Trichoderma Combined with 1-Aminocyclopropane-1-carboxylic acid (ACC) Soil Amendments Modulates the Root Microbiome and Improves Wheat Growth Under Salinity Stress

• Halotolerant Trichoderma isolate and ACC soil amendments orchestrate and shape the root microbiome. • Trichoderma and ACC soil amendments counteract salinity stress in wheat plants by modifying sodium (Na + ) homeostasis and decreasing ionic, osmotic, and oxidative stress. • Compared with the stress control, the application of T. viride Th4 and ACC individually and in combination substantially decreased root sodium (Na + ) accumulation by 21.5%, 27%, and 19.5%, respectively. • The application of T. viride Th4 and ACC individually and in combination substantially decreased shoot Na + accumulation by 31.6%, 9.9%, and 23.4%, respectively, compared with the stress control. • Despite these benefits, the synergetic impacts of T. viride Th4 and ACC amendment on the proliferation of beneficial root microbes and the improvement of salinity tolerance in plants remain to be elucidated. Salinity stress in agricultural soils impairs plant defense responses and imposes multiple effects, including ionic imbalance, osmotic and oxidative stress. Consequently, devising and customizing more effective solutions for mitigating salinity stress in crops are vital. The microbial enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, which cleaves the ethylene precursor, ACC, is presumed to decrease stress-induced senescence and promote plant growth. In this study, halotolerant Trichoderma viride Th4 was isolated from salt cedar ( Tamarix chinensis Lour.) rhizosphere soils and mass-cultured for use as a seed inoculant. ACC soil amendment is thought to promote the proliferation of root-associated microorganisms with ACC deaminase activity. A glasshouse experiment was conducted to determine the effects of T. viride Th4 and ACC, when applied individually or in combination, on the root microbiome communities and physio-biochemical attributes of wheat plants grown in pots containing nonsaline or saline soil. Control (CK) and stress-CK reference pots were also prepared. The highest fungal richness was observed in the roots of plants treated with T. viride Th4, in both nonsaline and saline soils, whereas the highest fungal diversity was observed in the T. viride Th4, ACC, and their coapplication treatments in saline soil. Moreover, ACC soil amendment consistently increased bacterial richness and diversity in the root endosphere, whereas T. viride Th4, ACC, and their coapplication decreased the richness and diversity of the rhizosphere microbiome in saline soil. Individual ACC soil amendment or coapplication with T. viride Th4 increased the abundance of the genus Rhodanobacter and reduced that of the genus Ochrobactrum in the root endosphere of the stressed plants. Saline soil significantly increased sodium (Na + ) accumulation in wheat roots and shoots. However, T. viride Th4, ACC, and their coapplication reduced the Na + content in the roots by 21.5%, 27%, and 9.5%, respectively, and in the shoots by 31.7%, 9.9%, and 23.44%, respectively, compared with the stress CK treatment. Salinity stress also decreased the leaf chlorophyll a content, but T. viride Th4 application or coapplication with ACC increased it by approximately 6.6% and 11.3%, respectively. Furthermore, salinized wheat treated with T. viride Th4 alone or in combination with ACC presented increased activities of superoxide dismutase (SOD; 27.23% and 14.23%, respectively), catalase (CAT; 161.85% and 151.28%, respectively), ascorbate peroxidase (APX; 64.15% and 128.74%, respectively), and guaiacol peroxidase (GPX; 57.61% and 12.38%, respectively) compared with those in the stress CK treatment. Compared with the stress CK treatment, the ACC treatment slightly reduced SOD activity (5.29%) but increased CAT (78.86% and GPX (58.57%) activity. The findings of the present study suggest that T. viride Th4 application alone or in combination with ACC results in increased antioxidant activity and counteracts detrimental effects, thus improving wheat growth. Additionally, our results provide insights into a promising way to leverage plant-beneficial soil microbes to reinforce salinity tolerance in wheat tissues, although the multifaceted synergies between Trichoderma and ACC and their broad-scale applications need to be more fully elucidated.