Revisiting plant cuticle biophysics.

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      Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE
    • Publication Information:
      Publication: Oxford : Wiley on behalf of New Phytologist Trust
      Original Publication: London, New York [etc.] Academic Press.
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    • Abstract:
      The plant cuticle is located at the interface of the plant with the environment, thus acting as a protective barrier against biotic and abiotic external stress factors, and regulating water loss. Additionally, it modulates mechanical stresses derived from internal tissues and also from the environment. Recent advances in the understanding of the hydric, mechanical, thermal, and, to a lower extent, optical and electric properties of the cuticle, as well as their phenomenological connections and relationships are reviewed. An equilibrium based on the interaction among the different biophysical properties is essential to ensure plant growth and development. The notable variability reported in cuticle geometry, surface topography, and microchemistry affects the analysis of some biophysical properties of the cuticle. This review aimed to provide an updated view of the plant cuticle, understood as a modification of the cell wall, in order to establish the state-of-the-art biophysics of the plant cuticle, and to serve as an inspiration for future research in the field.
      (© 2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.)
    • References:
      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.
      Bargel H, Spatz HC, Speck T, Neinhuis C. 2004. Two‐dimensional tension tests in plant biomechanics – sweet cherry fruit skin as a model system. Plant Biology 6: 432–439.
      Baur P, Stulle K, Schönherr J, Uhlig B. 1998. Absorption of UV‐B to blue light radiation by leaf cuticles of selected crop plants. Gartenbauwissenschaft 63: 145–152.
      Benavente J, Ramos‐Barrado JR, Heredia A. 1998. A study of the electrical behaviour of isolated tomato cuticular membranes and cutin by impedance spectroscopy measurements. Colloids and Surfaces A: Physicochemical and Engineering Aspects 140: 333–338.
      Benítez JJ, González Moreno A, Guzmán‐Puyol S, Heredia‐Guerrero JA, Heredia A, Domínguez E. 2022. The response of tomato fruit cuticles against heat and light. Frontiers in Plant Science 12: 807723.
      Benítez JJ, Guzmán‐Puyol S, Vilaplana F, Heredia‐Guerrero JA, Domínguez E, Heredia A. 2021. Mechanical performances of isolated cuticles along tomato fruit growth and ripening. Frontiers in Plant Science 12: 787839.
      Beyer M, Lau S, Knoche M. 2005. Studies on water transport through the sweet cherry fruit surface: IX. Comparing permeability in water uptake and transpiration. Planta 220: 474–485.
      Bidhendi AJ, Lampron O, Frédérick PG, Geitmann A. 2023. Cell geometry regulates tissue fracture. Nature Communications 14: 8275.
      Boanares D, Bueno A, de Souza AX, Kozovits AR, Sousa HC, Pimenta LPS, Isaias RMS, França MGC. 2021. Cuticular wax composition contributes to different strategies of foliar water uptake in six plant species from foggy rupestrian grassland in tropical mountains. Phytochemistry 190: 112894.
      Bringe K, Hunsche M, Schmitz‐Eiberger M, Noga G. 2007. Retention and rainfastness of mancozeb as affected by physicochemical characteristics of adaxial apple leaf surface after enhanced UV‐B radiation. Journal of Environmental Science and Health – Part B Pesticides, Food Contaminants, and Agricultural Wastes 42: 133–141.
      Brüggenwirth M, Fricke H, Knoche M. 2014. Biaxial tensile tests identify epidermis and hypodermis as the main structural elements of sweet cherry skin. AoB Plants 6: plu019.
      Bueno A, Alfarhan A, Arand K, Burghardt M, Deininger AC, Hedrich R, Leide J, Seufert P, Staiger S, Riederer M. 2019. Effects of temperature on the cuticular transpiration barrier of two desert plants with water‐spender and water‐saver strategies. Journal of Experimental Botany 70: 1613–1625.
