Acetic acid enhances tolerance to long-term water deficit in tomato by partially buffering transcriptomic and proteomic reprogramming independently of canonical jasmonate signalling

Abstract

Acetic acid (AA), a volatile compound present in diverse microbial-derived biostimulants, enhances drought tolerance in plants. In Arabidopsis, soil-applied AA action has been linked to histone H4 acetylation and activation of jasmonate (JA) signalling. However, the mechanisms underlying AA action in crops of agronomic interest remain poorly understood. Here, we used an integrative approach to evaluate the effects of soil-applied AA on fruit yield, physiological performance, and leaf transcriptomic and proteomic profiles of tomato plants grown under optimal and suboptimal irrigation conditions (OIC and SOIC, respectively). While AA had little effect under OIC, it significantly enhanced fruit yield and photosynthesis under SOIC. Long-term water deficit triggered extensive transcriptomic and proteomic reprogramming, particularly affecting photosynthesis, RNA processing, protein biosynthesis-, modification- and homeostasis-related processes. Under SOIC, AA induced marked molecular changes that were not consistent with activation of canonical JA signaling pathways. Notably, only [~] 10% of the drought- or AA-responsive proteins were associated with corresponding transcript changes, highlighting a predominant role of regulatory layers beyond the transcriptional control to both long-term water deficit- and AA-induced protein remodeling. Strikingly, AA attenuated 47% and 35% of the transcriptomic and proteomic alterations induced by long-term water deficit, respectively. In addition, AA altered the abundance of numerous proteins that do not respond to drought, particularly ribosomal proteins and proteins involved in RNA processing. Collectively, our findings indicate that AA enhances tolerance to prolonged water deficit in tomato through mechanisms largely independent of canonical JA signaling and involving extensive downstream regulatory processes that partially mitigate stress-induced molecular reprogramming.