The recurrent evolution of extremely resistant xylem

  • Scott A. M. McAdamEmail author
  • Amanda A. Cardoso


Key message

Highly resistant xylem has evolved multiple times over the past 400 million years.


Water is transported under tension in xylem and consequently is vulnerable to invasion by air and the formation of embolism. A debate has raged over whether embolism formation is non-reversible occurring at low water potentials or a regular diurnal occurrence that is non-lethal because of a capacity to refill embolised conduits.


This commentary is on a recent article, which utilised new non-invasive imaging techniques for assessing the formation of embolism in xylem, finding that the xylem of Laurus nobilis was highly resistant to the formation of embolism.


The recent results of this discovery are placed in the context knowledge from a diversity of species that has so far been identified with xylem similarly highly resistant to embolism formation.


The discovery that L. nobilis has xylem highly resistant to embolism formation adds to a body of literature suggesting that the resistance of xylem to embolism formation is a key adaptation utilised by many species native to seasonally dry environments. Highly resistant xylem has evolved numerous times across the angiosperm clade.


With more studies utilising similar observational and direct methods of assessing embolism resistance, further insight into the ecological and evolutionary relevance of this trait is imminent.


Xylem Vulnerability Evolution Embolism Drought 



This work was supported by the USDA National Institute of Food and Agriculture, Hatch project 1014908.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13595_2018_786_MOESM1_ESM.xlsx (22 kb)
ESM 1 (XLSX 22.4 kb)


