Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton

Abstract Bacterial transcription activator-like effectors (TALEs) promote pathogenicity by activating host susceptibility (S) genes. To understand the pathogenicity and host adaptation of Xanthomonas citri pv. malvacearum (Xcm), we assemble the genome and the TALE repertoire of three recent Xcm Texa...

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Main Authors: Brendan W. Mormile, Yan Yan, Taran Bauer, Li Wang, Rachel C. Rivero, Sara C. D. Carpenter, Catherine Danmaigona Clement, Kevin L. Cox, Lin Zhang, Xiyu Ma, Terry A. Wheeler, Jane K. Dever, Ping He, Adam J. Bogdanove, Libo Shan
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-55926-7
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author Brendan W. Mormile
Yan Yan
Taran Bauer
Li Wang
Rachel C. Rivero
Sara C. D. Carpenter
Catherine Danmaigona Clement
Kevin L. Cox
Lin Zhang
Xiyu Ma
Terry A. Wheeler
Jane K. Dever
Ping He
Adam J. Bogdanove
Libo Shan
author_facet Brendan W. Mormile
Yan Yan
Taran Bauer
Li Wang
Rachel C. Rivero
Sara C. D. Carpenter
Catherine Danmaigona Clement
Kevin L. Cox
Lin Zhang
Xiyu Ma
Terry A. Wheeler
Jane K. Dever
Ping He
Adam J. Bogdanove
Libo Shan
author_sort Brendan W. Mormile
collection DOAJ
description Abstract Bacterial transcription activator-like effectors (TALEs) promote pathogenicity by activating host susceptibility (S) genes. To understand the pathogenicity and host adaptation of Xanthomonas citri pv. malvacearum (Xcm), we assemble the genome and the TALE repertoire of three recent Xcm Texas isolates. A newly evolved TALE, Tal7b, activates GhSWEET14a and GhSWEET14b, different from GhSWEET10 targeted by a TALE in an early Xcm isolate. Activation of GhSWEET14a and GhSWEET14b results in water-soaked lesions. Transcriptome profiling coupled with TALE-binding element prediction identify a pectin lyase gene as an additional Tal7b target, quantitatively contributing to Xcm virulence alongside GhSWEET14a/b. CRISPR-Cas9 gene editing supports the function of GhSWEETs in cotton bacterial blight and the promise of disrupting the TALE-binding site in S genes for disease management. Collectively, our findings elucidate the rapid evolution of TALEs in Xanthomonas field isolates and highlight the virulence mechanism wherein TALEs induce multiple S genes to promote pathogenicity.
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spelling doaj-art-8be68930dcbd4c37b0e788df5fa121c82025-01-19T12:30:02ZengNature PortfolioNature Communications2041-17232025-01-0116111710.1038/s41467-025-55926-7Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cottonBrendan W. Mormile0Yan Yan1Taran Bauer2Li Wang3Rachel C. Rivero4Sara C. D. Carpenter5Catherine Danmaigona Clement6Kevin L. Cox7Lin Zhang8Xiyu Ma9Terry A. Wheeler10Jane K. Dever11Ping He12Adam J. Bogdanove13Libo Shan14Department of Molecular, Cellular, and Developmental Biology, University of MichiganDepartment of Molecular, Cellular, and Developmental Biology, University of MichiganPlant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell UniversityPlant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell UniversityDepartment of Molecular, Cellular, and Developmental Biology, University of MichiganPlant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell UniversityDepartment of Plant Pathology and Microbiology, Texas A&M UniversityDepartment of Plant Pathology and Microbiology, Texas A&M UniversityDepartment of Plant Pathology and Microbiology, Texas A&M UniversityDepartment of Plant Pathology and Microbiology, Texas A&M UniversityTexas A&M AgriLife ResearchTexas A&M AgriLife ResearchDepartment of Molecular, Cellular, and Developmental Biology, University of MichiganPlant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell UniversityDepartment of Molecular, Cellular, and Developmental Biology, University of MichiganAbstract Bacterial transcription activator-like effectors (TALEs) promote pathogenicity by activating host susceptibility (S) genes. To understand the pathogenicity and host adaptation of Xanthomonas citri pv. malvacearum (Xcm), we assemble the genome and the TALE repertoire of three recent Xcm Texas isolates. A newly evolved TALE, Tal7b, activates GhSWEET14a and GhSWEET14b, different from GhSWEET10 targeted by a TALE in an early Xcm isolate. Activation of GhSWEET14a and GhSWEET14b results in water-soaked lesions. Transcriptome profiling coupled with TALE-binding element prediction identify a pectin lyase gene as an additional Tal7b target, quantitatively contributing to Xcm virulence alongside GhSWEET14a/b. CRISPR-Cas9 gene editing supports the function of GhSWEETs in cotton bacterial blight and the promise of disrupting the TALE-binding site in S genes for disease management. Collectively, our findings elucidate the rapid evolution of TALEs in Xanthomonas field isolates and highlight the virulence mechanism wherein TALEs induce multiple S genes to promote pathogenicity.https://doi.org/10.1038/s41467-025-55926-7
spellingShingle Brendan W. Mormile
Yan Yan
Taran Bauer
Li Wang
Rachel C. Rivero
Sara C. D. Carpenter
Catherine Danmaigona Clement
Kevin L. Cox
Lin Zhang
Xiyu Ma
Terry A. Wheeler
Jane K. Dever
Ping He
Adam J. Bogdanove
Libo Shan
Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
Nature Communications
title Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
title_full Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
title_fullStr Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
title_full_unstemmed Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
title_short Activation of three targets by a TAL effector confers susceptibility to bacterial blight of cotton
title_sort activation of three targets by a tal effector confers susceptibility to bacterial blight of cotton
url https://doi.org/10.1038/s41467-025-55926-7
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