschi A (eds) Water transport in plants under climate stress. Cambridge University Press, Cambridge, pp 99–113CrossRefGoogle Scholar
  76. Salleo S, Lo Gullo MA, de Paoli D, Zippo M (1996) Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. New Phytol 132:47–56.  https://doi.org/10.1111/j.1469-8137.1996.tb04507.x CrossRefGoogle Scholar
  77. Salleo S, Nardini A, Pitt F, Lo Gullo MA (2000) Xylem cavitation and hydraulic control of stomatal conductance in Laurel (Laurus nobilis L.). Plant Cell Environ 23:71–79.  https://doi.org/10.1046/j.1365-3040.2000.00516.x CrossRefGoogle Scholar
  78. Salleo S, Lo Gullo MA, Raimondo F, Nardini A (2001) Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange? Plant Cell Environ 24:851–859.  https://doi.org/10.1046/j.0016-8025.2001.00734.x CrossRefGoogle Scholar
  79. Salleo S, Lo Gullo MA, Trifilò P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant Cell Environ 27:1065–1076.  https://doi.org/10.1111/j.1365-3040.2004.01211.x CrossRefGoogle Scholar
  80. Salleo S, Trifilò P, Esposito S, Nardini A, Lo Gullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Funct Plant Biol 36:815–825.  https://doi.org/10.1071/FP09103 CrossRefGoogle Scholar
  81. Sanchez-Salguero R, Navarro-Cerrillo RM, Camarero JJ, Fernández-Cancio Á (2012) Selective drought-induced decline of pine species in southeastern Spain. Clim Chang 113:767–785.  https://doi.org/10.1007/s10584-011-0372-6 CrossRefGoogle Scholar
  82. Schuldt B, Knutzen F, Delzon S, Jansen S, Muller-Haubold H, Burlett R, Clough Y, Leuschner C (2016) How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol 210:443–458.  https://doi.org/10.1111/nph.13798 CrossRefPubMedGoogle Scholar
  83. Scoffoni C, Albuquerque C, Brodersen CR, Townes SV, John GP, Cochard H, Buckley TN, McElrone AJ, Sack L (2017) Leaf vein xylem conduit diameter influences susceptibility to embolism and hydraulic decline. New Phytol 213:1076–1092.  https://doi.org/10.1111/nph.14256 CrossRefPubMedGoogle Scholar
  84. Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol 214:561–569.  https://doi.org/10.1111/nph.14450 CrossRefPubMedGoogle Scholar
  85. Sperry JS, Pockman WP (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant Cell Environ 16:279–288.  https://doi.org/10.1111/j.1365-3040.1993.tb00870.x CrossRefGoogle Scholar
  86. Sperry JS, Ikeda T (1997) Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiol. 17:275–280.  https://doi.org/10.1093/treephys/17.4.275 CrossRefGoogle Scholar
  87. Sperry JS, Christman MA, Torres-Ruiz JM, Taneda H, Smith DD (2012) Vulnerability curves by centrifugation: is there an open vessel artefact, and are “r” shaped curves necessarily invalid? Plant Cell Environ 35:601–610.  https://doi.org/10.1111/j.1365-3040.2011.02439.x CrossRefPubMedGoogle Scholar
  88. Stojnic S, Suchocka M, Benito-Garzon M, Torres-Ruiz JM, Cochard H, Bolte A, Cocozza C, Cvjetkovic B, de Luis M, Martinez-Vilalta J, Raebild A, Tognetti R, Delzon S (2018) Variation in xylem vulnerability to embolism in European beech from geographically marginal populations. Tree Physiol 38:173–185.  https://doi.org/10.1093/treephys/tpx128 CrossRefPubMedGoogle Scholar
  89. Svenning JC (2003) Deterministic Plio-Pleistocene extinctions in the European cool-temperate tree flora. Ecol Lett 6:646–653.  https://doi.org/10.1046/j.1461-0248.2003.00477.x CrossRefGoogle Scholar
  90. Tobin MF, Pratt RB, Jacobsen AL, De Guzman M (2013) Xylem vulnerability to cavitation can be accurately characterized in species with long vessels using a centrifuge method. Plant Biol 15:496–504.  https://doi.org/10.1111/j.1438-8677.2012.00678.x CrossRefPubMedGoogle Scholar
  91. Torres-Ruiz JM, Cochard H, Mayr S, Beikircher B, Diaz-Espejo A, Rodriguez-Dominguez CM, Badel E, Fernandez JE (2014) Vulnerability to cavitation in Olea europaea current-year shoots: further evidence of an open-vessel artifact associated with centrifuge and air-injection techniques. Physiol Plant 152:465–474.  https://doi.org/10.1111/ppl.12185 CrossRefPubMedGoogle Scholar
  92. Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR, Li S, Morris H, Delzon S (2015) Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiol 167:40–43.  https://doi.org/10.1104/pp.114.249706 CrossRefPubMedGoogle Scholar
  93. Torres-Ruiz JM, Cochard H, Mencuccini M, Delzon S, Badel E (2016) Direct observation and modelling of embolism spread between xylem conduits: a case study in Scots pine. Plant Cell Environ 39:2774–2785.  https://doi.org/10.1111/pce.12840 CrossRefPubMedGoogle Scholar
