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Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice.
Mol Plant. 2019 11 04; 12(11):1434-1446.MP

Abstract

Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight of rice, employs the transcription activator-like effectors (TALEs) to induce the expression of the OsSWEET family of putative sugar transporter genes, which function in conferring disease susceptibility (S) in rice plants. To engineer broad-spectrum bacterial blight resistance, we used CRISPR/Cas9-mediated gene editing to disrupt the TALE-binding elements (EBEs) of two S genes, OsSWEET11 and OsSWEET14, in rice cv. Kitaake, which harbors the recessive resistance allele of Xa25/OsSWEET13. The engineered rice line MS14K exhibited broad-spectrum resistance to most Xoo strains with a few exceptions, suggesting that the compatible strains may contain new TALEs. We identified two PthXo2-like TALEs, Tal5LN18 and Tal7PXO61, as major virulence factors in the compatible Xoo strains LN18 and PXO61, respectively, and found that Xoo encodes at least five types of PthXo2-like effectors. Given that PthXo2/PthXo2.1 target OsSWEET13 for transcriptional activation, the genomes of 3000 rice varieties were analyzed for EBE variationsin the OsSWEET13 promoter, and 10 Xa25-like haplotypes were identified. We found that Tal5LN18 and Tal7PXO61 bind slightly different EBE sequences in the OsSWEET13 promoter to activate its expression. CRISPR/Cas9 technology was then used to generate InDels in the EBE of the OsSWEET13 promoter in MS14K to creat a new germplasm with three edited OsSWEET EBEs and broad-spectrum resistance against all Xoo strains tested. Collectively, our findings illustrate how to disarm TALE-S co-evolved loci to generate broad-spectrum resistance through the loss of effector-triggered susceptibility in plants.

Authors+Show Affiliations

School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China. Electronic address: zoulifang202018@sjtu.edu.cn.School of Agriculture and Biology/State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China. Electronic address: gyouchen@sjtu.edu.cn.

Pub Type(s)

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

Language

eng

PubMed ID

31493565

Citation

Xu, Zhengyin, et al. "Engineering Broad-Spectrum Bacterial Blight Resistance By Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice." Molecular Plant, vol. 12, no. 11, 2019, pp. 1434-1446.
Xu Z, Xu X, Gong Q, et al. Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice. Mol Plant. 2019;12(11):1434-1446.
Xu, Z., Xu, X., Gong, Q., Li, Z., Li, Y., Wang, S., Yang, Y., Ma, W., Liu, L., Zhu, B., Zou, L., & Chen, G. (2019). Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice. Molecular Plant, 12(11), 1434-1446. https://doi.org/10.1016/j.molp.2019.08.006
Xu Z, et al. Engineering Broad-Spectrum Bacterial Blight Resistance By Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice. Mol Plant. 2019 11 4;12(11):1434-1446. PubMed PMID: 31493565.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice. AU - Xu,Zhengyin, AU - Xu,Xiameng, AU - Gong,Qiang, AU - Li,Ziyang, AU - Li,Ying, AU - Wang,Sai, AU - Yang,Yangyang, AU - Ma,Wenxiu, AU - Liu,Longyu, AU - Zhu,Bo, AU - Zou,Lifang, AU - Chen,Gongyou, Y1 - 2019/09/04/ PY - 2019/05/13/received PY - 2019/08/01/revised PY - 2019/08/11/accepted PY - 2019/9/8/pubmed PY - 2020/5/6/medline PY - 2019/9/8/entrez KW - ETS KW - RLS KW - TALE KW - Xanthomonas oryzae pv. oryzae KW - susceptible gene SP - 1434 EP - 1446 JF - Molecular plant JO - Mol Plant VL - 12 IS - 11 N2 - Xanthomonas oryzae pv. oryzae (Xoo), the causal agent of bacterial blight of rice, employs the transcription activator-like effectors (TALEs) to induce the expression of the OsSWEET family of putative sugar transporter genes, which function in conferring disease susceptibility (S) in rice plants. To engineer broad-spectrum bacterial blight resistance, we used CRISPR/Cas9-mediated gene editing to disrupt the TALE-binding elements (EBEs) of two S genes, OsSWEET11 and OsSWEET14, in rice cv. Kitaake, which harbors the recessive resistance allele of Xa25/OsSWEET13. The engineered rice line MS14K exhibited broad-spectrum resistance to most Xoo strains with a few exceptions, suggesting that the compatible strains may contain new TALEs. We identified two PthXo2-like TALEs, Tal5LN18 and Tal7PXO61, as major virulence factors in the compatible Xoo strains LN18 and PXO61, respectively, and found that Xoo encodes at least five types of PthXo2-like effectors. Given that PthXo2/PthXo2.1 target OsSWEET13 for transcriptional activation, the genomes of 3000 rice varieties were analyzed for EBE variationsin the OsSWEET13 promoter, and 10 Xa25-like haplotypes were identified. We found that Tal5LN18 and Tal7PXO61 bind slightly different EBE sequences in the OsSWEET13 promoter to activate its expression. CRISPR/Cas9 technology was then used to generate InDels in the EBE of the OsSWEET13 promoter in MS14K to creat a new germplasm with three edited OsSWEET EBEs and broad-spectrum resistance against all Xoo strains tested. Collectively, our findings illustrate how to disarm TALE-S co-evolved loci to generate broad-spectrum resistance through the loss of effector-triggered susceptibility in plants. SN - 1752-9867 UR - https://www.unboundmedicine.com/medline/citation/31493565/Engineering_Broad_Spectrum_Bacterial_Blight_Resistance_by_Simultaneously_Disrupting_Variable_TALE_Binding_Elements_of_Multiple_Susceptibility_Genes_in_Rice_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1674-2052(19)30289-8 DB - PRIME DP - Unbound Medicine ER -