Morphological diversity of β-diketone wax tubules on Eucalyptus gunnii leaves and real time observation of self-healing of defects in the wax layer
Miriam A. Huth A B , Axel Huth A and Kerstin Koch A
+ Author Affiliations
- Author Affiliations
A Rhine-Waal University of Applied Sciences, Faculty of Life Sciences, Marie-Curie-Str. 1, 47533 Kleve, Germany.
B Corresponding author. Email: miriam-anna.huth@hochschule-rhein-waal.de
Australian Journal of Botany 66(4) 313-324 https://doi.org/10.1071/BT18035
Submitted: 16 February 2018 Accepted: 27 May 2018 Published: 9 July 2018
Abstract
As part of the plant cuticle, epicuticular waxes build the boundary layer of a plant to its environment, fulfilling many vital functions. Epicuticular waxes are small crystalline structures which originate by self-assembly. The morphology of β-diketone tubules on Eucalyptus gunnii Hook.f. leaves was studied by field emission scanning electron microscopy (FE-SEM) and regeneration of removed waxes was investigated in real time by atomic force microscopy (AFM) on leaf surfaces. Smooth tubules as well as helically wound ribbons and transitional forms of tubules were found on adaxial leaf surfaces. Leaves of different developmental stages revealed no differences in their wax morphologies, but in the amount of wax allocation. After removal of the waxes regeneration was observed on leaves of all investigated ages. The regeneration of wax crystals started directly after wax removal and tubule growth could be observed in real time.
Additional keywords: atomic force microscopy (AFM), β-diketone tubules, epicuticular waxes, leaf surface, regeneration, scanning electron microscopy (SEM), self-healing, wax morphology.
References
Baker EA, Hunt GM (1986) Erosion of waxes from leaf surfaces by simulated rain. New Phytologist 102, 161–173.| Erosion of waxes from leaf surfaces by simulated rain.Crossref | GoogleScholarGoogle Scholar |
Barnes JD, Percy KE, Paul ND, Jones P, McLaughlin CK, Mullineaux PM, Creissen G, Wellburn AR (1996) The influence of UV-B radiation on the physicochemical nature of tobacco (Nicotiana tabacum L.) leaf surfaces. Journal of Experimental Botany 47, 99–109.
| The influence of UV-B radiation on the physicochemical nature of tobacco (Nicotiana tabacum L.) leaf surfaces.Crossref | GoogleScholarGoogle Scholar |
Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126, 237–260.
| Classification and terminology of plant epicuticular waxes.Crossref | GoogleScholarGoogle Scholar |
Barthlott W, Theisen I, Borsch T, Neinhuis C (2003) Epicuticular waxes and vascular plant systematics: integrating micromorphological and chemical data. Deep morphology: Toward a Renaissance of Morphology in Plant Systematics 67, 189–206.
Baum BR, Tulloch AP, Bailey LG (1989) Epicuticular waxes of genus Hordeum: a survey of their chemical composition and ultrastructure. Canadian Journal of Botany 67, 3219–3226.
| Epicuticular waxes of genus Hordeum: a survey of their chemical composition and ultrastructure.Crossref | GoogleScholarGoogle Scholar |
Beattie GA, Marcell LM (2002) Effect of alterations in cuticular wax biosynthesis on the physicochemical properties and topography of maize leaf surfaces. Plant, Cell & Environment 25, 1–16.
| Effect of alterations in cuticular wax biosynthesis on the physicochemical properties and topography of maize leaf surfaces.Crossref | GoogleScholarGoogle Scholar |
Bhushan B, Jung YC, Niemietz A, Koch K (2009) Lotus-like biomimetic hierarchical structures developed by the self-assembly of tubular plant waxes. Langmuir 25, 1659–1666.
| Lotus-like biomimetic hierarchical structures developed by the self-assembly of tubular plant waxes.Crossref | GoogleScholarGoogle Scholar |
Canet D, Rohr R, Chamel A, Guillain F (1996) Atomic force microscopy study of isolated ivy leaf cuticles observed directly and after embedding in Epon®. New Phytologist 134, 571–577.
