Advertisement

Plant Cuticular Waxes: Composition, Function, and Interactions with Microorganisms

  • Viktoria Valeska Zeisler-Diehl
  • Wilhelm Barthlott
  • Lukas Schreiber
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

The interface between leaves and the surrounding environment is formed by the wax-covered plant cuticle, which is hydrophobic and highly impermeable to water and dissolved solutes. The surface itself may become superhydrophobic by complex three-dimensional wax crystals. There is evidence that this system evolved already early with the colonization of land some 450 million years ago. Although the leaf surface represents a hostile environment, because water and nutrient availability is very limited and variations in temperature and light intensity can be quite large, it forms the habitat for specialized epiphyllic microorganisms successfully colonizing the leaf surface which is also called phyllosphere. Certain strategies improving living conditions within the phyllosphere have been developed by epiphyllic microorganisms. They can significantly enhance leaf surface wetting and water permeability of the hydrophobic cuticle. This interaction significantly increases the abundance of water on the leaf surface, and as a consequence, leaching of nutrients to the leaf surface should be increased, thus becoming available for epiphyllic microorganisms. This strategy is supported by the ability of biosurfactant production, which represents a common and important adaptation of epiphyllic microorganisms.

Notes

Acknowledgments

Long-lasting financial support by the DFG (Deutsche Forschungsgemeinschaft) to LS is gratefully acknowledged.

