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

Background: The cells of growing plant organs secrete an extracellular fibrouscomposite (the primary wall) that allows the turgid protoplaststo expand irreversibly via wall-yielding events, which are regulatedby processes within the cytoplasm. The role of the epidermisin the control of stem elongation is described with specialreference to the outer epidermal wall (OEW), which forms a ‘tensileskin’. Novel Facts: The OEW is much thicker and less extensible than the walls ofthe inner tissues. Moreover, in the OEW the amount of celluloseper unit wall mass is considerably greater than in the innertissues. Ultrastructural studies have shown that the expandingOEW is composed of a highly ordered internal and a diffuse outerhalf, with helicoidally organized cellulose microfibrils inthe inner (load-bearing) region of this tension-stressed organwall. The structural and mechanical backbone of the wall consistsof helicoids, i.e. layers of parallel, inextensible cellulosemicrofibrils. These ‘plywood laminates’ containcrystalline ‘cables’ orientated in all directionswith 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 extracellularpolymers have also been found in certain bacteria, algae, fungiand animals. In the insect cuticle crystalline cutin nanofibrilsform characteristic ‘OEW-like’ herringbone patterns. Conclusions: Theoretical considerations, in vitro studies and computer simulationssuggest that extracellular biological helicoids form by directedself-assembly of the crystalline biopolymers. This spontaneousgeneration of complex design ‘without an intelligent designer’evolved independently in the protective ‘skin’ ofplants, animals and many other organisms.