  1. Axelrod DI (1966) Origin of deciduous and evergreen habits in temperate forests. Evolution 20:1–15CrossRefGoogle Scholar
  2. Bhaskar R, Valiente-Banuet A, Ackerly DD (2007) Evolution of hydraulic traits in closely related species pairs from mediterranean and nonmediterranean environments of North America. New Phytol 176:718–726CrossRefGoogle Scholar
  3. Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123CrossRefGoogle Scholar
  4. Brodersen CR, Lee EF, Choat B, Jansen S, Phillips RJ, Shackel KA, McElrone AJ, Matthews MA (2011) Automated analysis of three-dimensional xylem networks using high-resolution computed tomography. New Phytol 191:1168–1179CrossRefGoogle Scholar
  5. Brodribb TJ, McAdam SAM, Jordan GJ, Martins SC (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc Natl Acad Sci U S A 111:14489–14493CrossRefGoogle Scholar
  6. Brodribb TJ, Bienaimé D, Marmottant P (2016) Revealing catastrophic failure of leaf networks under stress. Proc Natl Acad Sci U S A 113:4865–4869CrossRefGoogle Scholar
  7. Brodribb TJ, Carriqui M, Delzon S, Lucani C (2017) Optical measurement of stem xylem vulnerability. Plant Physiol 174:2054–2061CrossRefGoogle Scholar
  8. Cardoso AA, Brodribb TJ, Lucani CJ, DaMatta FM, McAdam SAM (2018) Coordinated plasticity maintains hydraulic safety in sunflower leaves. Plant Cell Environ 41:2567–2576CrossRefGoogle Scholar
  9. Chanderbali AS, Werff H, Renner SS (2001) Phylogeny and historical biogeography of Lauraceae: evidence from the chloroplast and nuclear genomes. Ann Mo Bot Gard 88:104–134CrossRefGoogle Scholar
  10. Choat B, Brodie TW, Cobb AR, Zwieniecki MA, Holbrook NM (2006) Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. Am J Bot 93:993–1000CrossRefGoogle Scholar
  11. 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 long-vesseled species. Plant Cell Environ 33:1502–1512PubMedGoogle Scholar
  12. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Field TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-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 491:752–755CrossRefGoogle Scholar
  13. 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 170:273–282CrossRefGoogle Scholar
  14. Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558:531–539CrossRefGoogle Scholar
  15. 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 33:1543–1552PubMedGoogle Scholar
  16. 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 38:201–206CrossRefGoogle Scholar
  17. Cook CD (1999) The number and kinds of embryo-bearing plants which have become aquatic: a survey. Perspect Plant Ecol Syst 2:79–102CrossRefGoogle Scholar
  18. Dietrich L, Delzon S, Hoch G, Kahmen A (2018) No role for xylem embolism or carbohydrate shortage in temperate trees during the severe 2015 drought. J Ecol:1–16Google Scholar
  19. Donoghue MJ (2008) A phylogenetic perspective on the distribution of plant diversity. Proc Natl Acad Sci U S A 105:11549–11555CrossRefGoogle Scholar
  20. Feild TS, Holbrook NM (2000) Xylem sap flow and stem hydraulics of the vesselless angiosperm Drimys granadensis (Winteraceae) in a Costa Rican elfin forest. Plant Cell Environ 23:1067–1077CrossRefGoogle Scholar
  21. Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311CrossRefGoogle Scholar
  22. Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:619–701CrossRefGoogle Scholar
  23. Hacke UG, Sperry JS, Feild TS, Sano Y, Sikkema EH, Pittermann J (2007) Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. Int J Plant Sci 168:1113–1126CrossRefGoogle Scholar
  24. 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 205:116–127CrossRefGoogle Scholar
  25. Jacobsen AL, Pratt RB (2012) No evidence for an open vessel effect in centrifuge-based vulnerability curves of a long-vesselled liana (Vitis vinifera). New Phytol 194:982–990CrossRefGoogle Scholar
  26. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419CrossRefGoogle Scholar
  27. Klepsch M, Zhang Y, Kotowska MM, Lamarque LJ, Nolf M, Schuldt B, Torres-Ruiz JM, Qin DW, Choat B, Delzon S, Scoffoni C, Cao KF, Jansen S (2018) Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy. J Exp Bot:1–13Google Scholar
  28. Lamarque LJ, Corso D, Torres-Ruiz JM, Badel E, Brodribb TJ, Burlett R, Charrier G, Choat B, Cochard H, Gambetta GA, Jansen S, King A, Lenoir N, Martin-StPaul N, Steppe K, Bulcke JV, Zhang Y, Delzon S (2018) An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L. Ann For Sci 75:88CrossRefGoogle Scholar
  29. Larter M, Brodribb TJ, Pfautsch S, Burlett R, Cochard H, Delzon S (2015) Extreme aridity pushes trees to their physical limits. Plant Physiol 168:804–807CrossRefGoogle Scholar
  30. 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 215:97–112CrossRefGoogle Scholar
  31. Lobo A, Torres-Ruiz JM, Burlett R, Lemaire C, Parise C, Francioni C, Truffaut L, Tomášková I, Hansen JK, Kjær ED, Kremer A, Delzon S (2018) Assessing inter-and intraspecific variability of xylem vulnerability to embolism in oaks. For Ecol Manag 424:53–61CrossRefGoogle Scholar
  32. Martin-StPaul NK, 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 34:894–905CrossRefGoogle Scholar
  33. Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol 153:1919–1931CrossRefGoogle Scholar
  34. Pittermann J, Stuart SA, Dawson TE, Moreau A (2012) Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers. Proc Natl Acad Sci U S A 109:9647–9652CrossRefGoogle Scholar
  35. Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386CrossRefGoogle Scholar
  36. Rodriguez-Dominguez CM, Carins Murphy MR, Lucani C, Brodribb TJ (2018) Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytol 218:1025–1035CrossRefGoogle Scholar
  37. 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 36:1270–1281CrossRefGoogle Scholar
  38. Salleo S, Lo Gullo MA, Trifilo 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 27:1065–1076CrossRefGoogle Scholar
  39. Salleo S, Trifilò P, Esposito S, Nardini A, Gullo MAL (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 36:815–825CrossRefGoogle Scholar
  40. Schenk HJ, Steppe K, Jansen S (2015) Nanobubbles: a new paradigm for air-seeding in xylem. Trends Plant Sci 20:199–205CrossRefGoogle Scholar
  41. Scoffoni C, Albuquerque C, Brodersen C, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiol 173:1197–1210CrossRefGoogle Scholar
  42. Skelton RP, Brodribb TJ, McAdam SAM, Mitchell PJ (2017) Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland. New Phytol 215:1399–1412CrossRefGoogle Scholar
  43. Skelton RP, Dawson TE, Thompson SE, Shen Y, Weitz AP, Ackerly D (2018) Low vulnerability to xylem embolism in leaves and stems of North American oaks. Plant Physiol 177:1066–1077CrossRefGoogle Scholar
  44. Torres-Ruiz JM, Cochard H, Choat B, Jansen S, López R, Tomášková I, Padilla-Díaz 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 215:489–499CrossRefGoogle Scholar
  45. Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A (2014) Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant Cell Environ 37:2491–2499CrossRefGoogle Scholar
  46. Vaz M, Cochard H, Gazarini L, Graça J, Chaves MM, Pereira JS (2012) Cork oak (Quercus suber L.) seedlings acclimate to elevated CO2 and water stress: photosynthesis, growth, wood anatomy and hydraulic conductivity. Trees 26:1145–1157CrossRefGoogle Scholar
  47. Vilagrosa A, Bellot J, Vallejo VR, Gil-Pelegrín E (2003) Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. J Exp Bot 54:2015–2024CrossRefGoogle Scholar
  48. Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812CrossRefGoogle Scholar
  49. Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Botany and Plant Pathology, Purdue Center for Plant BiologyPurdue UniversityWest LafayetteUSA

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