References

  1. Bailey MJ, Lilley AK, Timms-Wilson TM, Spencer-Phillips PTN (2006) Microbial ecology of aerial plant surfaces. CABI, WallingfordCrossRefGoogle Scholar
  2. Barthlott W, Mail M, Bhushan B, Koch K (2017) Plant surfaces: structures and functions for biomimetic innovations. Nano-Micro Letters 9:23CrossRefGoogle Scholar
  3. Barthlott W, Mail M, Neinhuis C (2016) Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications. Philos Trans R Soc Lond A 374:20160–20191CrossRefGoogle Scholar
  4. Barthlott W, Neinhuis C (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202:1–8CrossRefGoogle Scholar
  5. Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Bot J Linn Soc 126:237–260CrossRefGoogle Scholar
  6. Bhardwaj G, Cameotra SS, Chopra HK (2013) Biosurfactants from fungi: a review. J Pet Environ Biotechnol 4:1–6CrossRefGoogle Scholar
  7. Bunster L, Fokkema NJ, Schippers B (1989) Effect of surface-active Pseudomonas spp. on leaf wettability. Appl Environ Microbiol 55:1340–1345PubMedPubMedCentralGoogle Scholar
  8. Burch AY, Do PT, Sbodio A, Suslow TV, Lindow SE (2016) High-level culturability of epiphytic bacteria and frequency of biosurfactant producers on leaves. Appl Environ Microbiol 82:5997–6009CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burch AY, Zeisler V, Yokota K, Schreiber L, Lindow SE (2014) The hygroscopic biosurfactant syringafactin produced by Pseudomonas syringae enhances fitness on leaf surfaces during fluctuating humidity. Environ Microbiol 16:2086–2098CrossRefPubMedGoogle Scholar
  10. Burghardt M, Schreiber L, Riederer M (1998) Enhancement of the diffusion of active ingredients in barley leaf cuticular wax by monodisperse alcohol ethoxylates. J Agric Food Chem 46:1593–1602CrossRefGoogle Scholar
  11. Buschhaus C, Jetter R (2011) Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces? J Exp Bot 62:841–853CrossRefPubMedGoogle Scholar
  12. Cussler EL (1984) Diffusion. Mass transfer in fluid systems. Cambridge University Press, CambridgeGoogle Scholar
  13. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106:16428–16433CrossRefPubMedPubMedCentralGoogle Scholar
  14. Groombridge B, Jenkins M (2002) World atlas of biodiversity: Earth’s living resources in the 21st century. University of California Press, BerkeleyGoogle Scholar
  15. Guzman P, Fernandez V, Graca J, Cabral V, Kayali N, Khayet M, Gil L (2014) Chemical and structural analysis of Eucalyptus globulus and E. camaldulensis leaf cuticles: a lipidized cell wall region. Front Plant Sci.  https://doi.org/10.3389/fpls.2014.00481
  16. Hansjakob A, Bischof S, Bringmann G, Riederer M, Hildebrandt U (2010) Very-long-chain aldehydes promote in vitro prepenetration processes of Blumeria graminis in a dose- and chain length-dependent manner. New Phytol 188:1039–1054CrossRefPubMedGoogle Scholar
  17. Holmes-Farley SR, Bain CD, Whitesides GM (1988) Wetting of functionalized polyethylene film having ionizable organic acids and bases at the polymer-water interface: relations between functional group polarity, extent of ionisation, and contact angle with water. Langmuir 4:921–937CrossRefGoogle Scholar
  18. Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl Environ Microbiol 76:8117–8125CrossRefPubMedPubMedCentralGoogle Scholar
  19. Jetter R, Kunst L, Samuels AL (2006) Composition of plant cuticular waxes. In: Riederer M, Müller C (eds) Biology of the plant cuticle. Blackwell, Oxford, pp 145–181CrossRefGoogle Scholar
  20. Jetter R, Riederer M (2016) Localization of the transpiration barrier in the epi- and intracuticular waxes of eight plant species: water transport resistances are associated with fatty acyl rather than alicyclic components. Plant Physiol 170:921–934CrossRefPubMedGoogle Scholar
  21. Jetter R, Schäffer S, Riederer M (2000) Leaf cuticular waxes are arranged in chemically and mechanically distinct layers: evidence from Prunus laurocerasus L. Plant Cell Environ 23:619–628CrossRefGoogle Scholar
  22. Joubes J, Domergue F (2018) Biosynthesis of the plant cuticle. In: Wilkes H (ed) Hydrocarbons, oils and lipids: diversity, origin, chemistry and fate, Handbook of hydrocarbon and lipid microbiology. Springer, Berlin.  https://doi.org/10.1007/978-3-319-54529-5_8-1CrossRefGoogle Scholar
  23. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  24. Kinkel LL (1997) Microbial population dynamics on leaves. Annu Rev Phytopathol 35:327–347CrossRefPubMedGoogle Scholar
