A varied AvrXa23-like TALE enables the bacterial blight pathogen to avoid being trapped by Xa23 resistance gene in rice

[Display omitted] •This study, for the first time, uncover a naturally-emerging Xa23-breaking Xoo isolate.•The ability of AvrXa23 to be trapped by the EBE of Xa23 gene can be altered by one or more RVDs of AvrXa23.•Seven AvrXa23-like TALEs determine the “arms-race” in the AvrXa23 and Xa23 pair.•This study provide new insights into the diversified strategies used by Xoo to evade host resistance.•Planting single R gene (like Xa23) rice in a great region is risk to make Xoo minority to majority. Xa23 as an executor mediates broad-spectrum resistance to Xanthomonas oryzae pv. oryzae (Xoo), which contains a matching avirulence gene avrXa23, in rice for bacterial leaf blight (BLB). avrXa23 encodes a transcription activator-like effector (TALE) protein which binds to the EBE (effector-binding element) of the Xa23 promoter. It is unclear whether the considerable pressure of Xa23 leads to an emerging Xoo strain that overcomes Xa23 resistance. This study aimed to uncover new Xoo isolate(s) that overcome Xa23-mediated resistance and to investigate how the pathogen evades the resistance. Totally 185 Xoo isolates were used to screen possibly compatible strain(s) with Xa23-containing rice CBB23 by pathogenicity test. Genome Sequencing, Southern blot, tal gene cloning, Western blot, qRT-PCR and electrophoretic mobility shift assays (EMSA) were conducted to determine the mechanism of one Xoo isolate being compatible with Xa23-containing rice. One isolate AH28 from Anhui province is compatible with CBB23. AH28 strain contains an ortholog of avrXa23, tal7b and has 17 tal genes. The 4th RVD (repeat-variable diresidue) in Tal7b are missed and the 5th and 8th RVDs changed from NG and NS to NS and S*, respectively. These alternations made Tal7b unable to bind to the EBE of Xa23 promoter to activate the expression of Xa23 in rice. The ectopic expression of tal7b in a tal-free mutant PH of PXO99A did not alter the virulence of the strain PH, whereas avrXa23 made AH28 from compatibility to incompatibility with Xa23 rice. Best to our knowledge, this is the first insight of a naturally-emerging Xoo isolate that overcomes the broad-spectrum resistance of Xa23 by the variable AvrXa23-like TALE Tal7b. The RVD alteration in AvrXa23 may be a common strategy for the pathogen evolution to avoid being “trapped” by the executor R gene.