Evidence for a Leaf-to-Fruit Signal Regulating the Antioxidant System in Tomato Fruits Under Stress: Involvement of ABA, Ascorbate Redox State, H2 O2 and NO

Abstract

Ramzi Murshed, Sanders Junglee, Huguette Sallanon, Laurent Urban and Felicie Lauri

In plants, environmental stresses trigger reactive oxygen species (ROS) overproduction, causing oxidative damage but also generating systemic signals that prime defense responses in distal organs. How such signals are transmitted from leaves to fruits is a key question for crop stress tolerance and quality. Here, tomato plants were subjected to mercury chloride (5 ppm HgCl2 ) for 24 hours to induce a selective arrest of water flux and to evaluate oxidative parameters and antioxidant defense in leaves, fruit peduncles and fruits. Mercury treatment induced oxidative damage — evidenced by increased H2O2 and MDA accumulation — in leaves and fruit peduncles, while fruits remained unaffected. Nevertheless, antioxidant enzyme activities (SOD, CAT, APX, DHAR and MDHAR) and transcript levels of SlAPXcyto, SlAPXt, SlDHAR1, SlDHAR2 and SlMDHAR were upregulated in fruits, despite the absence of local oxidative stress, suggesting a systemic leaf-to-fruit signal priming antioxidant defenses. To test this hypothesis, detached tomato fruits were treated with four putative stress signals: abscisic acid (ABA), exogenous H2 O2 , nitric oxide (NO, via sodium nitroprusside, SNP) and varying ascorbate (AsA) redox states. Oxidative parameters (H2 O2 and MDA), ascorbate levels, and antioxidant enzyme activities and transcript levels were monitored at 4, 8 and 24 h after treatment. The results indicate that ABA, AsA redox state, H2 O2 and NO each modulate antioxidant enzyme activities and gene expression in tomato fruits. Notably, while ABA, H2 O2 and AsA redox state generally induced antioxidant enzyme activities, NO acted primarily as a direct ROS scavenger, suppressing enzymatic induction, an effect reversed by the NO scavenger cPTIO. Frequent dissociation between activity and transcript levels indicates post-transcriptional regulation. These findings support a model in which ABA, H2 O2 act as interconnected systemic signals co-ordinating antioxidant defense in fruits under leaf stress.

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