The growing outer epidermal wall: Design and physiological role of a composite structure

Background The cells of growing plant organs secrete an extracellular fibrous composite (the primary wall) that allows the turgid protoplasts to expand irreversibly via wall-yielding events, which are regulated by processes within the cytoplasm. The role of the epidermis in the control of stem elongation is described with special reference to the outer epidermal wall (OEW), which forms a 'tensile skin'. Novel Facts The OEW is much thicker and less extensible than the walls of the inner tissues. Moreover, in the OEW the amount of cellulose per unit wall mass is considerably greater than in the inner tissues. Ultrastructural studies have shown that the expanding OEW is composed of a highly ordered internal and a diffuse outer half, with helicoidally organized cellulose microfibrils in the inner (load-bearing) region of this tension-stressed organ wall. The structural and mechanical backbone of the wall consists of helicoids, i.e. layers of parallel, inextensible cellulose microfibrils. These 'plywood laminates' contain crystalline 'cables' orientated in all directions with respect to the axis of elongation (isotropic material). Cessation of cell elongation is accompanied by a loss of order, i.e. the OEW is a dynamic structure. Helicoidally arranged extracellular polymers have also been found in certain bacteria, algae, fungi and animals. In the insect cuticle crystalline cutin nanofibrils form characteristic 'OEW-like' herringbone patterns. Conclusions Theoretical considerations, in vitro studies and computer simulations suggest that extracellular biological helicoids form by directed self-assembly of the crystalline biopolymers. This spontaneous generation of complex design 'without an intelligent designer' evolved independently in the protective 'skin' of plants, animals and many other organisms.