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A transcription activator-like effector from Xanthomonas oryzae pv. oryzicola elicits dose-dependent resistance in rice.
Mol Plant Pathol. 2017 01; 18(1):55-66.MP

Abstract

Xanthomonas spp. reduce crop yields and quality worldwide. During infection of their plant hosts, many strains secrete transcription activator-like (TAL) effectors, which enter the host cell nucleus and activate specific corresponding host genes at effector binding elements (EBEs) in the promoter. TAL effectors may contribute to disease by activating the expression of susceptibility genes or trigger resistance associated with the hypersensitive reaction (HR) by activating an executor resistance (R) gene. The rice bacterial leaf streak pathogen X. oryzae pv. oryzicola (Xoc) is known to suppress host resistance, and no host R gene has been identified against it, despite considerable effort. To further investigate Xoc suppression of host resistance, we conducted a screen of effectors from BLS256 and identified Tal2a as an HR elicitor in rice when delivered heterologously by a strain of the closely related rice bacterial blight pathogen X. oryzae pv. oryzae (Xoo) or by the soybean pathogen X. axonopodis pv. glycines. The HR required the Tal2a activation domain, suggesting an executor R gene. Tal2a activity was differentially distributed among geographically diverse Xoc isolates, being largely conserved among Asian isolates. We identified four genes induced by Tal2a in next-generation RNA sequencing experiments and confirmed them using quantitative real-time reverse transcription-polymerase chain reaction (qPCR). However, neither individual nor collective activation of these genes by designer TAL effectors resulted in HR. A tal2a knockout mutant of BLS256 showed virulence comparable with the wild-type, but plasmid-based overexpression of tal2a at different levels in the wild-type reduced virulence in a directly corresponding way. Overall, the results reveal that host resistance suppression by Xoc plays a critical role in pathogenesis. Further, the dose-dependent avirulence activity of Tal2a and the apparent lack of a single canonical target that accounts for HR point to a novel, activation domain-dependent mode of action, which might involve, for example, a non-coding gene or a specific pattern of activation across multiple targets.

Authors+Show Affiliations

Department of Plant Pathology and Microbiology, Iowa State University, 351 Bessey Hall, Ames, IA, 50011, USA.Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA. Graduate Field of Computational Biology, Cornell University, Ithaca, NY, 14853, USA.Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.Department of Plant Pathology and Microbiology, Iowa State University, 351 Bessey Hall, Ames, IA, 50011, USA. Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.

Pub Type(s)

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

Language

eng

PubMed ID

26821568

Citation

Hummel, Aaron W., et al. "A Transcription Activator-like Effector From Xanthomonas Oryzae Pv. Oryzicola Elicits Dose-dependent Resistance in Rice." Molecular Plant Pathology, vol. 18, no. 1, 2017, pp. 55-66.
Hummel AW, Wilkins KE, Wang L, et al. A transcription activator-like effector from Xanthomonas oryzae pv. oryzicola elicits dose-dependent resistance in rice. Mol Plant Pathol. 2017;18(1):55-66.
Hummel, A. W., Wilkins, K. E., Wang, L., Cernadas, R. A., & Bogdanove, A. J. (2017). A transcription activator-like effector from Xanthomonas oryzae pv. oryzicola elicits dose-dependent resistance in rice. Molecular Plant Pathology, 18(1), 55-66. https://doi.org/10.1111/mpp.12377
Hummel AW, et al. A Transcription Activator-like Effector From Xanthomonas Oryzae Pv. Oryzicola Elicits Dose-dependent Resistance in Rice. Mol Plant Pathol. 2017;18(1):55-66. PubMed PMID: 26821568.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A transcription activator-like effector from Xanthomonas oryzae pv. oryzicola elicits dose-dependent resistance in rice. AU - Hummel,Aaron W, AU - Wilkins,Katherine E, AU - Wang,Li, AU - Cernadas,R Andres, AU - Bogdanove,Adam J, Y1 - 2016/04/21/ PY - 2015/11/15/received PY - 2016/01/24/revised PY - 2016/01/27/accepted PY - 2016/1/30/pubmed PY - 2017/6/20/medline PY - 2016/1/30/entrez KW - TAL effector KW - Xanthomonas KW - bacterial leaf streak of rice KW - resistance SP - 55 EP - 66 JF - Molecular plant pathology JO - Mol Plant Pathol VL - 18 IS - 1 N2 - Xanthomonas spp. reduce crop yields and quality worldwide. During infection of their plant hosts, many strains secrete transcription activator-like (TAL) effectors, which enter the host cell nucleus and activate specific corresponding host genes at effector binding elements (EBEs) in the promoter. TAL effectors may contribute to disease by activating the expression of susceptibility genes or trigger resistance associated with the hypersensitive reaction (HR) by activating an executor resistance (R) gene. The rice bacterial leaf streak pathogen X. oryzae pv. oryzicola (Xoc) is known to suppress host resistance, and no host R gene has been identified against it, despite considerable effort. To further investigate Xoc suppression of host resistance, we conducted a screen of effectors from BLS256 and identified Tal2a as an HR elicitor in rice when delivered heterologously by a strain of the closely related rice bacterial blight pathogen X. oryzae pv. oryzae (Xoo) or by the soybean pathogen X. axonopodis pv. glycines. The HR required the Tal2a activation domain, suggesting an executor R gene. Tal2a activity was differentially distributed among geographically diverse Xoc isolates, being largely conserved among Asian isolates. We identified four genes induced by Tal2a in next-generation RNA sequencing experiments and confirmed them using quantitative real-time reverse transcription-polymerase chain reaction (qPCR). However, neither individual nor collective activation of these genes by designer TAL effectors resulted in HR. A tal2a knockout mutant of BLS256 showed virulence comparable with the wild-type, but plasmid-based overexpression of tal2a at different levels in the wild-type reduced virulence in a directly corresponding way. Overall, the results reveal that host resistance suppression by Xoc plays a critical role in pathogenesis. Further, the dose-dependent avirulence activity of Tal2a and the apparent lack of a single canonical target that accounts for HR point to a novel, activation domain-dependent mode of action, which might involve, for example, a non-coding gene or a specific pattern of activation across multiple targets. SN - 1364-3703 UR - https://www.unboundmedicine.com/medline/citation/26821568/A_transcription_activator_like_effector_from_Xanthomonas_oryzae_pv__oryzicola_elicits_dose_dependent_resistance_in_rice_ L2 - https://doi.org/10.1111/mpp.12377 DB - PRIME DP - Unbound Medicine ER -