      Camacho‐Vázquez C, Ruiz‐May E, Guerrero‐Analco JA, Elizalde‐Contreras JM, Enciso‐Ortiz EJ, Rosas‐Saito G, López‐Sánchez L, Kiel‐Martínez AL, Bonilla‐Landa I, Monribot‐Villanueva JL et al. 2019. Filling gaps in our knowledge on the cuticle of mangoes (Mangifera indica) by analyzing six fruit cultivars: architecture/structure, postharvest physiology and possible resistance to fruit fly (Tephritidae) attack. Postharvest Biology and Technology 148: 83–96.
      Chamel A, Pineri M, Escoubes M. 1991. Quantitative determination of water sorption by plant cuticles. Plant, Cell & Environment 14: 87–95.
      Chen M, Zhang Y, Kong X, Du Z, Zhou H, Yu Z, Qin J, Chen C. 2021. Leaf cuticular transpiration barrier organization in tea tree under normal growth conditions. Frontiers in Plant Science 12: 655799.
      Chen M, Zhu X, Zhang Y, Du Z, Chen X, Kong X, Sun W, Chen C. 2020. Drought stress modify cuticle of tender tea leaf and mature leaf for transpiration barrier enhancement through common and distinct modes. Scientific Reports 10: 6696.
      Diarte C, Xavier de Souza A, Staiger S, Deininger AC, Bueno A, Burghardt M, Graell J, Riederer M, Lara I, Leide J. 2021. Compositional, structural and functional cuticle analysis of Prunus laurocerasus L. sheds light on cuticular barrier plasticity. Plant Physiology and Biochemistry 158: 434–445.
      Domínguez E, Cuartero J, Heredia A. 2011a. An overview on plant cuticle biomechanics. Plant Science 181: 77–84.
      Domínguez E, Heredia A. 1999. Water hydration in cutinized cell walls: a physico‐chemical analysis. Biochimica et Biophysica Acta – General Subjects 1426: 168–176.
      Domínguez E, Heredia‐Guerrero JA, Heredia A. 2011b. The biophysical design of plant cuticles: an overview. New Phytologist 189: 938–949.
      Domínguez E, Heredia‐Guerrero JA, Heredia A. 2017. The plant cuticle: old challenges, new perspectives. Journal of Experimental Botany 68: 5251–5255.
      Domínguez E, López‐Casado G, Cuartero J, Heredia A. 2008. Development of fruit cuticle in cherry tomato (Solanum lycopersicum). Functional Plant Biology 35: 403–411.
      Fernández V, Almonte L, Bahamonde HA, Galindo‐Bernabeu A, Sáenz‐Arce G, Colchero J. 2024. Chemical and structural heterogeneity of olive leaves and their trichomes. Communications Biology 7: 352.
      Fernández V, Bahamonde HA, Peguero‐Pina JJ, Gil‐Pelegrín E, Sancho‐Knapik D, Gil L, Goldbach HE, Eichert T. 2017. Physico‐chemical properties of plant cuticles and their functional and ecological significance. Journal of Experimental Botany 68: 5293–5306.
      Fernández V, Gil‐Pelegrín E, Eichert T. 2021. Foliar water and solute absorption: an update. The Plant Journal 105: 870–883.
      Fernández V, Khayet M. 2015. Evaluation of the surface free energy of plant surfaces: toward standardizing the procedure. Frontiers in Plant Science 6: 510.
      Fernández‐Muñoz R, Heredia A, Domínguez E. 2022. The role of cuticle in fruit shelf‐life. Current Opinion in Biotechnology 78: 102802.
      Fich EA, Fisher J, Zamir D, Rose JKC. 2020. Transpiration from tomato fruit occurs primarily via trichome‐associated transcuticular polar pores. Plant Physiology 184: 1840–1852.
      González Moreno A, de Cózar A, Prieto P, Domínguez E, Heredia A. 2022. Radiationless mechanism of UV deactivation by cuticle phenolics in plants. Nature Communications 13: 1786.
      González Moreno A, Domínguez E, Mayer K, Xiao N, Bock P, Heredia A, Gierlinger N. 2023a. 3D (x‐y‐t) Raman imaging of tomato fruit cuticle: microchemistry during development. Plant Physiology 191: 219–232.
