Elemental localisation and a reduced glutathione redox state protect seeds of the halophyte Suaeda maritima from salinity during over-wintering and germination

Saltmarshes are increasingly at risk from sea level rise through climate change. Their vegetation is comprised of halophytes, salt-tolerant plants, that naturally regenerate from seed, yet the combination of functional traits associated with salinity tolerance in seeds is still poorly characterised. Combining approaches in scanning electron microscopy, energy-dispersive spectrometry, biochemistry and physiology, we focussed on elucidating two mechanisms that are commonly utilised by adult halophyte plants: (1) ion accumulation and elemental localisation, and (2) enhanced antioxidant capacity to protect against oxidative stress, in seeds of the saltmarsh halophyte Suaeda maritima during over-wintering and germination. Freshly collected seeds were dormant, and required 19 weeks of submergence in artificial sea water (ASW) at 5 °C, mimicking over-wintering in the field, to release dormancy. Fresh and pre-treated seeds had an abundance of Na+ and Cl−, as well as the reactive oxygen species H2O2 and glutathione disulphide (i.e., oxidised glutathione). This was accompanied by a large pool of reduced glutathione and the low molecular weight thiols cysteine, cysteinyl-glycine and γ-glutamyl-cysteinyl, suggesting a potentiated antioxidant system in preparation for germination. During germination in ASW, the glutathione and thiol redox state was highly reduced, with no consistent production of H2O2. Na and Cl localised in the seed testa and tegmen, while Mg and K were concentrated in the embryo, and Ca and S had a broad distribution across the seed. Small differences in seed moisture content, measured to indicate the extent of osmotic adjustment, did not account for a higher maximum threshold to germination of 2.22 times the concentration of ASW compared to 1.76 times ASW-equivalents for iso-osmotic solutions of polyethylene glycol (PEG). Moreover, the halotime constant (θHalo) was higher (i.e., slower germination) in the presence of ASW than PEG, suggesting that slower germination may give more time to initiate tolerance mechanisms in response to salinity that promote germination. Seeds of S. maritima appear to utilise seawater ions to their benefit during germination in salinity, using elemental localisation to protect the embryo from potential toxicity of Na and Cl, while maintaining a highly reduced cellular redox state.