Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

Evans Review No. 3: Structure–function relationships of the plant cuticle and cuticular waxes — a smart material?

Hendrik Bargel A C , Kerstin Koch B , Zdenek Cerman B and Christoph Neinhuis A D

A Institut für Botanik, Technische Universität Dresen, Zellescher Weg 22, 01062 Dresden, Germany.

B Nees-Institut für Biodiversität der Pflanzen, Universität Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany.

C Present address: Biotechnical Center, Technische Universität Darmstadt, Petersenstraße 20, 64287 Darmstadt, Germany.

D Corresponding author. Email:

E This paper is part of The Evans Review Series, named for Dr Lloyd Evans. The series contains reviews that are critical, state-of-the-art evaluations that aim to advance our understanding, rather than being exhaustive compilations of information, and are written by invitation.

F This paper is dedicated to Prof. Wilhelm Barthlott on the occasion of his 60th birthday.

Functional Plant Biology 33(10) 893-910
Submitted: 30 May 2006  Accepted: 18 August 2006   Published: 2 October 2006


The cuticle is the main interface between plants and their environment. It covers the epidermis of all aerial primary parts of plant organs as a continuous extracellular matrix. This hydrophobic natural composite consists mainly of the biopolymer, cutin, and cuticular lipids collectively called waxes, with a high degree of variability in composition and structure. The cuticle and cuticular waxes exhibit a multitude of functions that enable plant life in many different terrestrial habitats and play important roles in interfacial interactions. This review highlights structure–function relationships that are the subjects of current research activities. The surface waxes often form complex crystalline microstructures that originate from self-assembly processes. The concepts and results of the analysis of model structures and the influence of template effects are critically discussed. Recent investigations of surface waxes by electron and X-ray diffraction revealed that these could be assigned to three crystal symmetry classes, while the background layer is not amorphous, but has an orthorhombic order. In addition, advantages of the characterisation of formation of model wax types on a molecular scale are presented. Epicuticular wax crystals may cause extreme water repellency and, in addition, a striking self-cleaning property. The principles of wetting and up-to-date concepts of the transfer of plant surface properties to biomimetic technical applications are reviewed. Finally, biomechanical studies have demonstrated that the cuticle is a mechanically important structure, whose properties are dynamically modified by the plant in response to internal and external stimuli. Thus, the cuticle combines many aspects attributed to smart materials.

Keywords: AFM, anti-adhesive surfaces, biomimetics, biopolymer, epicuticular waxes, Lotus-Effect®, mechanical properties, plant cuticle, self-assembly, structure–function relationships, template effect.


Andrews J Adams SR Burton KS Edmondson RN 2002 a Partial purification of tomato fruit peroxidase and its effect on the mechanical properties of tomato fruit skin. Journal of Experimental Botany 53 2393 2399 doi:10.1093/jxb/erf109

Andrews J Adams SR Burton KS Evered CE 2002 b Subcellular localization of peroxidase in tomato fruit skin and the possible implications for the regulation of fruit growth. Journal of Experimental Botany 53 2185 2191 doi:10.1093/jxb/erf070

Baker EA 1974 The influence of environment on leaf wax development in Brassica oleracea var. gemmifera. New Phytologist 73 955 966 doi:10.1111/j.1469-8137.1974.tb01324.x

Baker EA (1982) Chemistry and morphology of plant epicuticular waxes. In ‘The plant cuticle’. (Eds DF Cutler, KL Alvin, CE Price) pp. 139–166. (Academic Press: London)

Baker EA , Bukovac MJ , Hunt GM (1982) Composition of tomato fruit cuticle as related to fruit growth and development. In ‘The plant cuticle’. (Eds DF Cutler, KL Alvin’ CE Price) pp. 33–44. (Academic Press: London)

Bargel H (2005) Biomechanical properties of the plant cuticle and its possible role as a structural stabilisation component. PhD thesis, Technische Universität Dresden.

Bargel H Neinhuis C 2004 Altered tomato (Lycopersicon esculentum Mill.) fruit cuticle biomechanics of a pleiotropic non-ripening mutant. Journal of Plant Growth Regulation 23 61 75 doi:10.1007/s00344-004-0036-0

Bargel H Neinhuis C 2005 Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. Journal of Experimental Botany 56 1049 1060 doi:10.1093/jxb/eri098

Bargel H , Barthlott W , Koch K , Schreiber L , Neinhuis C (2004 a) Plant cuticles: multifunctional interfaces between plant and environment. In ‘The evolution of plant physiology’. (Eds AR Hemsley, I Poole) pp. 171–194. (Elsevier Academic Press: London)

