A Benzimidazole Proton Pump Inhibitor Increases Growth and Tolerance to Salt Stress in Tomato

Abstract

Pre-treatment of tomato plants with micromolar concentrations of omeprazole (OP), a benzimidazole proton pump inhibitor in mammalian systems, improves plant growth in terms of fresh weight of shoot and roots by 49 and 55% and dry weight by 54 and 105% under salt stress conditions (200 mM NaCl), respectively. Assessment of gas exchange, ion distribution, and gene expression profile in different organs strongly indicates that OP interferes with key components of the stress adaptation machinery, including hormonal control of root development (improving length and branching), protection of the photosynthetic system (improving quantum yield of photosystem II) and regulation of ion homeostasis (improving the K+:Na+ ratio in leaves and roots). To our knowledge OP is one of the few known molecules that at micromolar concentrations manifests a dual function as growth enhancer and salt stress protectant. Therefore, OP can be used as new inducer of stress tolerance to better understand molecular and physiological stress adaptation paths in plants and to design new products to improve crop performance under suboptimal growth conditions.Highlight: Omeprazole enhances growth of tomato and increases tolerance to salinity stress through alterations of gene expression and ion uptake and transport.

Omeprazole treatment elicits contrasting responses to salt stress in two basil genotypes

“…Strikingly, GEN plants accumulated 2.5‐fold more nitrate when treated with OP under unstressed conditions, while no significant difference was found under salt stress (Figure e). Similar results have been previously reported on tomato plants treated with OP (Rouphael et al, ; Van Oosten et al, ). On the contrary, no significant changes were observed in unstressed conditions in NAP plants, while the nitrate accumulation was reduced 65% by OP treatment under salt stress (Figure e).…”

“…NAP appears to be more sensitive due to less efficient mechanisms involved in salt stress adaptation. Based on previous results (Van Oosten et al, ), we hypothesized that OP treatment would increase the salt tolerance in basil by augmenting salt stress adaptation mechanisms present in both basil genotypes. Interestingly, while OP treatment increased growth, only the salt sensitive genotype, NAP, responded positively to OP treatment under salt stress.…”

“…It has also been demonstrated that successful tolerance mechanisms in plants may rely on a reduced perception of the stress environment and lack of activation of alarm reactions that trigger many stress‐related responses, including reduced growth (Barbieri et al, ; Jakab et al, ; Mancarella et al, ; Orsini et al, ; Yang & Guo, ) Based on these findings, it seems critical to understand how growth and stress adaptation are functionally connected. We have recently demonstrated that feeding OP via root systems enhances plant growth (in the absence of salinity or drought stress) but also improves both salinity (Rouphael et al, ; Van Oosten et al, ) and drought (unpublished) stress tolerance. Considering that we observed these responses under micromolar treatments, we attributed to this molecule a signalling and/or hormonal action that could be of interest in exploring the relationship between plant growth and stress adaptation (Savvides, Ali, Tester, & Fotopoulos, ).…”

“…Ion measurements were performed according to a procedure described by Van Oosten et al (). Plant material was dried and pulverised using a cutting‐grinded head (IKA, MF10.1, Staufen, Germany).…”

“…While the target of OP is well understood in animals its role in plants is largely unknown. It has been shown that in tomato OP enhances growth and tolerance to salt stress (Rouphael et al, ; Van Oosten et al, ). The mechanism of action is the subject of scrutiny and will provide a valuable point of control for modifying growth and osmotic tolerance in plants.…”