Multi-Omics Insights into Arbuscular Mycorrhizal Fungus-Mediated Enhancement of Sunflower Resistance to Salinity, Drought and Orobanche Stresses

Sunflower (Helianthus annuus L.) production is increasingly challenged by multiple environmental stresses, including salinity, drought, and parasitic plants such as Orobanche cumana. Arbuscular mycorrhizal fungi (AMF) are widely recognized as beneficial microorganisms that enhance plant stress tolerance. However, the molecular mechanisms underlying AMF-mediated adaptation to multiple stresses remain largely unclear. In this study, we investigated the effects of AMF inoculation on sunflower resistance to salinity, drought, and O. cumana parasitism through physiological, transcriptomic, metabolomic, and integrated multi-omics analyses. AMF inoculation promoted lateral root development in different sunflower varieties and induced physiological priming responses, characterized by enhanced antioxidant activity and improved regulation of reactive oxygen species homeostasis and osmotic balance under stress conditions. Transcriptomic analysis revealed a conserved AMF-responsive gene module across different stress environments, which was mainly associated with phenylpropanoid metabolism, cell wall organization, redox regulation, and lipid-related pathways. Metabolomic profiling further demonstrated that AMF extensively reshaped root metabolic networks, particularly affecting organic acids, amino acid derivatives, phenolic compounds, flavonoids, alkaloids, and lipid-associated metabolites. Integrated transcriptomic–metabolomic analysis identified key gene–metabolite associations involved in carbon metabolism, nutrient transport, hormone signaling, and membrane remodeling, providing potential molecular targets underlying AMF-mediated stress adaptation. Overall, this study reveals how AMF enhances sunflower resilience against biotic and abiotic stresses through coordinated physiological, transcriptional, and metabolic regulation. These findings highlight the potential application of AMF as a sustainable biological strategy for improving crop stress resistance and quality-related metabolic traits.