      González Moreno A, Woolley JM, Domínguez E, de Cózar A, Heredia A, Stavros VG. 2023b. Synergic photoprotection of phenolic compounds present in tomato fruit cuticle: a spectroscopic investigation in solution. Physical Chemistry Chemical Physics 25: 12791–12799.
      Grimm E, Peschel S, Becker T, Knoche M. 2012. Stress and strain in the sweet cherry skin. Journal of the American Society for Horticultural Science 137: 383–390.
      Guzmán P, Fernández V, García ML, Khayet M, Fernández A, Gil L. 2014. Localization of polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzyme‐gold labelling. Plant Physiology and Biochemistry 76: 1–6.
      Guzmán‐Delgado P, Laca E, Zwieniecki MA. 2021. Unravelling foliar water uptake pathways: the contribution of stomata and the cuticle. Plant, Cell & Environment 44: 1728–1740.
      Henningsen JN, Bahamonde HA, Mühling KH, Fernández V. 2023. Tomato and pepper leaf parts contribute differently to the absorption of foliar‐applied potassium dihydrogen phosphate. Plants 12: 2152.
      Heredia A, Benavente J. 1991. A study of membrane potential across isolated fruit cuticles for NaCl and CaCl2 solutions. Biochimica et Biophysica Acta (BBA) – Biomembranes 1062: 239–244.
      Hunt GM, Baker EA. 1980. Phenolic constituents of tomato fruit cuticles. Phytochemistry 19: 1415–1419.
      Jetter R, Kunst L, Samuels AL. 2006. Composition of plant cuticular waxes. In: Riederer M, Müller C, eds. Biology of the plant cuticle. Oxford, UK: Blackwell, 182–215.
      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.
      Kakani VG, Reddy KR, Zhao D, Mohammed AR. 2003. Effects of ultraviolet‐B radiation on cotton (Gossypium hirsutum L.) morphology and anatomy. Annals of Botany 91: 817–826.
      Kamtsikakis A, Baales J, Zeisler‐Diehl VV, Vanhecke D, Zoppe JO, Schreiber L, Weder C. 2021. Asymmetric water transport in dense leaf cuticles and cuticle‐inspired compositionally graded membranes. Nature Communications 12: 1267.
      Karabourniotis G, Liakopoulos G, Bresta P, Nikolopoulos D. 2021. The optical properties of leaf structural elements and their contribution to photosynthetic performance and photoprotection. Plants 10: 1455.
      Khanal BP, Knoche M. 2017. Mechanical properties of cuticles and their primary determinants. Journal of Experimental Botany 68: 5351–5367.
      Khanal BP, Knoche M, Bußler S, Schlüter O. 2014. Evidence for a radial strain gradient in apple fruit cuticles. Planta 240: 891–897.
      Kirchhelle C, Hamant O. 2023. Discretizing the cellular bases of plant morphogenesis: emerging properties from subcellular and noisy patterning. Current Opinion in Cell Biology 81: 102159.
      Knoche M, Lang A. 2017. Ongoing growth challenges fruit‐skin integrity. Critical Reviews in Plant Sciences 36: 190–215.
      Kosma DK, Parsons EP, Isaacson T, Lü S, Rose JKC, Jenks MA. 2010. Fruit cuticle lipid composition during development in tomato ripening mutants. Physiologia Plantarum 139: 107–117.
      Krauss P, Markstädter C, Riederer M. 1997. Attenuation of UV radiation by plant cuticles from woody species. Plant, Cell & Environment 20: 1079–1085.
      Lai X, Khanal BP, Knoche M. 2016. Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. Planta 244: 1145–1156.
      Lara I, Belge B, Goulao LF. 2014. The fruit cuticle as a modulator of postharvest quality. Postharvest Biology and Technology 87: 103–112.
      Lara I, Heredia A, Domínguez E. 2019. Shelf life potential and the fruit cuticle: the unexpected player. Frontiers in Plant Science 10: 770.
      Lashbrooke J, Aharoni A, Costa F. 2015. Genome investigation suggests MdSHN3, an APETALA2‐domain transcription factor gene, to be a positive regulator of apple fruit. Journal of Experimental Botany 66: 6579–6589.
