Tomato leaf transcriptomic changes promoted by long-term water scarcity stress can be largely prevented by a fungal-based biostimulant

Water availability is by far the leading environmental factor limiting crop productivity worldwide. The use of cell-free microbial culture filtrates (CF) as biostimulant is gaining ground as a safe and ecologically sound approach to improving crop yields while reducing anthropogenic pressure. However, their action mechanisms remain unknown. Here we found that foliar application of Trichoderma harzianum CF enhanced fruit yield, root growth and photosynthesis in plants of a commercial tomato cultivar grown under long-term water deficit in Mediterranean greenhouse conditions. To investigate the biochemical and molecular mechanisms underlying this phenomenon, we adopted an integrative and systems biology approach to characterize plants grown under optimal and suboptimal irrigation conditions (OIC and SOIC, respectively) with or without the fungal CF treatment. Water shortage promoted changes in the levels of drought stress-related signalling molecules, and in the transcriptome of leaves that potentially accounted for the physiochemical differences recorded between OIC– and SOIC-grown plants. Notably, many of these changes were largely prevented by the foliar application of fungal CF to SOIC-grown plants, including the expression of ca. 50% of the expression of water scarcity-responsive genes. These genes did not respond to CF in OIC-grown plants, indicating that the transcriptomic response to CF is strongly determined by the water status of the plant. Taken together, the data provided evidence that foliar application of fungal CF improves yield and long-term water scarcity tolerance by preventing a large portion of the stress-induced transcriptional response, rendering plants “blind”, or less sensitive to water stress.