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Between protection and defence: the plant cuticle

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JOYARD Jacques, Honorary CNRS Research Director, Laboratory of Cellular & Plant Physiology, Grenoble Alpes University.

About 450 million years ago, in the middle of the Paleozoic, the first plants to colonize the Earth had to face a set of challenges related to this a priori hostile environment. In moving from an aquatic to a terrestrial lifestyle, plants have had to cope with the risks of desiccation, extreme temperatures, gravity, increased exposure to UV radiation, etc. They have introduced new morphological and physiological characteristics that allowed them to live in this new environment. For example, the development of complex cell walls for biomechanical support and structural protection of cells characterizes modern terrestrial plants.

However, the most critical adaptive trait for the survival of these organisms out of water is certainly the ability to avoid desiccation, i.e. to retain water inside cells and tissues. Therefore, the ability to form and maintain a hydrophobic surface layer, or cuticle, on the surfaces of airborne organs is probably one of the most important innovations in the history of terrestrial plant evolution. This idea is confirmed by fossil evidence and the omnipresence of cuticles among all existing terrestrial plants, from mosses to flowering plants [1].

Figure 1. Leaf surface area observed with a Scanning Microscope. A, Image of the upper surface of a winged tobacco leaf (Nicotiana alata) showing trichomes and some stomata; Photo Louisa Howard (Dartmouth electron microscope facility)[Public domain], via Wikimedia Commons; B, Image of the lower surface of a leaf of Arabidopsis thaliana showing trichomes and some stomata; Photo Louisa Howard & M.L. Guerinot (Dartmouth electron microscope facility) [Public domain], via Wikimedia Commons. C, Image of a stomata of a Haemanthus albiflos leaf; Photo Judyta Dulnik (Own work) [CC BY-SA 4.0], via Wikimedia Commons. D, Image of a stomata and epicuticular waxes on the surface of a Rose leaf; Photo Plantsurfer [Public domain], via Wikimedia Common. E, Diagram representing a part of the cuticle of a leaf covering an epidermal cell (zone without stomata or trichome). To get an idea of the scale, the part of the cuticle shown in the diagram corresponds approximately to the areas identified on the images by white rectangles (length 20mm).

Observed by the scanning electron microscope (Figure 1A-D), the outer surface of the sheets is more or less smooth. It often has small ovoid structures, called stomata. They allow the gaseous exchanges between the plant and the atmosphere essential for photosynthesis and respiration. Hairs of varying appearance (or trichomes) emerge largely from the surface. Trichomes are structures that adapt to environmental conditions and contain terpenes, phenolic compounds, alkaloids or other repellent substances that play an important role in the plant’s defence reactions against insects or other predators.

The more or less smooth surface covering the leaf is in fact the outer part of the plant cuticle. It is an extracellular hydrophobic layer that covers the aerial epidermis of all terrestrial plants. The cuticle (Figure 1E) is divided into two areas based on its chemical composition:

at the base, covering the epidermal cells, a domain called the cuticular layer. Composed of cutin, it is rich in polysaccharides.
above, the cutin [2] itself, enriched with waxes [3] (which are hydrophobic, i.e. repel water). The waxes deposited inside the cutin matrix are called intracuticular waxes. On the surface, the cutin is covered with a film and epicuticular wax crystals that give the leaf a more or less brilliant appearance.

Thanks to its hydrophobic properties, the cuticle offers the leaf protection against desiccation and external environmental stresses. Armed with protective skin and a range of adaptation strategies for water acquisition and conservation, terrestrial plants have developed in many drying environments.

Figure 2. Water drops on the surface of an alchemilla leaf. [Source: Photo © Jacques Joyard]

Many leaves have a particular characteristic: water tends to behave like drops on the surface of their leaves (Figure 2), cleaning the surface of particles and debris. It’s superhydrophobia. The effectiveness of this self-cleaning mechanism, called the “lotus effect“, which varies according to species, has been correlated with the abundance of epicuticular wax crystals [4]. This observation is at the origin of the development of effective biomimetic technical materials [5], such as paints or self-cleaning glass.

While the cuticle provides a very effective barrier against UV-B rays that alter cellular structures (DNA in particular), it largely allows the active wavelengths for photosynthesis to pass through. However, epicuticular wax crystals promote the reflection of light by the leaf surface: shiny surfaces reflect light more than others.

Finally, the plant cuticle presents a physical barrier to pathogens (e.g. fungi), at least against those that do not enter the leaf via stomata or wounds. Some pathogens can hydrolyze the cutin polymer into monomers which then act as elicitors of plant defense responses. Epicuticular waxes also play an important role in the pathogenicity of certain fungi or in plant insect interactions [1].

Videos on the Lotus effect:

References and notes

[1] Yeats T.H. & Rose J.K.C. (2013) The Formation and Function of Plant Cuticles. Plant Physiol. 163, 5-20.

[2] The last decade has seen considerable progress in understanding the biosynthetic pathways (and the genes encoding the enzymes responsible for them) of the two major components of the cuticle, cutin and cuticular waxes.

[3] Insoluble in water, waxes are soluble in organic solvents. They are lipids.

[4] Barthlott W. & Neinhuis C. (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202, 1-8.

[5] Bhushan B. (2012) Bioinspired structured surfaces. Langmuir 28, 1698-1714.