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Free keywords:
dark septate endophytes; effectors; lifestyle transition; root–fungus symbioses
Abstract:
Fungal accessory chromosomes (ACs), if not all, contribute to virulence in plants. However, mechanisms by which the 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 a poplar-associated fungus Stagonosporopsis rhizophilae. We identified an ∼0.6 Mb horizontally acquired AC in 16W that resulted in a mildly parasitic lifestyle in plants. The complete deletion of the AC (Δ16W) significantly altered the phenotypes. 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-seq analysis showed that AC loss induced upregulation of genes related to biosynthesis of indole acetic acid and melanin, and root colonization. We further 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 using comparable experiments of Triticum- and Arabidopsis–fungus associations. Furthermore, the three isolates generated symbiotic interactions with the 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 AC. We speculate that the AC-situated effectors and other potential secreted molecules may have evolved to specifically target the vascular plants and promote mild virulence.