Bargel H Spatz HC Speck T Neinhuis C 2004 b Two-dimensional tension testing in plant biomechanics — sweet cherry fruit skin as a model system. Plant Biology 6 432 439 doi:10.1055/s-2004-821002

Bargel H , Stehfest K , Neinhuis C (2006) Altered tomato (Lycopersicon esculentum Mill.) fruit cuticle biomechanics of the non-ripening (nor) mutant during maturation. In ‘Proceedings of the 5th plant biomechanics conference’. Stockholm. (Ed. L Salmen) pp. 549–554. (STFI Packforsk: Stockholm)

Barthlott W 1981 Epidermal and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nordic Journal of Botany 3 345 355

Barthlott W (1990) Scanning electron microscopy of the epidermal surface in plants. In ‘Scanning electron microscopy in taxonomy and functional morphology’. (Ed. D Claugher) pp. 69–94. (Clarendon Press: Oxford)

Barthlott W Ehler N 1977 Raster-Elektronenmikroskopie der Epidermisoberflächen von Spermatophyten. Tropische und Subtropische Pflanzenwelt 19 367 467

Barthlott W Neinhuis C 1997 Purity of the sacred lotus or escape from contamination in biological surfaces. Planta 202 1 7

Barthlott W Neinhuis C 2001 The lotus effect: a self-cleaning surface based on a model taken from nature. Tekstil 50 461 465

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

Barthlott W , Theisen I , Borsch T , Neinhuis C (2003) Epicuticular waxes and vascular plant systematics: integrating micromorphological and chemical data. In ‘Deep morphology — towards a Renaissance of morphology in plant systematics’. (Eds TF Stuessy, V Mayer, E Hörandl) pp. 189–206. (A.R.G. Gantner: Ruggell)

Bateman RM Crane R DiMichele WA Kenrick PR Rowe NP Speck T Stein WE 1998 Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annual Reviews of Ecology and Systematics 29 263 292 doi:10.1146/annurev.ecolsys.29.1.263

Baum BR Tulloch AP Bailey LG 1989 Epicuticular waxes of the genus Hordeum: a survey of their chemical composition and ultrastructure. Canadian Journal of Botany 67 3219 3226

Beattie GA Lindow SE 1995 The secret life of foliar bacterial pathogens on leaves. Annual Review of Phytopathology 33 145 172

Benyus JM (1997) ‘Biomimicry: innovation inspired by nature.’ (Quill-William Morrow: New York)

Bianchi G (1995) Plant waxes. In ‘Waxes: chemistry, molecular biology and functions’. (Ed. RJ Hamilton) pp. 177–222. (The Oily Press: Dundee)

Bianchi G Lupotto E Russo S 1979 Composition of epicuticular wax of rice, Oryza sativa. Experientia 35 1417 doi:10.1007/BF01962755

Bird SM Gray JE 2003 Signals from the cuticle affect epidermal cell differentiation. New Phytologist 157 9 23 doi:10.1046/j.1469-8137.2003.00543.x

Bonaventure G Beisson F Ohlrogge J Pollard M 2004 Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6, cis-9-diene-1,18-dioate as the major component. The Plant Journal 40 920 930 doi:10.1111/j.1365-313X.2004.02258.x

Brownleader MD Jackson P Mobasheri A Pantelides AT Sumar S Trevan M Dey PM 1999 Molecular aspects of cell wall modifications during fruit ripening. Critical Reviews in Food Science and Nutrition 39 149 164 doi:10.1080/10408399908500494

Buchholz S Rabe JM 1992 Molecular imaging of alkanol monolayers on graphite. Angewandte Chemie International Edition 31 189 191 doi:10.1002/anie.199201891

Burton Z Bhushan B 2005 Hydrophobicity, adhesion, and friction properties of nanopatterned polymers and scale dependence for micro- and nanoelectromechanical systems. Nano Letters 5 1607 1613 doi:10.1021/nl050861b

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 doi:10.1111/j.1469-8137.1996.tb04922.x

Carr DJ Carr SGM Lenz JR 1985 Oriented arrays of epicuticular wax plates in Eucalyptus species. Protoplasma 124 205 212 doi:10.1007/BF01290771

Chambers TC Ritchie IM Booth MA 1976 Chemical models for plant wax morphogenesis. New Phytologist 77 43 49 doi:10.1111/j.1469-8137.1976.tb01499.x

Chamel A Pineri M Escoubes M 1991 Quantitative determination of water sorption by plant cuticles. Plant, Cell & Environment 14 87 95 doi:10.1111/j.1365-3040.1991.tb01374.x

Collinson ME Mösle B Finch P Scott AC Wilson R 1998 The preservation of plant cuticles in the fossil record: a chemical and microscopical investigation. Ancient Biomolecules 2 251 265

