Transcriptional memory of the pioneer mangrove Avicennia marina to repeated submergence stress

While mangroves are naturally adapted to coastal environments, prolonged tidal flooding that exceeds their tolerance threshold adversely impacts their growth and physiological health. Unlike transient stressors, cyclic environmental fluctuations can prime plants into a sustained acclimated state, enabling a more robust response to the subsequent exposure. However, our knowledge of such “stress memory” in mangroves remains limited. In this study, we employed an integrative approach combining physiological assays with comparative transcriptome analysis on the pioneer mangrove species Avicennia marina, to explore the impacts of repeated submergence and its underlying molecular responses. Submergence substantially suppressed the expression of photosynthesis-related genes, including those involved in chlorophyll biosynthesis, light harvesting, and light reactions, while accelerating leaf senescence. Genes associated with ethylene and abscisic acid (ABA) signaling were up-regulated to similar levels across successive submergence events. In contrast, genes governing auxin signaling, shoot system development, and water deprivation response displayed amplified expression during re-submergence compared to the initial exposure, indicating the acquisition of “transcriptional memory”. The priming of candidate hub regulators, including PILS7, ARF, ERD14 and bZIP23, during initial flooding were suggested to underpin this stress memory in A. marina, allowing for an accelerated and more robust defense against recurring submergence. Furthermore, excessively frequent flooding may exert cumulative negative impacts on A. marina seedlings, owing to their incomplete recovery after submergence, which could compromise to their growth and viability. In summary, our findings unravel the mechanistic basis underlying mangrove’s adaptation to intensifying flooding regimes and offer insights that may help inform future conservation and restoration efforts.