  25. Kirkwood RC (1999) Recent developments in our understanding of the plant cuticle as a barrier to the foliar uptake of pesticides. Pestic Sci 55:69–77CrossRefGoogle Scholar
  26. Kirsch T, Kaffarnik F, Riederer M, Schreiber L (1997) Cuticular permeability of the three tree species Prunus laurocerasus L., Ginkgo biloba L. and Juglans regia L. - comparative investigation of the transport properties of intact leaves, isolated cuticles and reconstituted cuticular waxes. J Exp Bot 48:1035–1045CrossRefGoogle Scholar
  27. Knoll D, Schreiber L (1998) Influence of epiphytic micro-organisms on leaf wettability: wetting of the upper leaf surface of Juglans regia L. and of model surfaces in relation to colonisation by micro-organisms. New Phytol 140:271–282CrossRefGoogle Scholar
  28. Knoll D, Schreiber L (2004) Methods for analysing the interactions between epiphyllic microorgansisms and leaf cuticles. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Heidelberg, pp 471–487Google Scholar
  29. Koch K, Bhushan B, Barthlott W (2008) Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4:1943–1963CrossRefGoogle Scholar
  30. Kolattukudy PE, Walton TJ (1973) The biochemistry of plant cuticular lipids. Prog Chem Fats Other Lipids 13:119–175CrossRefGoogle Scholar
  31. Krimm U, Abanda-Nkpwatt D, Schwab W, Schreiber L (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol Ecol 53:483–492CrossRefPubMedGoogle Scholar
  32. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42:51–80CrossRefPubMedGoogle Scholar
  33. Leveau JHJ, Lindow SE (2001) Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc Natl Acad Sci U S A 98:3446–3453CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lindberg SE, Lovett GM, Richter DD, Johnson DW (1986) Atmospheric deposition and canopy interactions of major ions in a forest. Science 231:141–146CrossRefPubMedGoogle Scholar
  35. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lohaus G, Pennewiss K, Sattelmacher B, Hussmann M, Mühling KH (2001) Is the infiltration-centrifugation technique appropriate for the isolation of apoplastic fluid? A critical evaluation with different plant species. Physiol Plant 111:457–465CrossRefPubMedGoogle Scholar
  37. Meyer KM, Leveau JHJ (2012) Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168:621–629CrossRefPubMedGoogle Scholar
  38. Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:429–453CrossRefPubMedGoogle Scholar
  39. Niklas KJ, Cobb ED, Matas AJ (2017) The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms. J Eperiment Botany.  https://doi.org/10.1093/jxb/erx215
  40. Parra JL, Guinea J, Manresa MA, Robert M, Mercadé ME, Comelles F, Bosch MP (1989) Chemical characterization and physicochemical behavior of biosurfactants. J Am Oil Chem Soc 66:141–145CrossRefGoogle Scholar
  41. Pollard M, Beisson F, Li YH, Ohlrogge JB (2009) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246CrossRefGoogle Scholar
  42. Reynhardt EC, Riederer M (1994) Structures and molecular dynamics of plant waxes. II Cuticular waxes from leaves of Fagus sylvatica L. and Hordeum vulgare L. Eur Biophys J 23:59–70CrossRefGoogle Scholar
  43. Riederer M, Müller C (2006) Biology of the plant cuticle. Blackwell Publishing, OxfordCrossRefGoogle Scholar
  44. Riederer M, Schneider G (1989) Comparative study of the composition of waxes extracted from isolated leaf cuticles and from whole leaves of Citrus: evidence for selective extraction. Physiol Plant 77:373–384CrossRefGoogle Scholar
  45. Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252CrossRefPubMedGoogle Scholar
  46. Ruan YL, Patrick JW, Brady CJ (1996) The composition of apoplast fluid recovered from intact developing tomato fruit. Aust J Plant Physiol 23:9–13CrossRefGoogle Scholar
  47. Ruinen J (1961) The phyllosphere: 1. An ecologically neglected milieu. Plant Soil 15:81–109CrossRefGoogle Scholar
  48. Samuels L, Kunst L, Jetter R (2009) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707CrossRefGoogle Scholar
  49. Schlegel TK, Schönherr J, Schreiber L (2005) Size selectivity of aqueous pores in stomatous cuticles of Vicia faba leaves. Planta 221:648–655CrossRefPubMedGoogle Scholar
  50. Schönherr J (1976) Water permeability of isolated cuticular membranes: the effect of cuticular waxes on diffusion of water. Planta 131:159–164CrossRefPubMedGoogle Scholar