Conn KL Tewari JP 1989 Ultrastructure of epicuticular wax in canola. Zeitschrift für Naturforschung C 44 705 711

Courtney TH (1990) ‘Mechanical behaviour of materials.’ (McGraw-Hill: New York)

Croteau R Kolattukudy PE 1974 Biosynthesis of hydroxy fatty acid polymers. Enzymatic synthesis of cutin from monomers acids by cell-free preparations from the epidermis of Vicia faba leaves. Biochemistry 13 3193 3202

Cyr DM Venkataraman B Flynn GW 1996 STM investigations of organic molecules physisorbed at the liquid–solid interface. Chemistry of Materials 8 1600 1615 doi:10.1021/cm960113a

de Bary A (1871) Ueber die Wachsüberzüge der Epidermis. Botanische Zeitschrift 29, 128–139, 145–154, 161–176, 566–571, 573–585, 605–619.

De Feyter S De Schryver FC 2005 Self-assembly at the liquid / solid interface: STM reveals. Journal of Physical Chemistry B. Materials, Surfaces, Interfaces, & Biophysical 109 4290 4302

de Gennes PG , Brochard-Wyart F , Quéré D (2004) ‘Capillarity and wetting phenomena — drops, bubbles, pearls, waves.’ (Springer: New York)

Deshmukh AP Simpson AJ Hadad CM Hatcher PG 2005 Insights into the structure of cutin and cutan from Agave americana leaf cuticle using HRMAS NMR spectroscopy. Organic Geochemistry 36 1072 1085

Dominguez E Heredia A 1999 Water hydration in cutinized cell walls: a physico-chemical analysis. Biochimica et Biophysica Acta 1426 168 176

Dorset DL 2002 From waxes to polymers — crystallography of polydisperse chain assemblies. Structural Chemistry 13 329 337

Edelmann HG Neinhuis C Bargel H 2005 Influence of hydration and temperature on the rheological properties of plant cuticles and their impact on plant organ integrity. Journal of Plant Growth Regulation 24 116 126 doi:10.1007/s00344-004-0015-5

Edwards D , Abbot GD , Raven JA (1996) Cuticles of early land plants. In ‘Plant cuticles: an integrated functional approach’. (Ed. G Kerstiens) pp. 1–31. (Bios Scientific: Oxford)

Engel H 1939 Das Verhalten der Blätter bei Benetzung mit Wasser. Jahrbücher für wissenschaftliche Botanik 48 816 861

Ensikat HJ Neinhuis C Barthlott W 2000 Direct access to plant epicuticular wax crystals by a new mechanical isolation method. International Journal of Plant Sciences 161 143 148

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 in press

Erbil HY Demirel AL Avci Y Mert O 2003 Transformation of a simple plastic into a superhydrophobic surface. Science 299 1377 1380

Espelie KE Dean BB Kolattukudy PE 1979 Composition of lipid-derived polymers from different anatomical regions of several plant species. Plant Physiology 64 1089 1093

Feng L Li S Li Y Li H Zhang L Zhai J Song Y Liu B Jiang L Zhu D 2002 Super-hydrophobic surfaces: from natural to artificial. Advanced Materials 14 1857 1860

Fernandez S Osorio S Heredia A 1999 Monitoring and visualising plant cuticles by confocal laser scanning microscopy. Plant Physiology and Biochemistry 37 789 794 doi:10.1016/S0981-9428(00)86692-9

Ferrer MA Munoz R Barcelo AR 1991 A biochemical and cytochemical study of the cuticle-associated peroxidases in Lupinus. Annals of Botany 67 561 568

Fischer RL Bennett AB 1991 Role of cell wall hydrolases in fruit ripening. Annual Review of Plant Physiology and Plant Molecular Biology 42 675 703

Franke R Briesen I Wojciechowski T Faust A Yephremov A Nawrath C Schreiber L 2005 Apoplastic polyesters in Arabidopsis surface tissues — a typical suberin and a particular cutin. Phytochemistry 66 2643 2658 doi:10.1016/j.phytochem.2005.09.027

Fürstner R Neinhuis C Barthlott W 2000 The lotus effect: self-purification of microstructured surfaces. Nachrichten aus der Chemie 48 24 28

Fürstner R Barthlott W Neinhuis C Walzel P 2005 Wetting and self-cleaning properties of artificial superhydrophobic surfaces. Langmuir 21 956 961

Gesquière A Abdel-Mottaleb MMS De Feyter S de Schryver FC Sieffert M Müllen K Calderone A Lazzaroni R Brédas J-L 2000 Dynamics in physisorbed monolayers of 5-alkoxy-isophrhalic derivatives at the liquid/solid interface investigated by scanning tunneling microscopy. Chemistry–A European Journal 6 3739 3746 doi:10.1002/1521-3765(20001016)6:20<3739::AID-CHEM3739>3.0.CO;2-1