      López‐Casado G, Matas AJ, Domínguez E, Cuartero J, Heredia A. 2007. Biomechanics of isolated tomato (Solanum lycopersicum L.) fruit cuticles: the role of cutin matrix. Journal of Experimental Botany 58: 3875–3883.
      Luque P, Gavara R, Heredia A. 1995. A study of the hydration process of isolated cuticular membranes. New Phytologist 129: 283–288.
      Matas AJ, López‐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.
      Meder F, Mondini A, Visentin F, Zini G, Crepaldi M, Mazzolai B. 2022. Multisource energy conversion in plants with soft epicuticular coatings. Energy and Environmental Science 15: 2545.
      Meder F, Must I, Sadeghi A, Mondini A, Filippeschi C, Beccai L, Mattoli V, Pingue P, Mazzolai B. 2018. Energy conversion at the cuticle of living plants. Advanced Functional Materials 28: 1806689.
      Nawrath C, Schreiber L, Franke RB, Geldner N, Reina‐Pinto JJ, Kunst L. 2013. Apoplastic diffusion barriers in Arabidopsis. Arabidopsis Book 11: e0167.
      Parsons EP, Popopvsky S, Lohrey GT, Alkalai‐Tuvia S, Perzelan Y, Bosland P, Bebeli PJ, Paran I, Fallik E, Jenks MA. 2013. Fruit cuticle lipid composition and water loss in a diverse collection of pepper (Capsicum). Physiologia Plantarum 149: 160–174.
      Pfündel EE, Agati G, Cerovic ZG. 2006. Optical properties of plant surfaces. In: Riederer M, Müller C, eds. Annual plant reviews, biology of the plant cuticle. Oxford, UK: Blackwell, 216–249.
      Philippe G, Geneix N, Petit J, Guillon F, Sandt C, Rothan C, Lahaye M, Marion D, Bakan B. 2020. Assembly of tomato fruit cuticles: a cros‐talk between the cutin polyester and cell wall polysaccharides. New Phytologist 226: 809–822.
      Reina JJ, Domínguez E, Heredia A. 2001. Water sorption‐desorption in conifer cuticles: the role of lignin. Physiologia Plantarum 112: 372–378.
      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.
      Reynoud N, Geneix N, D'Orlando A, Petit J, Mathurin J, Deniset‐Besseau A, Marion D, Rothan C, Lahaye M, Bakan B. 2023. Cuticle architecture and mechanical properties: a functional relationship delineated through correlated multimodal imaging. New Phytologist 238: 2033–2046.
      Reynoud N, Geneix N, Petit J, D'Orlando A, Fanuel M, Marion D, Rothan C, Lahaye M, Bakan B. 2022. The cutin polymer matrix undergoes a fine architectural tuning from early tomato fruit development to ripening. Plant Physiology 190: 1821–1840.
      Riederer M. 2006. Thermodynamics of the water permeability of plant cuticles: characterization of the polar pathway. Journal of Experimental Botany 57: 2937–2942.
      Roth‐Nebelsick A, Hacke UG, Voigt D, Schreiber SG, Krause M. 2023. Foliar water uptake in Pinus species depends on needle age and stomatal wax structures. Annals of Botany 131: 287–300.
      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 as studied by AFM and solid‐state NMR. Biophysical Journal 79: 2761–2797.
      Schönherr J. 1976. Water permeability of isolated cuticular membranes: the effect of pH and cations on diffusion, hydrodynamic permeability and size of polar pores in the cutin matrix. Planta 128: 113–126.
      Schönherr J, Schmidt HW. 1979. Water conductance of plant cuticles – dependence of conductance coefficients of cuticular transpiration on vapor pressure saturation deficit. Planta 144: 391–400.
      Schreiber L. 2005. Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Annals of Botany 95: 1069–1073.
      Segado P, Domínguez E, Heredia A. 2016. Ultrastructure of the epidermal cell wall and cuticle of tomato fruit (Solanum lycopersicum L.) during development. Plant Physiology 170: 935–946.
