Background and Aims Stomatal morphology and function have remained largely conserved throughout ∼400 million years of plant evolution. However, plant cell wall composition has evolved and changed. Here stomatal cell wall composition was investigated in different vascular plant groups in attempt to understand their possible effect on stomatal function. Methods A renewed look at stomatal cell walls was attempted utilizing digitalized polar microscopy, confocal microscopy, histology and a numerical finite-elements simulation. The six species of vascular plants chosen for this study cover a broad structural, ecophysiological and evolutionary spectrum: ferns (Asplenium nidus and Platycerium bifurcatum) and angiosperms (Arabidopsis thaliana and Commelina erecta) with kidney-shaped stomata, and grasses (angiosperms, family Poaceae) with dumbbell-shaped stomata (Sorghum bicolor and Triticum aestivum). Key Results Three distinct patterns of cellulose crystallinity in stomatal cell walls were observed: Type I (kidney-shaped stomata, ferns), Type II (kidney-shaped stomata, angiosperms) and Type III (dumbbell-shaped stomata, grasses). The different stomatal cell wall attributes investigated (cellulose crystallinity, pectins, lignin, phenolics) exhibited taxon-specific patterns, with reciprocal substitution of structural elements in the end-walls of kidney-shaped stomata. According to a numerical bio-mechanical model, the end walls of kidney-shaped stomata develop the highest stresses during opening. Conclusions The data presented demonstrate for the first time the existence of distinct spatial patterns of varying cellulose crystallinity in guard cell walls. It is also highly intriguing that in angiosperms crystalline cellulose appears to have replaced lignin that occurs in the stomatal end-walls of ferns serving a similar wall strengthening function. Such taxon-specific spatial patterns of cell wall components could imply different biomechanical functions, which in turn could be a consequence of differences in environmental selection along the course of plant evolution.

In the absence of minerals as stiffening agents, insects and spiders often use metal‐ion cross‐linking of protein matrices in their fully organic load‐bearing “tools.” In this comparative study, the hierarchical fiber architecture, elemental distribution, and the micromechanical properties of the manganese‐ and calcium‐rich cuticle of the claws of the spider Cupiennius salei, and the Zn‐rich cuticle of the cheliceral fangs of the same animal are analyzed. By correlating experimental results to finite element analysis, functional microstructural and compositional adaptations are inferred leading to remarkable damage resilience and abrasion tolerance, respectively. The results further reveal that the incorporation of both zinc and manganese/calcium correlates well with increased biomaterial's stiffness and hardness. However, the abrasion‐resistance of the claw material cross‐linked by incorporation of Mn/Ca‐ions surpasses that of many other non‐mineralized biological counterparts and is comparable to that of the fang with more than triple Zn content. These biomaterial‐adaptation paradigms for enhanced wear‐resistance may serve as novel design principles for advanced, high‐performance, functional surfaces, and graded materials.

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