Hormonal and transcriptomic reprogramming underlie responses to recurrent drought in the halophyte Atriplex halimus L.

Abstract

This study provides the first integrative assessment of drought stress memory in a halophyte, highlighting the role of recurrent drought in shaping physiological and molecular responses in plants adapted to unpredictable and stressful environments. Here, we investigated the physiological, biochemical and transcriptomic responses of the xerohalophyte Atriplex halimus L. exposed to one, two or three consecutive drought cycles (D1-D3). Each cycle consisted of severe water deficit (<5% field capacity) followed by a rehydration phase, evaluating water relations, gas exchange, phytohormone profiles, enzymatic activity and gene expression. D1 induced leaf osmotic stress (osmotic potential dropping to -3 MPa) and reduced photosynthetic performance, primarily associated with elevated abscisic acid (ABA) levels (2.3-fold increase), but without evidence of physiological damage. In contrast, plants subjected to repeated drought cycles (D2 and D3) exhibited more negative water potential (<-2 MPa), accompanied by increased jasmonic acid (JA) and salicylic acid (SA) levels (increasing by ∼2- and ∼1.2-fold, respectively), while photosynthetic rates remained suppressed. D3 was characterized by transcriptomic signatures consistent with metabolic downregulation and resource conservation. Across successive drought events, changes in hormonal signaling and gene expression revealed a dynamic adjustment to drought recurrence. Thus, the results suggest a progressive transition from an initial stress response (D1) to a primed state (D2) and finally to a conservative state (D3), suggesting that A. halimus adjusts its resource allocation and stress-response mechanisms to balance stress tolerance with resource economy, a strategy crucial for its survival and ecological success under increasingly severe climate constraints.