PthAW1, a Transcription Activator-Like Effector of Xanthomonas citri subsp. citri, Promotes Host-Specific Immune...

Citrus canker disease caused by Xanthomonas citri subsp. citri is one of the most destructive diseases in citrus. X. citri subsp. citri pathotypes display different host ranges. X. citri subsp. citri strain A (Xcc^A) causes canker disease in most commercial citrus varieties, whereas strain AW (Xcc^AW), which is genetically similar to Xcc^A, infects only lime and alemow. Understanding the mechanism that determines the host range of pathogens is critical to investigating and utilizing host resistance. We hypothesized that Xcc^AW would undergo mutations in genes that restrict its host range when artificially inoculated into incompatible citrus varieties. To test this hypothesis, we used an experimental evolution approach to identify phenotypic traits and genetic loci associated with the adaptation of Xcc^AW to incompatible sweet orange. Repeated inoculation and reisolation cycles improved the ability of three independent Xcc^AW strains to colonize sweet orange. Adapted Xcc^AW strains displayed increased expression of type III secretion system and effector genes. Genome sequencing analysis indicated that two of the adapted strains harbored mutations in pthAW1, a transcription activator-like effector (TALE) gene, that corresponded to the removal of one or two repeats from the central DNA-binding repeat region. Introduction of the original but not the adapted pthAW1 variants into Xcc^A abolished its ability to cause canker symptoms in sweet orange, Meyer lemon, and clementine but not in other Xcc^AW-resistant citrus varieties. The original pthAW1, when expressed in Xcc^A, induced ion leakage and the expression of pathogenesis-related genes but had no effect on CsLOB1 expression in sweet orange. Our study has identified a novel host-specific avirulence TALE and demonstrated active adaptive rearrangements of the TALE repeat array during host adaptation.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.