Giovannoni JJ 2004 Genetic regulation of fruit development and ripening. The Plant Cell 16 S170 S180 doi:10.1105/tpc.019158

Gleiche M Chi LF Fuchs H 2000 Nanoscopic channel lattices with controlled anisotropic wetting. Nature 403 173 175 doi:10.1038/35003149

Gomez-Campo C Tortosa ME Tewari I Tewari JP 1999 Epicuticular wax columns in cultivated Brassica species and in their close wild relatives. Annals of Botany 83 515 519 doi:10.1006/anbo.1999.0849

Graca J Schreiber L Rodrigues J Pereira H 2002 Glycerol and glyceryl esters of omega-hydroxyacids in cutins. Phytochemistry 61 205 215 doi:10.1016/S0031-9422(02)00212-1

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 doi:10.1007/s10886-005-7104-1

Gülz PG 1994 Epicuticular leaf waxes in the evolution of the plant kingdom. Journal of Plant Physiology 143 453 464

Günther I Wortmann GB 1966 Dust on the surface of leaves. Journal of Ultrastructure Research 15 522 527

Guo Z Zhou F Hao J Liu W 2005 Stable biomimetic super-hydrophobic engineering materials. Journal of the American Chemical Society 127 15 670 15 671

Haas K Brune T Rucker E 2001 Epicuticular wax crystalloids in rice and sugar cane leaves are reinforced by polymeric aldehydes. Journal of Applied Botany–Angewandte Botanik 75 178 187

Hallam ND Chambers TC 1970 The leaf waxes of the genus Eucalyptus L’Heritier. Australian Journal of Botany 18 335 386

Hasenstein KH Pescareta TC Sullivan VI 1993 Thigmonasticity of thistle staminal filaments II. Mechano-elastic properties. Planta 190 58 64 doi:10.1007/BF00195675

Heredia A 2003 Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochimica et Biophysica Acta 1620 1 7

Hoh JH Hansma PK 1992 Atomic force microscopy for high-resolution imaging in cell biology. Trends in Cell Biology 2 208 213

Holloway PJ 1969 The effects of superficial wax on leaf wettability. The Annals of Applied Biology 63 145 153

Holloway PJ 1970 Surface factors affecting the wetting of leaves. Pesticide Science 1 156 163

Holloway PJ (1971) The chemical and physical characteristics of leaf surfaces. In ‘Ecology of leaf surface micro-organisms’. (Eds TF Preece, CH Dickinson) pp. 39–53. (Academic Press: London)

Holloway PJ (1982) Structure and histochemistry of plant epicuticular membranes: an overview. In ‘The plant cuticle’. (Eds DF Cutler, KL Alvin, CE Price) pp. 1–32. (Academic Press: London)

Holloway PJ (1994) Plant cuticles: physicochemical characteristics and biosynthesis. In ‘Air pollution and the leaf cuticle’. (Eds KE Percy, JN Cape, R Jagels, CJ Simpson) pp. 1–13. (Springer: New York)

Holloway PJ Brown GA 1981 Ultrahistochemical detection of epoxides in plant cuticular membranes. Journal of Experimental Botany 32 1051 1066

Holloway PJ Jeffree CE Baker EA 1976 Structural determination of secondary alcohols from plant epicuticular waxes. Phytochemistry 15 1768 1770

Holton TA Cornish EC 1995 Genetics and biochemistry of anthocyanin biosynthesis. The Plant Cell 7 1071 1083 doi:10.1105/tpc.7.7.1071

Hunt GM Baker EA 1980 Phenolic constituents of tomato fruit cuticles. Phytochemistry 19 1415 1419

Jeffree CE (1996) Structure and ontogeny of plant cuticles. In ‘Plant cuticles an integrated functional approach’. (Ed. G Kerstiens) pp. 33–82. (Bios Scientific: Oxford)

Jeffree CE (2006) The fine structure of the plant cuticle. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 11–125. (Blackwell: Oxford)

Jeffree CE Baker EA Holloway PJ 1975 Ultrastructure and recrystallization of plant epicuticular waxes. New Phytologist 75 539 549

Jeffree CE , Baker EA , Holloway PJ (1976) Origins of the fine structure of plant epicuticular waxes. In ‘Microbiology of aerial plant surfaces’. (Eds CH Dickinson, TF Preece) pp. 119–158. (Academic Press: London)

Jenks MA Ashworth EN 1999 Plant epicuticular waxes: function, production and genetics. Horticultural Reviews 23 1 68

Jetter R Riederer M 1994 Epicuticular crystals of nonacosan-10-ol: in-vitro reconstitution and factors influencing crystal habits. Planta 195 257 270

