Tal2c Activates the Expression of OsF3H04g to Promote Infection as a Redundant TALE of Tal2b in Xanthomonas oryzae pv. oryzicola

Xanthomonas oryzae delivers transcription activator-like effectors (TALEs) into plant cells to facilitate infection. Following economic principles, the redundant TALEs are rarely identified in Xanthomonas. Previously, we identified the Tal2b, which activates the expression of the rice 2-oxoglutarate-dependent dioxygenase gene OsF3H(03g) to promote infection in the highly virulent strain of X. oryzae pv. oryzicola HGA4. Here, we reveal that another clustered TALE, Tal2c, also functioned as a virulence factor to target rice OsF3H(04g), a homologue of OsF3H(03g). Transferring Tal2c into RS105 induced expression of OsF3H(04g) to coincide with increased susceptibility in rice. Overexpressing OsF3H(04g) caused higher susceptibility and less salicylic acid (SA) production compared to wild-type plants. Moreover, CRISPR-Cas9 system-mediated editing of the effector-binding element in the promoters of OsF3H(03g) or OsF3H(04g) was found to specifically enhance resistance to Tal2b- or Tal2c-transferring strains, but had no effect on resistance to either RS105 or HGA4. Furthermore, transcriptome analysis revealed that several reported SA-related and defense-related genes commonly altered expression in OsF3H(04g) overexpression line compared with those identified in OsF3H(03g) overexpression line. Overall, our results reveal a functional redundancy mechanism of pathogenic virulence in Xoc in which tandem Tal2b and Tal2c specifically target homologues of host genes to interfere with rice immunity by reducing SA.

Automated summary

The study revealed that the pathogenic virulence mechanism of Xanthomonas oryzae pv. oryzicola involves Tal2b and Tal2c targeting homologues of host genes to interfere with rice immunity by reducing salicylic acid production. Overexpression of OsF3H(04g) caused higher susceptibility in rice, while CRISPR-Cas9 system-mediated editing of effector-binding elements enhanced resistance to specific strains. Transcriptome analysis showed altered expression of several defense-related genes in OsF3H(04g) overexpression line.