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 mecha-nisms by which ACs determine specific traits associated with lifestyle transitions along a symbiotic contin-uum 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(D16W)significantly altered the fungal phenotype.Specifically,D16W 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-situ-ated effectors and other potential secreted molecules may have evolved to specifically target vascular plants and promote mild virulence.