Molecular Mechanisms of the 1-Aminocyclopropane-1-Carboxylic Acid (ACC) Deaminase Producing Trichoderma asperellum MAP1 in Enhancing Wheat Tolerance to Waterlogging Stress

Abstract

Waterlogging stress (WS) induces ethylene (ET) and polyamine (spermine, putrescine, and spermidine) production in plants, but their reprogramming is a decisive element for determining the fate of the plant upon waterlogging-induced stress. WS can be challenged by exploring symbiotic microbes that improve the plant’s ability to grow better and resist WS. The present study deals with identification and application of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-producing fungal endophyte Trichoderma asperellum (strain MAP1), isolated from the roots of Canna indica L., on wheat growth under WS. MAP1 positively affected wheat growth by secreting phytohormones/secondary metabolites, strengthening the plant’s antioxidant system and influencing the physiology through polyamine production and modulating gene expression. MAP1 inoculation promoted yield in comparison to non-endophyte inoculated waterlogged seedlings. Exogenously applied ethephon (ET synthesis inducer) and 1-aminocyclopropane carboxylic acid (ACC; ET precursor) showed a reduction in growth, compared to MAP1-inoculated waterlogged seedlings, while amino-oxyacetic acid (AOA; ET inhibitor) application reversed the negative effect imposed by ET and ACC, upon waterlogging treatment. A significant reduction in plant growth rate, chlorophyll content, and stomatal conductance was noticed, while H2O2, MDA production, and electrolyte leakage were increased in non-inoculated waterlogged seedlings. Moreover, in comparison to non-inoculated waterlogged wheat seedlings, MAP1-inoculated waterlogged wheat exhibited antioxidant–enzyme activities. In agreement with the physiological results, genes associated with the free polyamine (PA) biosynthesis were highly induced and PA content was abundant in MAP1-inoculated seedlings. Furthermore, ET biosynthesis/signaling gene expression was reduced upon MAP1 inoculation under WS. Briefly, MAP1 mitigated the adverse effect of WS in wheat, by reprogramming the PAs and ET biosynthesis, which leads to optimal stomatal conductance, increased photosynthesis, and membrane stability as well as reduced ET-induced leaf senescence.

Phytohormone Production Profiles in Trichoderma Species and Their Relationship to Wheat Plant Responses to Water Stress

“…These results are also a consequence of working with strains from genetically very distant species, given the great diversity that exists within the Trichoderma genus [ 50 ]. Trichoderma ACCD has also been described as a mechanism in enhancing wheat tolerance to salt stress [ 35 ] and waterlogging [ 37 ]. Our study has included the application of Trichoderma to wheat plants to analyze the effect on growth and tolerance to water stress.…”

“…Trichoderma strains have the capacity to produce ACCD. This is the case of T. longibrachiatum TL-6, involved in promoting wheat growth and enhancing plant tolerance to salt stress [ 35 ], and T. asperelloides (formerly T. asperellum ) T203 that by being able to regulate the endogenous ACC levels stimulates root elongation of cucumber [ 36 ] and T. asperellum MAP1, which enhanced wheat plant tolerance to waterlogging stress [ 37 ].…”

“…ROS are key players in the complex signaling network of plant responses to drought stress, so it is essential to maintain ROS at non-toxic levels in a delicate balancing act between ROS production, involving ROS generating enzymes and the unavoidable production of ROS during basic cellular metabolism, and ROS-scavenging pathways [ 39 ]. The application of Trichoderma to wheat triggers systemic defense pathways [ 40 ] and seems to be a good choice to minimize damage caused by abiotic stresses [ 35 , 37 ], also limiting environmental pollution. There is sufficient evidence to consider that Trichoderma association can help plants in sustaining drought stress by increasing: (i) the expression of antioxidative enzymes that alleviate the damage caused by the accumulation of ROS and modulating the balance of plant’s phytohormones [ 25 , 41 ]; (ii) the absorption surface that leads the plant to improve water-use efficiency [ 33 ]; and (iii) the synthesis of phytohormones and phytohormonal analogues to promote plant performance.…”

Biostimulants for the Regulation of Reactive Oxygen Species Metabolism in Plants under Abiotic Stress

“…Wheat plants waterlogged for 5 d were inoculated with T. asperellum (strain MAP1), a fungal endophyte which was isolated from the roots of Canna indica L., which resulted in diminishing WL stress-induced MDA, H 2 O 2 and EL contents and regulating antioxidant system [166]. The ability of MAP1 inoculation to produce IAA, Pro, total phenols, flavonoid, and having the potential to scavenge free radicals helped it to facilitate plants with tolerance against WL stress.…”

Evaluation of Indigenous Olive Biocontrol Rhizobacteria as Protectants against Drought and Salt Stress

“…In addition to plant's defense mechanisms, the use of beneficial microorganisms can help to enhance or trigger these responses thereby reducing the negative effects caused by stress [85,86]. Related to this, the activity of the enzyme ACD, synthetized by some PGPR, has been shown to play an important role in increasing plants' tolerance to adverse circumstances [87].…”