| Atomic force microscopy study of isolated ivy leaf cuticles observed directly and after embedding in Epon®.Crossref | GoogleScholarGoogle Scholar |
Eaton P, West P (2010) ‘Atomic force microscopy.’ (Oxford University Press: Oxford, UK)
Edwards PB (1982) Do waxes on Eucalyptus leaves provide protection from grazing insects? Australian Journal of Ecology 7, 347–352.
| Do waxes on Eucalyptus leaves provide protection from grazing insects?Crossref | GoogleScholarGoogle Scholar |
Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Structure & Development 33, 91–102.
| The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects.Crossref | GoogleScholarGoogle Scholar |
Ensikat HJ, Barthlott W (1993) Liquid substitution: a versatile procedure for SEM specimen preparation of biological materials without drying or coating. Journal of Microscopy 172, 195–203.
| Liquid substitution: a versatile procedure for SEM specimen preparation of biological materials without drying or coating.Crossref | GoogleScholarGoogle Scholar |
Ensikat HJ, Boese M, Mader W, Barthlott W, Koch K (2006) Crystallinity of plant epicuticular waxes: electron and X-ray diffraction studies. Chemistry and Physics of Lipids 144, 45–59.
| Crystallinity of plant epicuticular waxes: electron and X-ray diffraction studies.Crossref | GoogleScholarGoogle Scholar |
Frewin CL (2012) ‘Atomic force microscopy investigation into biology – from cell to protein.’ (InTech Open: London)
Garrec JP, Henry C, Le Maout L (1995) Cires epi- et intracuticulaires: etude de leur separation, de leurs caracteristiques chimiques et de leurs rôles respectifs dans la permeabilité cuticulaire. Environmental and Experimental Botany 35, 399–409.
| Cires epi- et intracuticulaires: etude de leur separation, de leurs caracteristiques chimiques et de leurs rôles respectifs dans la permeabilité cuticulaire.Crossref | GoogleScholarGoogle Scholar |
Gorb EV, Baum MJ, Gorb SN (2013) Development and regeneration ability of the wax coverage in Nepenthes alata pitchers: a cryo-SEM approach. Scientific Reports 3, 3078
| Development and regeneration ability of the wax coverage in Nepenthes alata pitchers: a cryo-SEM approach.Crossref | GoogleScholarGoogle Scholar |
Guhling O, Kinzler C, Dreyer M, Bringmann G, Jetter R (2005) Surface composition of myrmecophilic plants: cuticular wax and glandular trichomes on leaves of Macaranga tanarius. Journal of Chemical Ecology 31, 2323–2341.
| Surface composition of myrmecophilic plants: cuticular wax and glandular trichomes on leaves of Macaranga tanarius.Crossref | GoogleScholarGoogle Scholar |
Hallam ND (1970) Growth and regeneration of waxes on the leaves of Eucalyptus. Planta 93, 257–268.
| Growth and regeneration of waxes on the leaves of Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Hallam ND, Chambers TC (1970) The leaf waxes of the genus Eucalyptus L’Héritier. Australian Journal of Botany 18, 335–386.
| The leaf waxes of the genus Eucalyptus L’Héritier.Crossref | GoogleScholarGoogle Scholar |
Henderson E (1994) Imaging of living cells by atomic force microscopy. Progress in Surface Science 46, 39–60.
| Imaging of living cells by atomic force microscopy.Crossref | GoogleScholarGoogle Scholar |
Heredia-Guerrero JA, De Lara R, Domínguez E, Heredia A, Benavente J, Benítez JJ (2012) Chemical-physical characterization of isolated plant cuticles subjected to low-dose γ-irradiation. Chemistry and Physics of Lipids 165, 803–808.
| Chemical-physical characterization of isolated plant cuticles subjected to low-dose γ-irradiation.Crossref | GoogleScholarGoogle Scholar |
Holmes MG, Keiller DR (2002) Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species. Plant, Cell & Environment 25, 85–93.
| Effects of pubescence and waxes on the reflectance of leaves in the ultraviolet and photosynthetic wavebands: a comparison of a range of species.Crossref | GoogleScholarGoogle Scholar |
Horn DHS, Kranz ZH, Lamberton JA (1964) The composition of Eucalyptus and some other leaf waxes. Australian Journal of Chemistry 17, 464–476.
