A Xanthomonas transcription activator-like effector is trapped in nonhost plants for immunity

Fazal Haq; Xiameng Xu; Wenxiu Ma; Syed Mashab Ali Shah; Linlin Liu; Bo Zhu; Lifang Zou; Gongyou Chen

doi:10.1016/j.xplc.2021.100249

A Xanthomonas transcription activator-like effector is trapped in nonhost plants for immunity

Plant Commun. 2021 Oct 14;3(1):100249. doi: 10.1016/j.xplc.2021.100249. eCollection 2022 Jan 10.

Authors

Fazal Haq^{1

2}, Xiameng Xu^{1

2}, Wenxiu Ma^{1

2}, Syed Mashab Ali Shah^{1

2}, Linlin Liu^{1

2}, Bo Zhu¹, Lifang Zou^{1

2}, Gongyou Chen^{1

2}

Affiliations

¹ School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, China.
² Key Laboratory of Urban Agriculture of the Ministry of Agriculture, Shanghai, 200240, China.

Abstract

Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial leaf blight in rice, delivers transcription activator-like effector (TALE) proteins into host cells to activate susceptibility or resistance (R) genes that promote disease or immunity, respectively. Nonhost plants serve as potential reservoirs of R genes; consequently, nonhost R genes may trap TALEs to trigger an immune response. In this study, we screened 17 Xoo TALEs for their ability to induce a hypersensitive response (HR) in the nonhost plant Nicotiana benthamiana (Nb); only AvrXa10 elicited an HR when transiently expressed in Nb. The HR generated by AvrXa10 required both the central repeat region and the activation domain, suggesting a specific interaction between AvrXa10 and a potential R-like gene in nonhost plants. Evans blue staining and ion leakage measurements confirmed that the AvrXa10-triggered HR was a form of cell death, and the transient expression of AvrXa10 in Nb induced immune responses. Genes targeted by AvrXa10 in the Nb genome were identified by transcriptome profiling and prediction of effector binding sites. Using several approaches (in vivo reporter assays, electrophoretic mobility-shift assays, targeted designer TALEs, and on-spot gene silencing), we confirmed that AvrXa10 targets NbZnFP1, a C2H2-type zinc finger protein that resides in the nucleus. Functional analysis indicated that overexpression of NbZnFP1 and its rice orthologs triggered cell death in rice protoplasts. An NbZnFP1 ortholog was also identified in tomato and was specifically activated by AvrXa10. These results demonstrate that NbZnFP1 is a nonhost R gene that traps AvrXa10 to promote plant immunity in Nb.

Keywords: AvrXa10; Xanthomonas oryzae pv. oryzae; hypersensitive response; nonhost plant; zinc finger protein.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Bacterial Proteins / genetics
Plant Diseases / microbiology
Plants / metabolism
Transcription Activator-Like Effectors* / metabolism
Xanthomonas* / metabolism

Substances

Bacterial Proteins
Transcription Activator-Like Effectors