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

Jetter R Schäffer S 2001 Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant Physiology 126 1725 1737

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 & Environment 23 619 628 doi:10.1046/j.1365-3040.2000.00581.x

Jetter R , Kunst L , Samuels AL (2006) Composition of plant cuticular waxes. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 145–181. (Blackwell Publishing: Oxford)

Jiang L Zhao Y Zhai J 2004 A lotus-leaf-like superhydrophobic surface: a porous microsphere / nanofiber composite film prepared by electrohydrodynamics. Angewandte Chemie International Edition 43 4438 4441

Jimenez A Creissen G Kular B Firmin J Robinson S Verhoeyen M Mullineaux P 2002 Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214 751 758

Juniper BE (1991) The leaf from the inside and the outside: a microbe’s perspective. In ‘Microbial ecology of leaves’. (Eds JH Andrews, SS Hirano) pp. 21–42. (Springer: New York)

Knoche M Beyer M Peschel S Oparlakov B Bukovac MJ 2004 Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiologia Plantarum 120 667 677 doi:10.1111/j.0031-9317.2004.0285.x

Koch K , Barthlott W , Neinhuis C (2003 a) Epicuticular waxes. In ‘Mac Graw-Hill yearbook of science & technology’. pp. 116–118. (Mac Graw-Hill: New York)

Koch K , Dommisse A , Neinhuis C , Barthlott W (2003 b) Self-assembly of epicuticular waxes on living plant surfaces by atomic force microscopy. In ‘Scanning tunneling microscopy / spectroscopy and related techniques’. (Eds PM Koenraad, M Kemerink) pp. 457–460. (American Institute of Physics: Melville)

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 doi:10.1093/jxb/erh077

Koch K Barthlott W Koch S Hommes A Wandelt K Mamdouh W De-Feyter S Broekmann P 2006 a Structural analysis of wheat wax (Triticum aestivum cv ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223 258 270 doi:10.1007/s00425-005-0081-3

Koch K Hartmann KD Schreiber L Barthlott W Neinhuis C 2006 b Influence of air humidity on epicuticular wax chemical composition, morphology and wettability of leaf surfaces. Environmental and Experimental Botany 56 1 9 doi:10.1016/j.envexpbot.2004.09.013

Kolattukudy PE 1980 Biopolyester membranes of plants: cutin and suberin. Science 208 990 1000

Kolattukudy PE (2001) Polyesters in higher plants. In ‘Advances in biochemical engineering / biotechnology’. (Ed. T Scheper) pp. 4–49. (Springer: Berlin)

Krauss P Markstädter C Riederer M 1997 Attenuation of UV radiation by plant cuticles from woody species. Plant, Cell & Environment 20 1079 1085

Kreger DR Schamhart C 1956 On the long crystal spacings in wax esters and their value in micro-analysis of plant cuticle waxes. Biochimica et Biophysica Acta 19 22 44 doi:10.1016/0006-3002(56)90382-1

Kunst L Samuels AL 2003 Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research 42 51 80 doi:10.1016/S0163-7827(02)00045-0

Kunst L , Jetter R , Samuels AL (2006) Biosynthesis and transport of plant cuticular waxes. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 182–215. (Blackwell: Oxford)

Kurdyukov S Faust A Nawrath C Bär S Voisin D et al 2006 The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. The Plant Cell 321 339 doi:10.1105/tpc.105.036079

Lafuma A Quéré D 2003 Superhydrophobic states. Nature Materials 2 457 460 doi:10.1038/nmat924

Laguna L Casado CG Heredia A 1999 Flavonoid biosynthesis in tomato fruit cuticles after in vivo incorporation of H-3-phenylalanine precursor. Physiologia Plantarum 105 491 498 doi:10.1034/j.1399-3054.1999.105314.x

Larsson K (1994) ‘Lipids — molecular organization, physical functions and technical applications.’ (Bell and Bain Ltd.: Glasgow)

Le Poulennec C Cousty J Xie ZX Mioskowski C 2000 Self-organisation of physisorbed secondary alcohol molecules on a graphite surface. Surface Science 448 93 100 doi:10.1016/S0039-6028(99)01106-1

Lees GL 1984 Cuticle and cell wall thickness: relation to mechanical strength of whole leaves and isolated cells from some forage legumes. Crop Science 24 1077 1081

Leveau JHJ (2006) Microbial communities in the phyllosphere. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 334–367. (Blackwell: Oxford)

Lownds NK Bukovac MJ 1988 Studies on octylphenoxy surfactants: V. toxicity to cowpea leaves and effects or spray application parameters. Journal of the American Society for Horticultural Science 113 205 210