| The composition of Eucalyptus and some other leaf waxes.Crossref | GoogleScholarGoogle Scholar |
Jeffree CE (2006) The fine structure of the plant cuticle. In ‘Biology of the plant cuticle’. (23rd edn) (Eds M Riederer, C Müller) pp. 11–125. (Blackwell Publishing Ltd: Oxford, UK)
Jeffree CE, Baker EA, Holloway PJ (1975) Ultrastructure and recrystallisation of plant epicuticular waxes. New Phytologist 75, 539–549.
| Ultrastructure and recrystallisation of plant epicuticular waxes.Crossref | GoogleScholarGoogle Scholar |
Jeffree C, Baker E, Holloway P (1976) ‘Microbiology of aerial plant surfaces.’ (Academic Press: New York)
Jetter R, Riederer M (1994) Epicuticular crystals of nonacosan-10-ol: in-vitro reconstitution and factors influencing crystal habits. Planta 195, 257–270.
| Epicuticular crystals of nonacosan-10-ol: in-vitro reconstitution and factors influencing crystal habits.Crossref | GoogleScholarGoogle Scholar |
Jetter R, Riederer M (1995) In vitro reconstitution of epicuticular wax crystals: formation of tubular aggregates by long-chain secondary alkanediols. Botanica Acta 108, 111–120.
| In vitro reconstitution of epicuticular wax crystals: formation of tubular aggregates by long-chain secondary alkanediols.Crossref | GoogleScholarGoogle Scholar |
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 Physiology 170, 921–934.
| 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.Crossref | GoogleScholarGoogle Scholar |
Jetter R, Riederer M, Lendzian KJ (1996) The effects of dry O3, SO2 and NO2 on reconstituted epicuticular wax tubules. New Phytologist 133, 207–216.
| The effects of dry O3, SO2 and NO2 on reconstituted epicuticular wax tubules.Crossref | GoogleScholarGoogle Scholar |
Kerstiens G (1996) Cuticular water permeability and its physiological significance. Journal of Experimental Botany 47, 1813–1832.
| Cuticular water permeability and its physiological significance.Crossref | GoogleScholarGoogle Scholar |
Koch K, Neinhuis C, Ensikat HJ, Barthlott W (2004) Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM). Journal of Experimental Botany 55, 711–718.
| Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM).Crossref | GoogleScholarGoogle Scholar |
Koch K, Barthlott W, Koch S, Hommes A, Wandelt K, Mamdouh W, De-Feyter S, Broekmann P (2006a) Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223, 258–270.
| Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals.Crossref | GoogleScholarGoogle Scholar |
Koch K, Dommisse A, Barthlott W (2006b) Chemistry and crystal growth of plant wax tubules of Lotus (Nelumbo nucifera) and Nasturtium (Tropaeolum majus) leaves on technical substrates. Crystal Growth & Design 6, 2571–2578.
| Chemistry and crystal growth of plant wax tubules of Lotus (Nelumbo nucifera) and Nasturtium (Tropaeolum majus) leaves on technical substrates.Crossref | GoogleScholarGoogle Scholar |
Koch K, Hartmann KD, Schreiber L, Barthlott W, Neinhuis C (2006c) Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability. Environmental and Experimental Botany 56, 1–9.
| Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability.Crossref | GoogleScholarGoogle Scholar |
Koch K, Bhushan B, Barthlott W (2008) Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4, 1943–1963.
| Diversity of structure, morphology and wetting of plant surfaces.Crossref | GoogleScholarGoogle Scholar |
Koch K, Bhushan B, Ensikat HJ, Barthlott W (2009) Self-healing of voids in the wax coating on plant surfaces. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 367, 1673–1688.
| Self-healing of voids in the wax coating on plant surfaces.Crossref | GoogleScholarGoogle Scholar |
Kolattukudy PE (1980) Biopolyester membranes of plants: cutin and suberin. Science 208, 990–1000.
| Biopolyester membranes of plants: cutin and suberin.Crossref | GoogleScholarGoogle Scholar |
Kolattukudy PE (2001) Polyesters in higher plants. Advances in Biochemical Engineering/Biotechnology 71, 1–49.
| Polyesters in higher plants.Crossref | GoogleScholarGoogle Scholar |
Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research 42, 51–80.
| Biosynthesis and secretion of plant cuticular wax.Crossref | GoogleScholarGoogle Scholar |
Meusel I, Neinhuis C, Markstädter C, Barthlott W (2000) Chemical composition and recrystallization of epicuticular waxes: coiled rodlets and tubules. Plant Biology 2, 462–470.
