The SeABI5 transcription factor couples ABA signaling with flavonoid antioxidant production to confer cadmium tolerance in Salicornia europaea

Understanding the extraordinary stress tolerance mechanisms of extremophile plants represented by Salicornia europaea is crucial for isolating genetic tools to improve crop resilience. However, the detailed mechanisms of S. europaea to cadmium (Cd) remain poorly understood. Here, combining transcriptomic and metabolomic profiling, we deciphered the adaptive response of S. europaea to Cd stress. Cd stress triggered extensive metabolic and transcriptional reprogramming, with 237 metabolites and 1677 genes upregulated, among which flavonoid biosynthetic genes (SeCHS and SeF3H) and their corresponding flavonoid products were most prominently induced in S. europaea root under Cd stress. Especially, the contents of antioxidant flavonoids kaempferol and quercetin increased 2.3- and 3.8-fold accumulation in S. europaea root under Cd stress. Exogenous application of these compounds confirmed their protective role against Cd-induced oxidative damage via reducing malondialdehyde (MDA) levels by 28.1-37.4%, highlighting the flavonoid pathway as a central adaptive strategy. Through targeted molecular screening, we identified and validated the bZIP transcription factor SeABI5 as a master regulator of this metabolic response. Meanwhile, an ABA-mediated signal activates SeABI5, which then directly binds to the promoters of SeCHS and SeF3H containing three ABRE cis-elements to increase flavonoid production under Cd stress. The essential nature of this regulatory module was confirmed in Arabidopsis, where the ABI5 knock-out mutant exhibited a 34.8% reduction in root elongation and 49.5% decrease in plant height under Cd stress, as well completely lost the capacity for both ABA induced flavonoid biosynthesis and Cd tolerance. Conversely, AtABI5 overexpression enhanced Cd tolerance by promoting flavonoid accumulation and reducing Cd induced oxyradical contents. Collectively, our findings establish SeABI5 as a high-value genetic resource that directly couples stress perception with antioxidant production, offering a precise molecular target for breeding crops with enhanced tolerance to heavy metal stress.