TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice

Abstract Bacterial blight (BB) of rice caused by Xanthomonas oryzae pv. oryzae (Xoo), is an important disease in rice-growing countries, including Pakistan, where it was first reported in the mid-1970s. Transcription activator-like effectors (TALEs) play vital roles in many plant diseases caused by...

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Main Authors: Syed Mashab Ali Shah, Rafia Ahsan, Linlin Liu, Ying Li, Qi Wang, Yong Wang, Jiali Yan, Moein Khojasteh, Xiameng Xu, Zhengyin Xu, Awais Rasheed, Muhammad Zakria, Gongyou Chen
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Phytopathology Research
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Online Access:https://doi.org/10.1186/s42483-024-00292-3
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author Syed Mashab Ali Shah
Rafia Ahsan
Linlin Liu
Ying Li
Qi Wang
Yong Wang
Jiali Yan
Moein Khojasteh
Xiameng Xu
Zhengyin Xu
Awais Rasheed
Muhammad Zakria
Gongyou Chen
author_facet Syed Mashab Ali Shah
Rafia Ahsan
Linlin Liu
Ying Li
Qi Wang
Yong Wang
Jiali Yan
Moein Khojasteh
Xiameng Xu
Zhengyin Xu
Awais Rasheed
Muhammad Zakria
Gongyou Chen
author_sort Syed Mashab Ali Shah
collection DOAJ
description Abstract Bacterial blight (BB) of rice caused by Xanthomonas oryzae pv. oryzae (Xoo), is an important disease in rice-growing countries, including Pakistan, where it was first reported in the mid-1970s. Transcription activator-like effectors (TALEs) play vital roles in many plant diseases caused by Xanthomonas spp.; however, Pakistani Xoo TALome diversity and their contribution to pathogenicity is largely unknown. In this study, 101 Xoo strains were screened using specific PCR primers. The genomic DNA from these strains underwent BamHI digestion and hybridized with the internal SphI fragment of PthXo1. Southern blot analysis revealed 16 to 20 putative tale fragments among the tested strains. These strains were further classified into 11 genotypes based on the number and size of the hybridizing bands. Genotypes 1, 2, 3, and 4 represented 24, 2, 51, and 17 strains, respectively. Pathogenicity assays on near-isogenic lines (NILs) containing different resistance (R) genes exhibited that CBB23 was incompatible with all tested Pakistani-Xoo genotypes, whereas IRBB5 and IRBB4 showed resistance against specific genotypes. In contrast, paddy trails on NILs containing single, double, and triple mutants of OsSWEET11a, OsSWEET13, and OsSWEET14 in the effector binding elements (EBEs) of cv. Kitaake revealed that KP-22 and LD-5 harbor novel virulent TAL effector/s. Interestingly, the expression analysis of six clade-III OsSWEET genes suggests that novel TALE/s targeting unidentified susceptibility gene/s. Altogether, this study highlights gene-for-gene relationships between tested rice lines and Pakistani-Xoo strains. This is the first report providing the diversity of TALEs and their relationship to R and S (susceptibility) genes. Further identification of novel virulent TALE/s and their cognate target/s is warranted to precisely elucidate their role in BB.
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spelling doaj-art-e7827ecedd9a4f2faba35a950c98b8202025-01-19T12:12:15ZengBMCPhytopathology Research2524-41672025-01-017111610.1186/s42483-024-00292-3TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of riceSyed Mashab Ali Shah0Rafia Ahsan1Linlin Liu2Ying Li3Qi Wang4Yong Wang5Jiali Yan6Moein Khojasteh7Xiameng Xu8Zhengyin Xu9Awais Rasheed10Muhammad Zakria11Gongyou Chen12Shanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityCrop Diseases Research Institute, National Agricultural Research CenterShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityDepartment of Plant Sciences, Quiad-e-Azam UniversityCrop Diseases Research Institute, National Agricultural Research CenterShanghai Collaborative Innovation Center of Agri-Seeds/State Key Laboratory of Microbial Metabolism, School of Agriculture and Biology, Shanghai Jiao Tong UniversityAbstract Bacterial blight (BB) of rice caused by Xanthomonas oryzae pv. oryzae (Xoo), is an important disease in rice-growing countries, including Pakistan, where it was first reported in the mid-1970s. Transcription activator-like effectors (TALEs) play vital roles in many plant diseases caused by Xanthomonas spp.; however, Pakistani Xoo TALome diversity and their contribution to pathogenicity is largely unknown. In this study, 101 Xoo strains were screened using specific PCR primers. The genomic DNA from these strains underwent BamHI digestion and hybridized with the internal SphI fragment of PthXo1. Southern blot analysis revealed 16 to 20 putative tale fragments among the tested strains. These strains were further classified into 11 genotypes based on the number and size of the hybridizing bands. Genotypes 1, 2, 3, and 4 represented 24, 2, 51, and 17 strains, respectively. Pathogenicity assays on near-isogenic lines (NILs) containing different resistance (R) genes exhibited that CBB23 was incompatible with all tested Pakistani-Xoo genotypes, whereas IRBB5 and IRBB4 showed resistance against specific genotypes. In contrast, paddy trails on NILs containing single, double, and triple mutants of OsSWEET11a, OsSWEET13, and OsSWEET14 in the effector binding elements (EBEs) of cv. Kitaake revealed that KP-22 and LD-5 harbor novel virulent TAL effector/s. Interestingly, the expression analysis of six clade-III OsSWEET genes suggests that novel TALE/s targeting unidentified susceptibility gene/s. Altogether, this study highlights gene-for-gene relationships between tested rice lines and Pakistani-Xoo strains. This is the first report providing the diversity of TALEs and their relationship to R and S (susceptibility) genes. Further identification of novel virulent TALE/s and their cognate target/s is warranted to precisely elucidate their role in BB.https://doi.org/10.1186/s42483-024-00292-3Xanthomonas oryzae pv. oryzaeBacterial blightTALome diversityMajor TALEs EBE edited susceptibility genesNILs containing R genes
spellingShingle Syed Mashab Ali Shah
Rafia Ahsan
Linlin Liu
Ying Li
Qi Wang
Yong Wang
Jiali Yan
Moein Khojasteh
Xiameng Xu
Zhengyin Xu
Awais Rasheed
Muhammad Zakria
Gongyou Chen
TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
Phytopathology Research
Xanthomonas oryzae pv. oryzae
Bacterial blight
TALome diversity
Major TALEs EBE edited susceptibility genes
NILs containing R genes
title TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
title_full TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
title_fullStr TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
title_full_unstemmed TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
title_short TALome and phenotypic analysis of Pakistani Xanthomonas oryzae pv. oryzae population revealed novel virulent TALEs contributing to bacterial blight of rice
title_sort talome and phenotypic analysis of pakistani xanthomonas oryzae pv oryzae population revealed novel virulent tales contributing to bacterial blight of rice
topic Xanthomonas oryzae pv. oryzae
Bacterial blight
TALome diversity
Major TALEs EBE edited susceptibility genes
NILs containing R genes
url https://doi.org/10.1186/s42483-024-00292-3
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