Secondary Metabolites Produced by the Epiphytic Actinobacteria of Wild Desert Plants: Growth Promoting and Pathogen Suppressing Potential of Streptomyces microflavus in Wheat Growing Under Water-Deficit Conditions

Drought is the most critical environmental stress factor for agriculture in the Arabian Peninsula. In this study, 54 epiphytic actinobacterial strains were isolated from the rhizosphere of three indigenous desert plants: Haloxylon persicum, Artemisia monosperma, and Calligonum comosum. While all isolates showed plant-growth promoting activities, one isolate identified molecularly as Streptomyces microflavus (RNCCA42) of C. comosum exhibited the highest activity, producing IAA (156 μg mL⁻¹), GA (8 μg mL⁻¹), ACC (76 μM mg⁻¹ h⁻¹), ABA (127 μg mL⁻¹), siderophores (85%), NH₃ (20 μmol mL⁻¹), and solubilized PO₄ (495 μg mL⁻¹) as well as the highest antagonistic activity against five fungal and three bacterial pathogens common in wheat. S. microflavus was studied for its activities under a decreasing water potential series of five values from normal (−0.0 MPa) to extreme drought conditions (−1.0 MPa) using the polyethylene glycol (PEG)-induced drought stress technique. The production of phytochemicals, mono- and polysaccharides, free amino acids, and hydrolytic enzymes, as well as antioxidant activities increased significantly (ANOVA, p < 0.05) with increasing water deficiency. These parameters increased in general two to fourfold from normal to extreme drought conditions. The highest increase was observed for the proline concentration, from 2.4 to 20 μg mg_dw⁻¹. A greenhouse experiment was carried out to study the effect of S. microflavus inoculation on six wheat cultivars in extreme drought conditions. Compared to normal watering conditions, drought stress decreased most morphological and biochemical properties. It also increased the root length and the concentration of soluble sugars and proline in grains compared to normal conditions. Compared to stress conditions, S. microflavus inoculation significantly enhanced all variables, including germination, number and weight of seeds, root and shoot weights, soluble sugars, carotenoids, proteins, and proline, as described by the principal component analysis (PCA). The seeds of the inoculated cultivar Rafha weighed three times more, and the seeds of the cultivar Najed weighed 1.5 times more compared to the non-inoculated seeds. The grain chemical quality variables (soluble sugars, protein, proline, and carotenoids) were significantly higher in inoculated seeds than in non-inoculated seeds. The greatest difference in the protein content was observed for the cultivar Najed, of which inoculation increased the protein content by 10%. PCA analysis showed that the Najed cultivar properties increased most of the six wheat cultivars due to the inoculation with S. microflavus. Thus, the epiphytic S. microflavus RNCCA42 can be developed to be used as an effective bioinoculant in sustainable agriculture in dry regions.