Plants have two types of reproduction: sexual, resulting in embryo production, and asexual, resulting in vegetative bodies commonly derived from stems and roots (e.g., bulb, tuber). Dead organs enclosing embryos (DOEEs, such as seed coat and pericarp) are emerging as central components of the dispersal unit acting to nurture the embryo and ensure its survival in the habitat. Here we wanted to investigate the properties of dead organs enclosing plant asexual reproductive bodies, focusing on the garlic (Allium sativum) bulb. We investigated the biochemical and biological properties of the outer peel enclosing the bulb and the inner peel enclosing the clove using various methodologies, including bioassays, proteomics, and metabolomics. The garlic peels differentially affected germination and post-germination growth, with the outer peel demonstrating a strong negative effect on seed germination of Sinapis alba and on post-germination growth of Brassica juncea. Proteome analysis showed that dead garlic peels possess 67 proteins, including chitinases and proteases, which retained their enzymatic activity. Among primary metabolites identified in garlic peels, the outer peel accumulated multiple sugars, including rhamnose, mannitol, sorbitol, and trehalose, as well as the modified amino acid 5-hydroxylysine, known as a major component of collagen, at a higher level compared to the clove and the inner peel. Growth of Escherichia coli and Staphylococcus aureus was promoted by garlic peel extracts but inhibited by clove extract. All extracts strongly inhibited spore germination of Fusarium oxysporum f.sp. melonis. Thus, the garlic peels not only provide physical protection to vegetative offspring but also appear to function as a refined arsenal of proteins and metabolites for enhancing growth and development, combating potential pathogens, and conferring tolerance to abiotic stresses.

Dead organs enclosing embryos, such as seed coats and pericarps, are emerging as important maternally-derived components of the dispersal unit that affect seed performance and fate. In the face of climate change and increased incidents of heatwaves, we sought to investigate the effect of salinity (S), short episodes of high temperature (HS), and combination of S + HS (SHS), at the reproductive phase, on the properties of dead pericarps of Brassica juncea. Proteome and metabolome analyses revealed multiple proteins and metabolites stored in dead pericarps whose levels and composition were altered under single and combined stress conditions. The protein profile of SHS showed a higher correlation with salt than with HS indicating the dominant effect of salt over heat stress. On the other hand, the analysis of metabolites showed that the profile of SHS has better correlation with HS than with salt. The integration of metabolic and proteomic data showed that changes in TCA cycle intermediates and certain amino acids (e.g., proline) under salt treatments (S and SHS) are highly correlated with changes in proteins involved in their biosynthetic pathways. Thus, accumulation of proteins and metabolites in dead pericarps is differently affected by single and combination of salt and heat stresses. Salinity appears to dominate plant response to combined stresses at the protein level, while heat appears to be the major factor affecting metabolite accumulation in dead pericarps.

In the face of climate change and the predicted increase in the frequency and severity of abiotic stresses (e.g., hot spell, salinity), we sought to investigate the effect of salinity (S), short episodes of high temperature (HS) and combination of salinity and high temperature (SHS), at the reproductive phase, on yield with a special focus on the properties of dead pericarps of Brassica juncea. Three interval exposures to HS resulted in massive seed abortion, and seeds from salt-treated plants germinated poorly. Germination rate and final germination of B. juncea seeds were slightly reduced in the presence of salt and SHS pericarp extracts. All pericarp extracts completely inhibited seed germination of tomato and Arabidopsis, but removal of pericarp extracts almost fully restored seed germination. Heat and salinity profoundly affected the accumulation of phytohormones in dead pericarps. Combined stresses highly reduced IAA and ABA levels compared with salt, and enhanced the accumulation of GA1, but abolished the positive effect of salt on the accumulation of GA4, JA and SA. Interestingly, pericarp extracts displayed priming activity and significantly affected seedling performance in a manner dependent on the species and on the origin of the pericarp. While control pericarps improved and reduced the seedlings’ performance of autologous and heterologous species, respectively, pericarps from salt-treated plants were harmless or improved heterologous seedling performance. Thus, the strategy employed by the germinating seed for securing resources is set up, at least partly, by the mother plant in conjunction with the maternal environment whose components are stored in the dead maternal organs enclosing the embryo.