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

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 .

TALEs as double-edged swords in plant–pathogen interactions: Progress, challenges, and perspectives

“…vesicatoria ( Xcv ) Romer et al., (2007) Bs3-E FMO homolog pepper AvrBs3Δ16 Xcv Romer et al., (2007) Bs4C-R unknown executor pepper AvrBs4 Xcv Strauss et al., (2012) Xa7 unknown executor rice AvrXa7, PthXo3 Xanthomonas oryzae pv. oryzae ( Xoo ) Chen et al., (2021) ; Luo et al., (2021) ; Wang et al., (2021) Xa10 unknown executor rice AvrXa10 Xoo Tian et al., (2014) Xa10-Ni unknown executor rice dTALE-Xa10-Ni designed TALEs Wang et al., (2017) Xa23 unknown executor rice AvrXa23 Xoo Wang et al., (2015) Xa23-Ni unknown executor rice dTALE-Xa23-Ni-1, dTALE-Xa23-Ni-2 designed TALEs Wang et al., (2017) Xa27 unknown executor rice AvrXa27 Xoo Gu et al., (2005) ; Romer et al., (2009) Non-host R gene NbZnFP1 C2H2-type zinc-finger protein tobacco AvrXa10 Xoo Haq et al., (2022) …”

“…AvrXa10 has been reported to induce a non-host R gene, NbZnFP1 , in tobacco ( Haq et al., 2022 ). An EBE for AvrXa10 has been found in the promoter of NbZnFP1 , and activation of NbZnFP1 leads to cell death in tobacco and rice protoplasts ( Haq et al., 2022 ).…”

“…AvrXa10 has been reported to induce a non-host R gene, NbZnFP1 , in tobacco ( Haq et al., 2022 ). An EBE for AvrXa10 has been found in the promoter of NbZnFP1 , and activation of NbZnFP1 leads to cell death in tobacco and rice protoplasts ( Haq et al., 2022 ). NbZnFP1 encodes a C2H2-type zinc-finger protein that differs from XA10; its homolog has been identified in tomato, contains a similar EBE, and can also be activated by AvrXa10 ( Haq et al., 2022 ).…”

“…An EBE for AvrXa10 has been found in the promoter of NbZnFP1 , and activation of NbZnFP1 leads to cell death in tobacco and rice protoplasts ( Haq et al., 2022 ). NbZnFP1 encodes a C2H2-type zinc-finger protein that differs from XA10; its homolog has been identified in tomato, contains a similar EBE, and can also be activated by AvrXa10 ( Haq et al., 2022 ). The discovery of NbZnFP1 may increase research interest in non-host R genes in many other plants.…”

TALE-induced cell death executors: an origin outside immunity?

“…Expression of executors triggered by an intrinsic stimulus is likely to be restricted to a specific tissue or developmental stage and is likely to be involved in the formation of specific cells, tissues, or plant organs. Note that TALEs can also possibly induce cell death via transcriptional activation of a gene encoding a transcription factor, which in turn activates an executor gene ([63].…”