Dry architecture - towards the understanding of the variation of longevity in desiccation-tolerant germplasm

Authors: BALLESTEROS, DANIEL - Royal Botanic Gardens, Kew; PRITCHARD, HUGH - Royal Botanic Gardens, Kew; Walters, Christina

Submitted to: Seed Science Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/23/2020
Publication Date: 6/1/2020
Citation: Ballesteros, D., Pritchard, H., Walters, C.T. 2020. Dry architecture - towards the understanding of the variation of longevity in desiccation-tolerant germplasm. Seed Science Research. 30(2):142-155. https://doi.org/10.1017/S0960258520000239.
DOI: https://doi.org/10.1017/S0960258520000239

Interpretive Summary: Conventional freezer storage is used to preserve germplasm that naturally survives drying. However, the effectiveness of preservation - meaning how long germplasm survives in storage - can vary from weeks to centuries, and no one knows why. Our work in this paper seeks to understand how drying affects organization of organelles within plant cells, specifically chloroplasts and lipid bodies, and how this might, in turn, affect the kinetics of reactions that cause germplasm to age and eventually die. We show that reactions involving free radicals, which are believed to cause aging reactions, can be promoted in intact chloroplasts because they allow continued production of high energy intermediate metabolites (the source of free radicals). Moreover, free radicals have greater mobility at low temperatures that allow lipids to crystallize because of the gaps that form in the solid aqueous matrix. Therefore, both chemical composition and structure of dried cytoplasm have important roles in affecting stability and ultimately longevity of stored germplasm.

Technical Abstract: Desiccation tolerant (DT) plant germplasm (i.e., seeds, pollen and spores) survive drying to low moisture contents, when cytoplasm solidifies, forming a glass, and chemical reactions are slowed. DT germplasm may survive for long periods in this state, though inter-specific and intra-specific variation occurs and is not currently explained. Such variability has consequences for agriculture, forestry and biodiversity conservation. Longevity was previously considered in the context of morphological features, cellular constituents or habitat characteristics. We suggest, however, that a biophysical perspective, which considers the molecular organization - or structure - within dried cytoplasm, can provide a more integrated understanding of the fundamental mechanisms that control ageing rates, hence the variation of longevity among species and cell types. Based on biochemical composition and physical-chemical properties of dried materials, we explore three types of interplay between structural conformations of dried cytoplasm and ageing: 1) cells that lack chlorophyll and contain few storage lipids may exhibit long shelf life, with ageing probably occurring through slow autoxidative processes within the glassy matrix as it relaxes; 2) cells with active chlorophyll may die quickly, possibly because they are prone to oxidative stress promoted by the photosynthetic pigments in the absence of metabolic water; and 3) cells that lack chloroplasts but contain high storage lipids may die quickly during storage at -20°C, possibly because lipids crystallize and destabilize the glassy matrix. Understanding the complex variation in structural conformation in space and time may help to design strategies that increase longevity in germplasm with generally poor shelf life.