Fracture of the dimorphic fruits ofAethionema arabicum(Brassicaceae)

Abstract

Fruits exhibit highly diversified morphology, and are arguably one of the most highly specialised organs to have evolved in higher plants. Fruits range in morphological, biomechanical, and textural properties, often as adaptations for their respective dispersal strategy. While most plant species possess monomorphic (of a single type) fruit and seeds, here we focus on Aethionema arabicum (L.) Andrz. ex DC. (Brassicaceae). Its production of two distinct fruit (dehiscent and indehiscent) and seed types on the same individual plant provides a unique model system with which to study structural and functional aspects of dimorphism. Using comparative analyses of fruit fracture biomechanics, fracture surface morphology, and internal fruit anatomy, we reveal that the dimorphic fruits of A. arabicum exhibit clear material, morpho-anatomical, and adaptive properties underlying their fracture behaviour. A separation layer along the valve-replum boundary is present in dehiscent fruit, whereas indehiscent fruit have numerous fibres with spiral thickening, linking their winged valves at the adaxial surface. Our study evaluates the biomechanics underlying fruit-opening mechanisms in a heteromorphic plant species. Elucidating dimorphic traits aids our understanding of adaptive biomechanical morphologies that function as a bet-hedging strategy in the context of seed and fruit dispersal within spatially and temporally stochastic environments.Résumé : Les fruit présentent une morphologie hautement diversifiée et ils constituent probablement un des organes les plus hautement spécialisés ayant évolué chez les plantes supérieures. Les fruit varient en ce qui concerne leurs propriétés morphologiques, biomécaniques et texturales, souvent comme adaptations de leurs stratégies respectives de dispersion. Alors que la plupart des espèces de plantes possèdent des fruit et graines monomorphes (d'un type unique), les auteurs se concentrent ici sur Aethionema arabicum (L.) Andrz. ex DC. (Brassicaceae). Sa production de deux types distincts de fruit (déhiscent et indéhiscent) et de graines chez le même individu fournit un système modèle unique sur lequel étudier les aspects structuraux et fonctionnels du dimorphisme. À l'aide d'analyses comparatives de la biomécanique de la fracture du fruit, de la morphologie à la surface de la fracture et de l'anatomie interne du fruit, les auteurs révèlent que les fruit dimorphes d'A. arabicum présentent des propriétés matérielles, morpho-anatomiques et adaptatives claires qui sous-tendent le fonctionnement de la fracture. Une couche de séparation le long de la frontière valve-replum est présente chez les fruit déhiscents, alors que les fruit indéhiscents possèdent de nombreuses fibres avec un épaississement hélicoïdal, liant leurs valves ailées à la surface adaxiale. Cette étude évalue la biomécanique qui sous-tend les mécanismes d'ouverture du fruit chez les espèces végétales hétéromorphes. L'élucidation des traits dimorphes contribue à notre compréhension des morphologies biomécaniques adaptatives qui fonct...

A tale of two morphs: developmental patterns and mechanisms of seed coat differentiation in the dimorphic diaspore model Aethionema arabicum (Brassicaceae)

“…Seed myxospermy is an advanced trait with an origin that may extend back to the Eocene, a geologic epoch with climatic variability and vegetation adaptation to long-term warming also evident from fossil fruits and seeds (Collinson et al, 2012;Smith et al, 2009b). SRXTM imaging of fossil (Friis et al, 2019;Friis et al, 2014;Manchester and Collinson, 2019;Smith et al, 2009b) and modern (this work and Arshad et al, 2020;Benedict et al, 2016;Smith et al, 2009b) flowers, seeds and fruits revealed internal structures that may have evolved as adaptations to climatic change and variable environments Linkies et al, 2010;Walck et al, 2011).…”

“…To explore the internal anatomy underlying the morph‐specific phenotypic changes, we performed comparative SRXTM during the time‐course of DEH and IND reproductive development. SRXTM is non‐destructive and has been used successfully to reveal cryptic features and internal structures of modern and fossil flowers, fruits and seeds (Arshad et al , 2020; Friis et al , 2014; Smith et al , 2009a). Reconstructed digital sections of Ae.…”

“…Projections were post-processed and reconstructed using a Fourier-based algorithm (Marone and Stampanoni, 2012). Tomographic slice data derived from the scans were analysed using AV-IZO TM 9.5.0 (Thermo Scientific TM ; Visualization Science Group Inc., Burlington, MA, USA) for Windows 10 Pro 64-bit, and contrast adjusted in Adobe Photoshop Lightroom CC as described (Arshad et al, 2020). Details of whole seed staining and microscopical analysis of seed coat differentiation are described in Supporting Information.…”

Genome Improvement and Genetic Map Construction for Aethionema arabicum, the First Divergent Branch in the Brassicaceae Family

“…Finally, quantitative trait loci (QTL) mapping for the wide range of traits in Aethionema ( e.g. , flowering time, chemical defenses (Hofberger et al 2013; Mohammadin et al 2018), fruit heteromorphism (Lenser et al 2016; Wilhelmsson et al 2019; Arshad et al 2019) and light-control of germination (Mérai et al 2019) will be greatly enabled by the genetic map and improved genome assembly.…”

Plant biomechanics — an interdisciplinary lens on plant biology

“…One of the important functions of such motion is the release, and sometimes violent expulsion, of seed from fruit. Arshad et al (2019) investigated the mechanical behavior of the dimorphic fruits of Aethionema arabicum with the intention to characterize the opening mechanism. One of the two types of fruit present on the same plant is dehiscent, the other indehiscent, offering an excellent opportunity to decipher the adaptive biomechanical morphologies that function as a bet-hedging strategy in the context of seed and fruit dispersal.…”