Solid-State biology and seed longevity: A mechanical analysis of glasses in pea and soybean embryonic axes

Authors: BALLESTEROS, DANIEL - ROYAL BOTANICAL GARDENS; Walters, Christina

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/28/2019
Publication Date: 7/16/2019
Citation: Ballesteros, D., Walters, C.T. 2019. Solid-State biology and seed longevity: A mechanical analysis of glasses in pea and soybean embryonic axes. Frontiers in Plant Science. 10:920. https://doi.org/10.3389/fpls.2019.00920.
DOI: https://doi.org/10.3389/fpls.2019.00920

Interpretive Summary: In a genebank, some seeds can survive for hundreds of years and some might survive a decade or two. We wish to understand why and to predict how long a seed will survive during storage. Seeds survive in the freezer because they survive drying. Drying causes the cytoplasm within the seed cells to solidify. Therefore, we call upon the tools used to predict expiration dates in solids, such as plastics, dry foods and pharmaceuticals, to explain the slow changes that occur in seeds during storage. Here we explore a technique that uses dynamic mechanical analysis (DMA), which is common in a material sciences lab, but unusual for biology. DMA measures how much the solid deforms when pressure is applied and this tells us about the structure and mobility of molecules within the solid. We compared these properties in pea (long-lived) and soybean (short-lived) seeds and found that there is less molecular movement in pea compared to soybean seeds and that the solid is "strongest" when seeds are stored at the optimum water content. Our next step is to compare a wider range of seeds to see if DMA properties correlate with known longevities.

Technical Abstract: The cytoplasm of anhydrobiotes (organisms that persist in the absence of water) solidifies during drying. Despite this stabilization, anhydrobiotes vary in how long they persist while dry. In this paper, we call upon concepts currently used to explain stability of amorphous solids (also known as glasses) in synthetic polymers, foods and pharmaceuticals to the understand variation in longevity of biological systems. We use embryonic axes of pea (Pisum sativum) and soybean (Glycine max) seeds as test systems that have relatively long and short survival times, respectively, but similar geometries and water sorption behaviors. We used dynamic mechanical analysis to gain insights on structural and mobility properties that relate to stability of other organic systems with controlled composition. Measurements of elastic and loss moduli, and the dissipation function, tan d, were made in pea and soybean tissues containing less than 0.2 g H2O g-1 dry mass across broad temperature ranges. Discrete changes in mechanical properties were observed and indicated that multiple relaxations of structural constraints to molecular movement. The relaxations demonstrate that substantial localized, “fast” motion occurs within solidified cytoplasm of embryonic axes. Glasses in pea showed evidence of high constraint, while glasses in soybean exhibited more “fragile” properties. These analyses demonstrate that long-range diffusive motion of cytoplasmic molecules is largely restricted within dried seeds; however, short-range vibrational motion is feasible. Fragility and short range motions have been linked to physical aging in well-characterized polymers. The work shows high complexity of structure-regulated molecular mobility within dried seed matrices that is unexplored but likely contributes to variation in the nature and kinetics of reactions leading to viability decline in diverse seeds.