Pretreatment with Trichoderma harzianum alleviates waterlogging-induced growth alterations in tomato seedlings by modulating physiological, biochemical, and molecular mechanisms

•Waterlogging (WL) inhibited plant growth and oxidative stress.•Trichoderma harzianum (TH) improved plant physiology and metabolism under WL.•TH maintains plant nutrient status and improves the content of photosynthetic pigments under WL.•TH upregulates antioxidant defense system and decreases oxidative stress under WL.•TH upregulates gene expression related to sugar and alcohol metabolism as well as aquaporin. We studied the role of Trichoderma harzianum (TH) in improving the physiological, biochemical, hormonal, and molecular parameters of tomato seedlings grown under waterlogging (WL, for 14 and 28 days). Pretreatment with TH significantly improved the growth of tomato by enhancing the chlorophyll synthesis and uptake of essential ions, including nitrogen, phosphorus, and potassium. A reduction in anthocyanin content was also ameliorated significantly by TH pretreatment. TH significantly mitigated the WL-induced decline in height and in fresh and dry biomass accumulation. Accumulation of proline, flavonoids, anthocyanin, sugars, and soluble protein increased with TH pretreatment. At both growth periods (14 and 28 days after treatment [DAT]), the accumulation of secondary metabolites, including total phenols and flavonoids, and the redox components (tocopherols) were increased significantly by TH pretreatment. Increased synthesis of metabolites maintained the antioxidant status of tomato, resulting in amelioration of WL-induced oxidative effects on membranes. WL and TH treatments significantly increased ethylene production and decreased abscisic acid content at both growth periods. The accumulation of reactive oxygen species, like hydrogen peroxide, in TH treated seedlings was correlated with the upregulation of the Fe-SOD gene. WL stress triggered the activity of sucrose synthase (SUS), lactate dehydrogenase (LDH), and pyruvate decarboxylase (PDC), which reached a maximum at 14 DAT, and TH pretreatment resulted in further enhancement above control and WL-stressed levels. Quantitative RT-PCR revealed differential expression of genes, where Fe-SOD and ADH were upregulated due to TH treatment and ARE, ACO, ERF, and aquaporin were downregulated relative to control plants. Pretreatment of tomato seedlings with TH improved tolerance to WL by maintaining the antioxidant status, sugar metabolism, and expression of critical genes. These results suggest that TH pretreatment is an effective way to improve WL tolerance in tomato at vegetative stage.