Yunxia Liu, Yutong Long, Yazhuo Li, Xin Zhao, Fanlong Wang, Zhibing Luo, Yongjun Zhang
The entomopathogenic fungus Beauveria bassiana endophytically colonizes a diverse array of plants including the model, Nicotiana benthamiana stimulating photosynthesis and growth. During this interaction, sulfate transporter genes are upregulated in both organisms. However, the mechanisms mediating this potential mutualistic sulfate exchange remain elusive. Here, we demonstrate that the three activated fungal sulfate transporters synergistically facilitated sulfate utilization and promoted fungal colonization of the plant. Among these, the high-affinity sulfate transporter BbSulTR1 plays a primary role. Disruption of any single fungal sulfate transporter genes decreased B. bassiana plant colonization, consequently decreasing plant sulfur accumulation and growth promotion. Similarly, single interference of the three activated plant sulfate transporter genes severely attenuated plant sulfate acquisition and biomass, subsequently restricting fungal colonization. Mechanistically, the endophytic fungus actively acquires sulfate from the host to enhance its own organic sulfur synthesis. This depletion of host sulfate and organic sulfur pools triggers the plant's low-sulfur response, upregulating host sulfate transporters to accelerate external sulfate uptake. Notably, loss of BbSulTR1 significantly abolished these reciprocal dynamics. Our findings reveal that fungal sulfate acquisition is critical for fungal endophytic colonization, and that the mutualistic interaction integrates a feedback mechanism which stimulates host sulfur assimilation pathways ultimately contributing to plant growth. This study elucidates a novel nutritional coordination mechanism underpinning fungal plant endophytism.