| Chemical composition and recrystallization of epicuticular waxes: coiled rodlets and tubules.Crossref | GoogleScholarGoogle Scholar |
Morris VJ, Kirby AR, Gunning AP (2009) ‘Atomic force microscopy for biologists.’ (2nd edn) (Imperial College Press: London)
Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Current Opinion in Plant Biology 9, 281–287.
| Unraveling the complex network of cuticular structure and function.Crossref | GoogleScholarGoogle Scholar |
Neinhuis C, Koch K, Barthlott W (2001) Movement and regeneration of epicuticular waxes through plant cuticles. Planta 213, 427–434.
| Movement and regeneration of epicuticular waxes through plant cuticles.Crossref | GoogleScholarGoogle Scholar |
Niemietz A, Wandelt K, Barthlott W, Koch K (2009) Thermal evaporation of multi-component waxes and thermally activated formation of nanotubules for superhydrophobic surfaces. Progress in Organic Coatings 66, 221–227.
| Thermal evaporation of multi-component waxes and thermally activated formation of nanotubules for superhydrophobic surfaces.Crossref | GoogleScholarGoogle Scholar |
Reina-Pinto JJ, Yephremov A (2009) Surface lipids and plant defenses. Plant Physiology and Biochemistry 47, 540–549.
| Surface lipids and plant defenses.Crossref | GoogleScholarGoogle Scholar |
Rentschler I (1971) Die Wasserbenetzbarkeit von Blattoberflächen und ihre submikroskopische Wachsstruktur. Planta 96, 119–135.
| Die Wasserbenetzbarkeit von Blattoberflächen und ihre submikroskopische Wachsstruktur.Crossref | GoogleScholarGoogle Scholar |
Richardson A, Franke R, Kerstiens G, Jarvis M, Schreiber L, Fricke W (2005) Cuticular wax deposition in growing barley (Hordeum vulgare) leaves commences in relation to the point of emergence of epidermal cells from the sheaths of older leaves. Planta 222, 472–483.
| Cuticular wax deposition in growing barley (Hordeum vulgare) leaves commences in relation to the point of emergence of epidermal cells from the sheaths of older leaves.Crossref | GoogleScholarGoogle Scholar |
Riederer M, Schreiber L (1995) Waxes: the transport barriers of plant cuticles. In ‘Waxes: chemistry, molecular biology and functions. Vol. 6. (Ed. RJ Hamilton) pp. 131–156. (The Oily Press: Dundee, Scotland)
Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52, 2023–2032.
| Protecting against water loss: analysis of the barrier properties of plant cuticles.Crossref | GoogleScholarGoogle Scholar |
Tulloch AP, Hoffman LL (1974) Epicuticular waxes of Secale cereale and Triticale hexaploide leaves. Phytochemistry 13, 2535–2540.
| Epicuticular waxes of Secale cereale and Triticale hexaploide leaves.Crossref | GoogleScholarGoogle Scholar |
von Wettstein-Knowles P (1972) Genetic control of β-diketone and hydroxy-β-diketone synthesis in epicuticular waxes of barley. Planta 106, 113–130.
| Genetic control of β-diketone and hydroxy-β-diketone synthesis in epicuticular waxes of barley.Crossref | GoogleScholarGoogle Scholar |
von Wettstein-Knowles P (1974) Ultrastructure and origin of epicuticular wax tubes. Journal of Ultrastructure Research 46, 483–498.
| Ultrastructure and origin of epicuticular wax tubes.Crossref | GoogleScholarGoogle Scholar |
Wirthensohn MG, Collins G, Jones GP, Sedgley M (1999) Variability in waxiness of Eucalyptus gunnii foliage for floriculture. Scientia Horticulturae 82, 279–288.
| Variability in waxiness of Eucalyptus gunnii foliage for floriculture.Crossref | GoogleScholarGoogle Scholar |
Zeisler V, Schreiber L (2016) Epicuticular wax on cherry laurel (Prunus laurocerasus) leaves does not constitute the cuticular transpiration barrier. Planta 243, 65–81.
| Epicuticular wax on cherry laurel (Prunus laurocerasus) leaves does not constitute the cuticular transpiration barrier.Crossref | GoogleScholarGoogle Scholar |
