Functional packaging of seeds

Abstract

The encapsulation of seeds in hard coats and fruit walls (pericarp layers) fulfils protective and dispersal functions in many plant families. In angiosperms, packaging structures possess a remarkable range of different morphologies and functionalities, as illustrated by thermo and hygro-responsive seed pods and appendages, as well as mechanically strong and water-impermeable shells. Key to these different functionalities are characteristic structural arrangements and chemical modifications of the underlying sclerenchymatous tissues. Although many ecological aspects of hard seed encapsulation have been well documented, a detailed understanding of the relationship between tissue structure and function only recently started to emerge, especially in the context of environmentally driven fruit opening and seed dispersal (responsive encapsulations) and the outstanding durability of some seed coats and indehiscent fruits (static encapsulations). In this review, we focus on the tissue properties of these two systems, with particular consideration of water interactions, mechanical resistance, and force generation. Common principles, as well as unique adaptations, are discussed in different plant species. Understanding how plants integrate a broad range of functions and properties for seed protection during storage and dispersal plays a central role for seed conservation, population dynamics, and plant-based material developments.

Keywords: diaspore adaptations; hard plant shells; physical dormancy; sclerenchyma; seed storage and protection; serotiny; tissue mechanics.

Fig. 1

Schematic overview of the functional aspects of seed encapsulation in angiosperms. (a) Generalized, sclerenchymatous shell with common chemical and structural properties of seed coats (testa), fruit walls (pericarp), and caryopses (testa and pericarp fused). As part of the sclerenchymatous tissue, a predetermined breaking point (water gaps or sutures) and a number of multifunctional compounds (aromatic and aliphatic) are often found. In some species, the hard shell is covered by a fleshy layer (e.g. mesocarp) or has a fleshy appendage (e.g. aril). If surface structures (trichomes, mucilage, or waxes) are present, they typically regulate water interactions. Depending on the structure of sclerenchyma, encapsulations may be static or responsive. (b) Static and (c) responsive encapsulation with different states: (1) maturity, characterized by on‐plant storage of the encapsulated seed(s); (2) diaspore release from the mother plant, which involves detachment in static and opening in responsive encapsulations; (3) after dispersal, corresponding to soil storage; and (4) germination, which requires imbibition and radicle penetration through the covering layers. In seeds with physical dormancy and in serotinous fruits, stages 4 and 2, respectively, are delayed and require specific environmental cues to be ‘unlocked’ (clock and lock symbols in (b) and (c)).

Fig. 2

Static encapsulations and their tissue anatomy in selected species. (a) The fruit capsule (lignified endocarp) of the trample‐burr Ibicella lutea is entirely fibrous, containing longitudinal (L) fibre bundles in a matrix of transversely (T) oriented fibres (cross‐section inspired by Horbens et al. (2014); microscopy image kindly provided by Christoph Neinhuis/Institut für Botanik, TU Dresden, Germany). (b) Diverse sclereids without a preferred orientation (and vasculature) form the endocarp shell of the coconut Cocos nucifera (computed tomography (CT) and microscopy images adapted from Schmier et al. (2020a); CC‐BY 4.0). (c) The hard pericarp of the Persian walnut Juglans regia (cv Geisenheim120) consists of a single cell type, characterized by interlocked three‐dimensional puzzle‐shaped sclereids with thinner cell walls in the inner shell part (CT and microscopy images adapted from Antreich et al. (2019) and Xiao et al. (2020); both CC‐BY 4.0). (d) Strong differences in the testa of the pea Pisum sativum explain physical dormancy (PY) in wild peas (P. sativum subsp. elatius JI64) when compared with domesticated ones (cv Cameor). Notably, cuticular modifications, a thicker macrosclereid/palisade layer (indicated by arrow), and a higher content of proanthocyanidins in this layer contribute to PY. Osteosclereids form a thin inner shell layer that is well visible in the dormant wild‐type due to the surrounding greenish compounds (images adapted from Smýkal et al. (2014); CC‐BY 4.0). Scale bars apply to both images always. Stainings: (a, c) fuchsin–chrysoidin–astrablue; (d) toluidine blue; (b) none.

Fig. 3

Responsive encapsulations and their tissue anatomy in selected species. (a) In the mesocarp of banksia (Banksia serrata) follicles, forces are generated by a network of branched fibre bundles surrounded by a matrix of condensed tannins (microscopy images kindly provided by Friedrich Reppe, MPI of Colloids and Interfaces). The bundles are lignified (fuchsin–chrysoidin–astrablue (FCA) staining) and, as illustrated schematically, tensile stresses are generated by drying and shrinkage of the hemicelluloses in the secondary cell wall, which are surrounding cellulose microfibrils that form a large angle (microfibril angle (MFA) γ = 75–90°) with the longitudinal fibre axis. This shrinkage results in shortening of fibres upon drying (Huss et al., 2018). (b) Force generation in awns of the storksbill Erodium gruinum occurs in a similar manner, but fibres (with a large MFA and a tilted helix) are arranged parallel to each other instead of in bundles, and drying kinetics are modulated by a lignin (ferulic acid) gradient. Polarization microscopy image adapted by permission from RightsLink: John Wiley and Sons New Phytologist (Abraham & Elbaum, 2013) © 2013, and autofluorescence images from RightsLink: Springer Nature Cellulose (Abraham et al., 2018) © 2018. (c) Seed pods of the iceplant Delosperma nakurense open when wetted with liquid water due to the swelling pressure of cellulosic keel cells (microscopy images adapted by permission from RightsLink: Springer Nature Nature Communications (Harrington et al., 2011) © 2011). Tissue is stained with FCA, showing nonlignified cell walls that are able to absorb large amounts of water and thereby exert swelling pressure.

Fig. 4

Mechanical reinforcement by septa and ingrowths in uni‐ and multilocular fruits (schematic cross‐sections). The Persian walnut Juglans regia and the eastern black walnut Juglans nigra each develop one locule with one seed (yellow), partially separated by a lignified central septum. The septum is much thicker in J. nigra, which significantly reinforces the shell from within by increasing the cross‐sectional area for load bearing. A similar effect is achieved by the local shell ingrowths (dark brown) in the lignified, multilocular fruits of the Borneo giant fan palm Borassodendron borneense (developing three locules separated by septa; marked by dashed lines. Drawing inspired by Bellot et al. (2020). Lignified septa and local shell ingrowths can be found in many species of the walnut family (Juglandaceae) and the palm family (Arecaceae).