Dark septate endophyte Periconia macrospinosa enhances wheat seedling growth and mitigates Fusarium crown rot by reprogramming the host's immune responses

Abstract

Fusarium crown rot (FCR) in wheat, caused by Fusarium graminearum , is among the world's major fusarium diseases. This study aimed to assess the potential of the dark septate endophyte Periconia macrospinosa PmVS01 in promoting wheat seedlings growth and inducing resistance against F. graminearum Fg1 under greenhouse conditions, as well as its ability to inhibit pathogen growth under axenic culture. The results demonstrated that P. macrospinosa PmSV01 enhances key plant ecophysiological traits, including photosynthetic activity (18 %), nitrogen nutritional status (18 %), and the accumulation of defensive flavonol compounds (22 %), which collectively result in average increase of 10 %–30 % in both root and shoot growth and biomass. These stimulating effects correlate with its symbiotic nature, as it colonizes the rhizodermis and peripheral parenchyma regions of the roots without causing morbid symptoms. It also significantly protects seedlings against FCR disease. Transcriptomic analyses by q PCR indicate that this protective effect is associated with its ability to enhance host immunity and to reprogram multiple metabolic processes involved in plant defense, including pathways related to oxidative and water stress responses, as well as jasmonic acid and salicylic acid signaling. In addition, confrontation assays revealed an antagonistic activity of P. macrospinosa PmSV01 against F. graminearum Fg1 through the production of diffusible and volatile compounds, leading to an inhibition rate of the pathogen's mycelia growth that ranges from 28 % to 85 %. This is the first report of the beneficial effect of P. macrospinosa PmSV01 on wheat and resistance to FCR, and provides new alternatives for exploiting the potential of DSEs as plant growth-promoting fungi and biocontrol agents for sustainable crop production. • The fungus Periconia macrospinosa exhibited potential plant growth promoting properties. • This beneficial fungal species penetrated in the wheat roots as an endophyte. • Application of P. macrospinosa decreased progress of crown rot disease caused by Fusarium graminearum in wheat seedlings. • The endophytic P. macrospinosa reprograms defense genes actively hijacked by F. graminearum , restoring plant resistance. • Cytotoxic secondary metabolites secreted by P. macrospinosa affected the growth of F. graminearum.