  51. Schönherr J (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J Exp Bot 57:2471–2491CrossRefPubMedGoogle Scholar
  52. Schönherr J, Baur P (1996) Cuticle permeability studies - a model for estimating leaching of plant metabolits to leaf surfaces. In: Morris CE, Nicot PC, Nguyen-The C (eds) Aerial plant surface microbiology. Plenum Press, New York, pp 1–23Google Scholar
  53. Schönherr J, Lendzian K (1981) A simple and inexpensive method of measuring water permeability of isolated plant cuticular membranes. Z Pflanzenphysiol 102:321–327CrossRefGoogle Scholar
  54. Schönherr J, Riederer M (1989) Foliar penetration and accumulation of organic chemicals in plant cuticles. Rev Environ Contam Toxicol 108:1–70CrossRefGoogle Scholar
  55. Schreiber L (1996) Wetting of the upper needle surface of Abies grandis: influence of pH, wax chemistry and epiphyllic microflora on contact angles. Plant Cell Environ 19:455–463CrossRefGoogle Scholar
  56. Schreiber L (2005) Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Ann Bot 95:1069–1073CrossRefPubMedPubMedCentralGoogle Scholar
  57. Schreiber L (2006) Review of sorption and diffusion of lipophilic molecules in cuticular waxes and the effects of accelerators on solute mobilities. J Exp Bot 57:2515–2523CrossRefPubMedGoogle Scholar
  58. Schreiber L, Krimm U, Knoll D, Sayed M, Auling G, Kroppenstedt RM (2005) Plant-microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability. New Phytol 166:589–594CrossRefPubMedGoogle Scholar
  59. Schreiber L, Riederer M (1996) Ecophysiology of cuticular transpiration: comparative investigation of cuticular water permeability of plant species from different habitats. Oecologia 107:426–432CrossRefPubMedGoogle Scholar
  60. Schreiber L, Schönherr J (1993) Mobilities of organic compounds in reconstituted cuticular wax of barley leaves: determination of diffusion coefficients. Pestic Sci 38:353–361CrossRefGoogle Scholar
  61. Schreiber L, Schönherr J (2009) Water and solute permeability of plant cuticles. Springer, HeidelbergGoogle Scholar
  62. Segado P, Dominguez E, Heredia A (2016) Ultrastructure of the epidermal cell wall and cuticle of tomato fruit (Solanum lycopersicum L.) during development. Plant Physiol 170:935–946CrossRefPubMedGoogle Scholar
  63. Shi T, Simanova E, Schönherr J, Schreiber L (2005) Effects of accelerators on mobility of 14C-2,4-dichlorophenoxy butyric acid in plant cuticles depends on type and concentration of accelerator. J Agric Food Chem 53:2207–2212CrossRefPubMedGoogle Scholar
  64. Ueda H, Mitsuhara I, Tabata J, Kugimiya S, Watanabe T, Suzuki K, Yoshida S, Kitamoto H (2015) Extracellular esterases of phylloplane yeast Pseudozyma antarctica induce defect on cuticle layer structure and water-holding ability of plant leaves. Appl Microbiol Biotechnol 99:6405–6415CrossRefPubMedGoogle Scholar
  65. Villena JF, Dominguez E, Stewart D, Heredia A (1999) Characterization and biosynthesis of non-degradable polymers in plant cuticles. Planta 208:181–187CrossRefPubMedGoogle Scholar
  66. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840CrossRefGoogle Scholar
  67. Wang ZH, Guhling O, Yao RN, Li FL, Yeats TH, Rose JKC, Jetter R (2011) Two oxidosqualene cyclases responsible for biosynthesis of tomato fruit cuticular triterpenoids. Plant Physiol 155:540–552CrossRefPubMedGoogle Scholar
  68. Wang Y, Wang JH, Chai GQ, Li CL, Hu YG, Chen XH, Wang ZH (2015) Developmental changes in composition and morphology of cuticular waxes on leaves and spikes of glossy and glaucous wheat (Triticum aestivum L.). PLoS One 10(11):e0143671CrossRefGoogle Scholar
  69. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755CrossRefPubMedGoogle Scholar
  70. Zabka V, Stangl M, Bringmann G, Vogg G, Riederer M, Hildebrandt U (2008) Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol 177:251–263PubMedGoogle Scholar
  71. Zeisler V, Schreiber L (2016) Epicuticular wax on cherry laurel (Prunus laurocerasus) leaves does not constitute the cuticular transpiration barrier. Planta 243:65–81CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Viktoria Valeska Zeisler-Diehl
    • 1
  • Wilhelm Barthlott
    • 2
  • Lukas Schreiber
    • 1
  1. 1.Institute of Cellular and Molecular Botany (IZMB)University of BonnBonnGermany
  2. 2.Nees Institut for Biodiversity of PlantsUniversity of BonnBonnGermany

Personalised recommendations