Loss of the accessory chromosome converts a pathogenic tree-root fungus into a mutualistic endophyte

Some fungal accessory chromosomes (ACs) may contribute to virulence in plants. However, the mechanisms by which ACs determine specific traits associated with lifestyle transitions along a symbiotic continuum are not clear. Here we delineated the genetic divergence in two sympatric but considerably variable isolates (16B and 16W) of the poplar-associated fungus Stagonosporopsis rhizophilae. We identified a ∼0.6-Mb horizontally acquired AC in 16W that resulted in a mildly parasitic lifestyle in plants. Complete deletion of the AC (Δ16W) significantly altered the fungal phenotype. Specifically, Δ16W was morphologically more similar to 16B, showed enhanced melanization, and established beneficial interactions with poplar plants, thereby acting as a dark septate endophyte. RNA sequencing (RNA-seq) analysis showed that AC loss induced the upregulation of genes related to root colonization and biosynthesis of indole acetic acid and melanin. We observed that the AC maintained a more open status of chromatin across the genome, indicating an impressive remodeling of cis-regulatory elements upon AC loss, which potentially enhanced symbiotic effectiveness. We demonstrated that the symbiotic capacities were non-host-specific through comparable experiments on Triticum- and Arabidopsis-fungus associations. Furthermore, the three isolates generated symbiotic interactions with a nonvascular liverwort. In summary, our study suggests that the AC is a suppressor of symbiosis and provides insights into the underlying mechanisms of mutualism with vascular plants in the absence of traits encoded by the AC. We speculate that AC-situated effectors and other potential secreted molecules may have evolved to specifically target vascular plants and promote mild virulence.