Tal6b/AvrXa27A, a hidden TALE targeting the susceptibility gene OsSWEET11aand the resistance gene Xa27in rice

Xanthomonas oryzaepv. oryzae(Xoo) secretes transcription activator-like effectors (TALEs) to activate rice susceptibility (S) genes, causing bacterial blight (BB), as well as resistance (R) genes, leading to defense against BB. This activation follows a gene-for-gene paradigm that results in an arms race between the TALE of the pathogen and effector-binding elements (EBEs) in the promoters of host genes. In this study, we characterized a novel TALE, designated Tal6b/AvrXa27A, that activates the rice Sgene OsSWEET11aand the rice Rgene Xa27. Tal6b/AvrXa27A is a member of the AvrXa27/TalAO class and contains 16 repeat variable diresidues (RVDs); one RVD is altered and one is deleted in Tal6b/AvrXa27A compared with AvrXa27, a known avirulence (avr) effector of Xa27. Tal6b/AvrXa27A can transcriptionally activate the expression of Xa27and OsSWEET11avia EBEs in their corresponding promoters, leading to effector-triggered immunity and susceptibility, respectively. The 16 RVDs in Tal6b/AvrXa27A have no obvious similarity to the 24 RVDs in the effector PthXo1, but EBETal6band EBEPthXo1are overlapped in the OsSWEET11apromoter. Tal6b/AvrXa27A is prevalent among Asian Xooisolates, but PthXo1 has only been reported in the Philippine strain PXO99A. Genome editing of EBETal6bin the OsSWEET11apromoter further confirmed the requirement for OsSWEET11aexpression in Tal6b/AvrXa27A-dependent susceptibility to Xoo. Moreover, Tal6b/AvrXa27A resulted in higher transcription of Xa27than of OsSWEET11a,which led to a strong, rapid resistance response that blocked disease development. These findings suggest that Tal6b/AvrXa27A has a dual function: triggering resistance by activating Xa27gene expression as an avirulence factor and inducing transcription of the Sgene OsSWEET11a, resulting in virulence. Intriguingly, Tal6b/AvrXa27A, but not AvrXa27, can bind to the promoter of OsSWEET11a. The underlying recognition mechanism for this binding remains unclear but appears to deviate from the currently accepted TALE DNA code.