Marechal Y Chamel A 1996 Water in a biomembrane by infrared spectrometry. Journal of Physical Chemistry 100 8551 8555

Marga F Pesacreta TC Hasenstein KH 2001 Biochemical analysis of elastic and rigid cuticles of Cirsium horridulum Michx. Planta 213 841 848

Marmur A 2003 Wetting on hydrophobic rough surfaces: to be heterogeneous or not to be? Langmuir 19 8343 8348

Matas A Heredia A 1999 Molecular dynamics modellization and simulation of water diffusion through plant cutin. Zeitschrift für Naturforschung C 54 896 902

Matas AJ Sanz MJ Heredia A 2003 Studies on the structure of the plant wax nonacosan-10-ol, the main component of epicuticular wax conifers. International Journal of Biological Macromolecules 33 31 35

Matas AJ Cobb ED Bartsch JA Paolillo DJ Niklas KJ 2004 a Biomechanics and anatomy of Lycopersicon esculentum fruit peels and enzyme-treated samples. American Journal of Botany 91 352 360

Matas AJ Cobb ED Paolillo DJ Niklas KJ 2004 b Crack resistance in cherry tomato fruit correlates with cuticular membrane thickness. HortScience 36 1354 1358

Matas AJ Cuartero J Heredia A 2004 c Phase transitions in the biopolyester cutin isolated from tomato fruit cuticles. Thermochimica Acta 409 165 168

Matas AJ Lópes-Casado G Cuartero J Heredia A 2005 Relative humidity and temperature modify the mechanical properties of isolated tomato fruit cuticles. American Journal of Botany 92 462 468

Meusel I Leistner E Barthlott W 1994 Chemistry and micromorphology of compound epicuticular wax crystalloids (Strelitzia type). Plant Systematics and Evolution 193 115 123

Meusel I Neinhuis C Markstädter C Barthlott W 1999 Ultrastructure, chemical composition and recrystallisation of epicuticular waxes: transversely ridged rodlets. Canadian Journal of Botany 77 706 720 doi:10.1139/cjb-77-5-706

Meusel I Barthlott W Kutzke H Barbier B 2000 a Crystallographic studies of plant waxes. Powder Diffraction 15 123 129

Meusel I Neinhuis C Markstadter C Barthlott W 2000 b Chemical composition and recrystallization of epicuticular waxes: coiled rodlets and tubules. Plant Biology 2 462 470

Mo H Trogisch S Taub H Ehrlich SN Volkmann UG Hansen FY Pino M 2004 Studies on the structure and growth mode of dotriacontane films by synchrotron x-ray scattering and molecular dynamics simulations. Journal of Physics Condensed Matter 16 S2905 S2910 doi:10.1088/0953-8984/16/29/005

Mondal K Sharma NS Malhotra SP Dhawan K Singh R 2004 Antioxidant systems in ripening tomato fruits. Biologia Plantarum 48 49 53 doi:10.1023/B:BIOP.0000024274.43874.5b

Morris VJ , Kirby AR , Gunning AP (1999) ‘Atomic force microscopy for biologists.’ (Imperial College Press: London)

Mösle B Finch P Collinson ME Scott AC 1997 Comparison of modern and fossil plant cuticles by selective chemical extraction monitored by flash pyrolysis–gas chromatography–mass spectroscopy and electron microscopy. Journal of Analytical and Applied Pyrolysis 40–41 585 597 doi:10.1016/S0165-2370(97)00039-9

Neinhuis C Barthlott W 1997 Characterisation and distribution of water-repellent, self-cleaning plant surfaces. Annals of Botany 79 667 677 doi:10.1006/anbo.1997.0400

Neinhuis C Jetter R 1995 Ultrastructure and chemistry of epicuticular wax crystals in Polytrichales sporophytes. Journal of Bryology 18 399 406

Neinhuis C Koch K Barthlott W 2001 Movement and regeneration of epicuticular waxes through plant cuticles. Planta 213 427 434

Nielsen LE , Landel RF (1994) ‘Mechanical properties of polymers and composites.’ (Marcel Dekker: New York)

Noga G Knoche M Wolter M Barthlott W 1987 Changes in leaf micromorphology induced by surfactant application. Angewandte Botanik 61 521 528

Nosonovsky M Bhushan B 2005 Roughness optimization for biomimetic superhydrophobic surfaces. Microsystem Technologies 11 535 549

Otten A Herminghaus S 2004 How plants keep dry: a physicist’s point of view. Langmuir 20 2405 2408 doi:10.1021/la034961d

Patankar NA 2004 Mimicking the lotus-effect: influence of double roughness structures and slender pillars. Langmuir 20 8209 8213 doi:10.1021/la048629t