  94. Torres-Ruiz JM, Cochard H, Choat B, Jansen S, Lopez R, Tomaskova I, Padilla-Diaz CM, Badel E, Burlett R, King A, Lenoir N, Martin-StPaul NK, Delzon S (2017) Xylem resistance to embolism: presenting a simple diagnostic test for the open vessel artefact. New Phytol 215:489–499.  https://doi.org/10.1111/nph.14589 CrossRefPubMedGoogle Scholar
  95. Trifilò P, Barbera PM, Raimondo F, Nardini A, Lo Gullo MA (2014a) Coping with drought-induced xylem cavitation: coordination of embolism repair and ionic effects in three Mediterranean evergreens. Tree Physiol 34:109–122.  https://doi.org/10.1093/treephys/tpt119 CrossRefPubMedGoogle Scholar
  96. Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A (2014b) Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant Cell Environ 37:2491–2499.  https://doi.org/10.1111/pce.12313 CrossRefPubMedGoogle Scholar
  97. Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling in embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiol 120:11–21.  https://doi.org/10.1104/pp.120.1.11 CrossRefPubMedCentralGoogle Scholar
  98. Urli M, Porte AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683.  https://doi.org/10.1093/treephys/tpt030 CrossRefPubMedGoogle Scholar
  99. Urli M, Lamy J-B, Sin F, Burlett R, Delzon S, Porté AJ (2014) The high vulnerability of Quercus robur to drought at its southern margin paves the way for Quercus ilex. Plant Ecol 216:177–187.  https://doi.org/10.1007/s11258-014-0426-8 CrossRefGoogle Scholar
  100. Vallabh R, Ducoste J, Seyam A-F, Banks-Lee P (2011) Modeling tortuosity in thin fibrous porous media using computational fluid dynamics. J Porous Media 14:791–804.  https://doi.org/10.1615/JPorMedia.v14.i9.40 CrossRefGoogle Scholar
  101. Venturas MD, MacKinnon ED, Jacobsen AL, Pratt RB (2015) Excising stem samples underwater at native tension does not induce xylem cavitation. Plant Cell Environ 38:1060–1068.  https://doi.org/10.1111/pce.12461 CrossRefGoogle Scholar
  102. Vlassenbroeck J, Dierick M, Masschaele B, Cnudde V, Van Hoorebeke L, Jacobs P (2007) Software tools for quantification of X-ray microtomography at the UGCT. Nucl Instrum Methods Phys Res A 580:442–445.  https://doi.org/10.1016/j.nima.2007.05.073 CrossRefGoogle Scholar
  103. Wang R, Zhang L, Zhang S, Cai J, Tyree MT (2014) Water relations of Robinia pseudoacacia L.: do vessels cavitate and refill diurnally or are R-shaped curves invalid in Robinia? Plant Cell Environ 37:2667–2678.  https://doi.org/10.1111/pce.12315 CrossRefPubMedGoogle Scholar
  104. Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ 36:1938–1949.  https://doi.org/10.1111/pce.12139 CrossRefPubMedGoogle Scholar
  105. Zhang Y, Klepsch M, Jansen S (2017) Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates. Plant Cell Environ 40:2133–2146.  https://doi.org/10.1111/pce.13014 CrossRefPubMedGoogle Scholar
  106. Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Laurent J. Lamarque
    • 1
    • 2
  • Déborah Corso
    • 2
  • José M. Torres-Ruiz
    • 2
  • Eric Badel
    • 3
  • Timothy J. Brodribb
    • 4
  • Régis Burlett
    • 2
  • Guillaume Charrier
    • 2
    • 5
  • Brendan Choat
    • 6
  • Hervé Cochard
    • 3
  • Gregory A. Gambetta
    • 5
  • Steven Jansen
    • 7
  • Andrew King
    • 8
  • Nicolas Lenoir
    • 9
  • Nicolas Martin-StPaul
    • 10
  • Kathy Steppe
    • 11
  • Jan Van den Bulcke
    • 12
  • Ya Zhang
    • 7
  • Sylvain Delzon
    • 2
  1. 1.EGFV, INRA, Univ. BordeauxVillenave d’OrnonFrance
  2. 2.BIOGECO, INRA, Univ. BordeauxPessacFrance
  3. 3.Université Clermont-Auvergne, INRA, PIAFClermont-FerrandFrance
  4. 4.School of Biological SciencesUniversity of TasmaniaHobartAustralia
  5. 5.EGFV, INRA, BSA, ISVVVillenave d’OrnonFrance
  6. 6.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityRichmondAustralia
  7. 7.Institute of Systematic Botany and EcologyUlm UniversityUlmGermany
  8. 8.Synchrotron SOLEIL, L’Orme de MerisiersGif-sur-Yvette CedexFrance
  9. 9.CNRS, University of BordeauxPessacFrance
  10. 10.URFM, INRAAvignonFrance
  11. 11.Laboratory of Plant Ecology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  12. 12.Laboratory of Wood Technology, Department of Forest and Water ManagementUGCT-Woodlab-UGent, Ghent UniversityGhentBelgium

Personalised recommendations