An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L.
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.
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.).
The purpose of this study was to resolve the hydraulic properties of this species by documenting vulnerability curves of different organs in intact plants.
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.
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).
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.
KeywordsXylem embolism Drought resistance Laurel Refilling Hydraulics Desiccation
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.
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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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