Pesacreta TC Sullivan VI Hasenstein KH Durand JM 1991 Thigmonasticity of thistle staminal filaments I. Involvement of a contractile cuticle. Protoplasma 163 174 180 doi:10.1007/BF01323341

Petracek PD Bukovac MJ 1995 Rheological properties of enzymatically isolated tomato fruit cuticle. Plant Physiology 109 675 679

Popp C Burghardt M Friedmann A Riederer M 2005 Characterization of hydrophilic and lipophilic pathways of Hedera helix L. cuticular membranes: permeation of water and uncharged organic compounds. Journal of Experimental Botany 56 2797 2806

Post-Beittenmiller D 1996 Biochemistry and molecular biology of wax production in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47 405 430 doi:10.1146/annurev.arplant.47.1.405

Ramírez FJ Luque P Heredia A Bukovac MJ 1992 Fourier transform IR study of enzymatically isolated tomato fruit cuticular membrane. Biopolymers 32 1425 1429 doi:10.1002/bip.360321102

Reina JJ Heredia A 2001 Plant cutin biosynthesis: the involvement of a new acyltransferase. Trends in Plant Science 6 296 doi:10.1016/S1360-1385(01)02012-X

Rentschler I (1973) Die Bedeutung der Wachsstruktur auf den Blättern für die Empfindlichkeit der Pflanzen gegenüber Luftverunreinigungen. In ‘Proceedings of the 3rd international clean air congress’. pp. a139–a142. (VDI-Verlag: Düsseldorf)

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. European Biophysics Journal 23 59 70 doi:10.1007/BF00192206

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 doi:10.1007/s00425-005-1552-2

Riedel M Eichner A Jetter R 2003 Slippery surfaces of carnivorous plants: composition of epicuticular wax crystals in Nepenthes alata Blanco pitchers. Planta 218 87 97 doi:10.1007/s00425-003-1075-7

Riederer M Schönherr J 1988 Development of plant cuticles: fine structure and cutin composition of Clivia miniata Reg. leaves. Planta 174 127 138 doi:10.1007/BF00394885

Riederer M , Schreiber L (1995) Waxes — the transport barriers of plant cuticles. In ‘Waxes: chemistry, molecular biology and functions’. (Ed. RJ Hamilton) pp. 131–156. (The Oily Press: Dundee)

Riederer M Schreiber L 2001 Protecting against water loss: analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52 2023 2032 doi:10.1093/jexbot/52.363.2023

Riederer M , Müller C (2006) ‘Biology of the plant cuticle.’ (Blackwell: Oxford)

Round AN Yan B Dang S Estephan R Stark RE Batteas JD 2000 The influence of water on the nanomechanical behavior of the plant biopolyester cutin studies by AFM and solid-state NMR. Biophysical Journal 79 2761 2767

Schouten S Moerkerken P Gelin F Baas M de Leeuw JW Damste JSS 1998 Structural characterization of aliphatic, non-hydrolyzable biopolymers in freshwater algae and a leaf cuticle using ruthenium tetroxide degradation. Phytochemistry 49 987 993

Schreiber L 2005 Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Annals of Botany 95 1069 1073 doi:10.1093/aob/mci122

Schreiber L (2006) Characterization of polar paths of transport in plant cuticles. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 280–291. (Blackwell: Oxford)

Schreiber L Schorn K Heimburg T 1997 H-2 NMR study of cuticular wax isolated from Hordeum vulgare L. leaves: identification of amorphous and crystalline wax phases. European Biophysics Journal with Biophysics Letters 26 371 380

Shepherd T Robertson GW Griffiths DW Birch ANE Duncan G 1995 Effects of environment on the composition of epicuticular wax from kale and swede. Phytochemistry 40 407 417

Stark RE , Tian S (2006) The cutin biopolymer matrix. In ‘Biology of the plant cuticle’. (Eds M Riederer, C Müller) pp. 126–144. (Blackwell: Oxford)

Stark RE Yan B Ray AK Chen Z Fang X Garbow JR 2000 NMR studies of structure and dynamics in fruit cuticle polyesters. Solid State Nuclear Magnetic Resonance 16 37 45 doi:10.1016/S0926-2040(00)00052-7

Stevens JF Hart HT Pouw AJA Bolck A Zwaving JH 1994 Epicuticular waxes of Sedum series Rupestria. Phytochemistry 36 341 348 doi:10.1016/S0031-9422(00)97072-9

Suh MC Samuels AL Jetter R Kunst L Pollard M Ohlrogge J Beisson F 2005 Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiology 139 1649 1665 doi:10.1104/pp.105.070805

Sun M Luo C Xu L Ji H Ouyang Q Yu D Chen Y 2005 Artificial lotus leaf by nanocasting. Langmuir 21 8978 8981 doi:10.1021/la050316q

