Tal6b/AvrXa27A, a hidden TALE targeting the susceptibility gene OsSWEET11a and the resistance gene Xa27 in rice
Zhengyin Xu, Xiameng Xu, Ying Li, Linlin Liu, Qi Wang, Yijie Wang, Yong Wang, Jiali Yan, Guanyun Cheng, Lifang Zou, Bo Zhu, Gongyou Chen
Abstract
Xanthomonas oryzae pv. oryzae (Xoo) secretes transcription activator-like effectors (TALEs) to activate rice susceptibility (S), 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 pathogen and effector-binding elements (EBEs) in the promoter of host genes. In this study, we characterized a novel TALE designated Tal6b/AvrXa27A that activates the rice S gene OsSWEET11a and the rice R gene Xa27. Tal6b/AvrXa27A is a member of the AvrXa27/TalAO class and contains 16 repeat variable diresidues (RVDs); in Tal6b/AvrXa27A, one RVD is altered and one is deleted when compared to AvrXa27, a known avirulence (avr) effector of Xa27. Tal6b/AvrXa27A transcriptionally activated the expression of both Xa27 and OsSWEET11a via EBEs in their corresponding promoters, thus leading to effector-triggered immunity and susceptibility, respectively. The 16 RVDs in Tal6b/AvrXa27A have no obvious similarity with the 24 RVDs in effector PthXo1, but EBETal6b and EBEPthXo1 overlapped in the OsSWEET11a promoter. Tal6b/AvrXa27A was prevalent among Asian Xoo isolates, but PthXo1 has only been reported in the Philippine strain PXO99A. Genome editing of EBETal6b in the OsSWEET11a promoter further corroborated the requirement of OsSWEET11a expression for Tal6b/AvrXa27A-dependent susceptibility to Xoo. Moreover, Tal6b/AvrXa27A resulted in higher transcription of Xa27 than OsSWEET11a, which led to a strong, rapid resistance response that blocked disease development. These findings suggest that Tal6b/AvrXa27A plays dual functions: triggering resistance by activating Xa27 gene expression as an avirulence factor while inducing transcription of the S gene OsSWEET11a, resulting in virulence. Intriguingly, Tal6b/AvrXa27A,but not AvrXa27, can bind to the promoter of OsSWEET11a. The underlying recognition mechanism for this remains unclear but appears to deviate from the currently accepted TALE-DNA code.