Topological Interlocking and Geometric Stiffening as Complementary Strategies for Strong Plant Shells

Abstract

Many organisms encapsulate their embryos in hard, protective shells. While birds and reptiles largely rely on mineralized shells, plants often develop highly robust lignocellulosic shells. Despite the abundance of hard plant shells, particularly nutshells, it remains unclear which fundamental properties drive their mechanical stability. This multiscale analysis of six prominent (nut)shells (pine, pistachio, walnut, pecan, hazelnut, and macadamia) reveals geometric and structural strengthening mechanisms on the cellular and macroscopic length scales. The strongest tissues, found in walnut and pistachio, exploit the topological interlocking of 3D‐puzzle cells and thereby outperform the fiber‐reinforced structure of macadamia under tensile and compressive loading. On the macroscopic scale, strengthening occurs via an increased shell thickness, spherical shape, small size, and a lack of extended sutures. These functional interrelations suggest that simple geometric modifications are a powerful and resource‐efficient strategy for plants to enhance the fracture resistance of entire shells and their tissues. Understanding the interplay between structure, geometry, and mechanics in hard plant shells provides new perspectives on the evolutionary diversification of hard seed coats, as well as insights for nutshell‐based material applications.

Cellulosic wall thickenings restrict cell expansion to shape the 3D puzzle sclereids of the walnut shell

“…As shown in seeds of Portulaca oleracea, the wavy sutural interface between neighboring cells of the seed coat increase overall strength and fracture toughness compared to straight cell interfaces (Gao et al 2018). In the same way the interlocking of the polylobate sclereid cells in walnut lead to high values in tensile and compression tests on the tissue level (Antreich et al 2019, Huss et al 2020). On the cellular level, cells kept their LES low during development to reduce high stresses on the cell wall analogue to epidermal cells in A. thaliana (Sapala et al 2018).…”

“…A closer look into the shell reveals polylobate sclereid cells tightly interlocked in 3D with their neighbours, which leads to a higher contact area between cells and superior mechanical properties compared to tissues with isodiametric cells like in pine seed coats (Antreich et al 2019). Furthermore, the irregularly shaped cells are also found in shells of pecan and pistachio (Huss et al 2020). The morphogenesis of such shell tissues is controlled by physical forces as well as biochemical signalling (Landrein & Ingram, 2019).…”

Functional packaging of seeds

“…Another way is the development of undulating cell walls that also interlock neighbouring cells (as in walnuts and pistachios). This may additionally prevent global failure once the middle lamella ruptures (Huss et al ., 2020). The middle lamella connects adjacent cell walls and is initially pectin rich, but it then starts to lignify as secondary wall formation progresses (Donaldson, 2001; Xiao et al ., 2020).…”

“…Shell geometry is particularly important to resist shell cracking by granivores via compression loading, for example. Owing to a higher rigidity, small spherical shells are more advantageous than elongated shells of similar size and thickness (Huss et al ., 2020). For intact (avian) gut passage, geometry seems to be irrelevant, as long as the encapsulated seeds are small enough for ingestion.…”

“…In terms of cell types, a surprisingly uniform arrangement of isodiametric brachysclereids can be found in the seed coat of the Korean pine ( Pinus koraiensis ; Antreich et al ., 2019). In comparison with hard coats in angiosperms, this tissue appears less differentiated (Table 1); yet, in terms of strength, it can compete with some angiosperm shells (Huss et al ., 2020). Generally, it seems that thick shells rarely consist of a single cell type – most static shells show various cell types, often arranged in layers.…”