Thair BW Lister GR 1975 The distribution and fine structure of the epicuticular leaf wax of Pseudotsuga menziezii. Canadian Journal of Botany 53 1063 1071

Thompson DS 2001 Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit. Journal of Experimental Botany 52 1291 1301

Thompson DS Davies WJ Ho LC 1998 Regulation of tomato fruit growth by epidermal cell wall enzymes. Plant, Cell & Environment 21 589 599 doi:10.1046/j.1365-3040.1998.00308.x

Tulloch AP 1973 Composition of leaf surface waxes of Triticum species: variation with age and tissue. Phytochemistry 12 2225 2232 doi:10.1016/0031-9422(73)85124-6

Tulloch AP Hoffman LL 1974 Epicuticular waxes of Secale cereale and Triticale hexaploid leaves. Phytochemistry 13 2535 2540 doi:10.1016/S0031-9422(00)86932-0

Tulloch AP Baum BR Hoffman LL 1980 A survey of epicuticular waxes among genera of Triticeae. 2. Chemistry. Canadian Journal of Botany 58 2602 2615

Turunen M Huttunen S 1990 A review of the response of epicuticular waxes of conifer needles to air pollution. Journal of Environmental Quality 19 35 45

van Bergen PF , Blokker P , Collinson ME , Sinnighe Damsté JS , de Leeuw JW (2004) Structural biomacromolecules in plants: what can be learnt from the fossil record? In ‘The evolution of plant physiology — from whole plants to ecosystems’. (Eds AR Hemsley, I Poole) pp. 133–154. (Elsevier Academic Press: London)

Villena JF Dominguez E Stewart D Heredia A 1999 Characterization and biosynthesis of non-degradable polymers in plant cuticles. Planta 208 181 187

Villena JF Dominguez E Heredia A 2000 Monitoring biopolymers present in plant cuticles by FT–IR spectroscopy. Journal of Plant Physiology 156 419 422

von Wettstein-Knowles P 1974 Ultrastructure and origin of epicuticular wax tubes. Journal of Ultrastructure Research 46 483 498

von Wettstein-Knowles P (1995) Biosynthesis and genetics of waxes. In ‘Waxes: chemistry, molecular biology and functions’. (Ed. RJ Hamilton) pp. 91–130. (The Oily Press: Dundee)

Wagner T Neinhuis C Barthlott W 1996 Wettability and contaminability of insect wings as a function of their surface sculpture. Acta Zoologica 77 213 225

Wagner P Fürstner R Barthlott W Neinhuis C 2003 Quantitative assessment to the structural basis of water repellency in natural and technical surfaces. Journal of Experimental Botany 54 1295 1303

Walton TJ (1990) Waxes, cutin and suberin. In ‘Lipids, membranes and aspects of photobiology’. (Eds JL Harwood, JR Bowyer) pp. 105–158. (Academic Press: London)

Whitecross MI Armstrong DJ 1972 Environmental effects on epicuticular waxes of Brassica napus L. Australian Journal of Botany 20 87 95 doi:10.1071/BT9720087

Whitesides GM Mathias JP Seto CT 1991 Molecular self-assembly and nanochemistry — a chemical strategy for the synthesis of nanostructures. Science 254 1312 1319

Wiedemann P Neinhuis C 1998 Biomechanics of isolated plant cuticles. Botanica Acta 111 28 34

Wollenweber E (1984) The systematic implication of flavonoids secreted by plants. In ‘Biology and chemistry of plant trichomes’. (Ed. E Rodriguez, PL Healey, I Mehta) pp. 53–69. (Plenum Press: New York)

Wollenweber E Schneider H 2000 Lipophilic exudates of Pteridaceae — chemistry and chemotaxonomy. Biochemical Systematics and Ecology 28 751 777

Wolter M Barthlott W Knoche M Noga GJ 1988 Concentration effects and regeneration of epicuticular waxes after treatment with Triton X-100 surfactant. Angewandte Botanik 62 53 62

Xiao FM Goodwin SM Xiao YM Sun ZY Baker D Tang XY Jenks MA Zhou JM 2004 Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO Journal 23 2903 2913

Xie Q Xu J Feng L Jiang L Tang WX Luo X Han CC 2004 Facile creation of a super-amphiphobic coating surface with bionic microstructure. Advanced Materials 16 302 305 doi:10.1002/adma.200306281

Yephremov A Schreiber L 2005 The dark side of the cell wall: molecular genetics of plant cuticle. Plant Biosystems 139 74 79

Zhang S 2003 Fabrication of novel biomaterials through molecular self-assembly. Nature Biotechnology 21 1171 1178

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