      Seufert P, Staiger S, Arand K, Bueno A, Burghardt M, Riederer M. 2022. Building a barrier: the influence of different wax fractions on the water transpiration barrier of leaf cuticles. Frontiers in Plant Science 12: 766602.
      Solovchenko A, Merzlyak M. 2003. Optical properties and contribution of cuticle to UV protection in plants: experiments with apple fruit. Photochemical and Photobiological Sciences 2: 861–866.
      Staiger S, Seufert P, Arand K, Burghardt M, Popp C, Riederer M. 2019. The permeation barrier of plant cuticles: uptake of active ingredients is limited by very long‐chain aliphatic rather than cyclic wax compounds. Pest Management Science 75: 3405–3412.
      Steinmüller D, Tevini M. 1985. Action of ultraviolet radiation (UV‐B) upon cuticular waxes in some crop plants. Planta 164: 557–564.
      Takahashi Y, Tsubaki S, Sakamoto M, Watanabe S, Azuma JI. 2012. Growth‐dependent chemical and mechanical properties of cuticular membranes from leaves of Sonneratia alba. Plant, Cell & Environment 35: 1201–1210.
      Taneda H, Watanabe‐Taneda A, Chhetry R, Ikeda H. 2015. A theoretical approach to the relationship between wettability and surface microstructures of epidermal cells and structured cuticles of flower petals. Annals of Botany 115: 923–937.
      Tredenick EC, Farquhar GD. 2021. Dynamics of moisture diffusion and adsorption in plant cuticles including the role of cellulose. Nature Communications 12: 5042.
      Tredenick EC, Farrell TW, Forster WA, Psaltis STP. 2017. Nonlinear porous diffusion modeling of hydrophilic ionic agrochemicals in astomatous plant cuticle aqueous pores: a mechanistic approach. Frontiers in Plant Science 8: 746.
      Tsubaki S, Sugimura K, Teramoto Y, Yonemori K, Azuma J‐I. 2013. Cuticular membrane of Fuyu persimmon fruit is strengthened by triterpenoid nano‐fillers. PLoS ONE 8: e75275.
      Vega C, Valbuena‐Carabaña M, Gil L, Fernández V. 2021. Water sorption and desorption of isolated cuticles from three woody species with focus on Ilex aquifolium. Frontiers in Plant Science 12: 728627.
      Vignolini S, Gregory T, Kolle M, Lethbridge A, Moyroud E, Steiner U, Glover BJ, Vukusic P, Rudall PJ. 2016. Structural colour from helicoidal cell‐wall architecture in fruits of Margaritaria nobilis. Journal of the Royal Society Interface 13: 20160645.
      Xi X, Kim SH, Tittmann B. 2015. Atomic force microscopy based nanoindentation study of onion abaxial epidermis walls in aqueous environment. Journal of Applied Physics 117: 024703.
      Yeats TH, Buda GJ, Wang Z, Chehanovsky N, Moyle LC, Jetter R, Schaffer AA, Rose JKC. 2012. The fruit cuticles of wild tomato species exhibit architectural and chemical diversity, providing a new model for studying the evolution of cuticle function. The Plant Journal 69: 655–666.
      Zeisler‐Diehl V, Müller Y, Schreiber L. 2018. Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. Journal of Plant Physiology 227: 66–74.
      Zhang Y, Chen X, Du Z, Zhang W, Devkota AR, Chen Z, Chen C, Sun W, Chen M. 2020. A proposed method for simultaneous measurement of cuticular transpiration from different leaf surfaces in Camellia sinensis. Frontiers in Plant Science 11: 420.
    • Grant Information:
      PID2021-126604OB Ministerio de Ciencia e Innovación
    • Contributed Indexing:
      Keywords: biomechanics; biophysics; phenolics; plant cuticle; plant hydration; plant photoprotection; thermal properties; waxes
    • Publication Date:
      Date Created: 20240726 Date Completed: 20240916 Latest Revision: 20240916
    • Publication Date:
      20240917
    • Accession Number:
      10.1111/nph.20009
    • Accession Number:
      39061101