The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling

Abstract Plasmodiophora brassicae is one of the biggest threats to cruciferous plants and one of the most economically significant diseases worldwide. However, our current understanding of its pathogenic mechanisms remains limited. In this study, we have identified an effector, Pb257, which plays a...

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Main Authors: Hui Yang, Rong Liao, Chuang Jin, Xiaoya Feng, Yang Zhang, Xinyue Wang, Yuge Zhang, Liang Yu, Wenming Wang
Format: Article
Language:English
Published: BMC 2024-03-01
Series:Phytopathology Research
Subjects:
Online Access:https://doi.org/10.1186/s42483-024-00236-x
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author Hui Yang
Rong Liao
Chuang Jin
Xiaoya Feng
Yang Zhang
Xinyue Wang
Yuge Zhang
Liang Yu
Wenming Wang
author_facet Hui Yang
Rong Liao
Chuang Jin
Xiaoya Feng
Yang Zhang
Xinyue Wang
Yuge Zhang
Liang Yu
Wenming Wang
author_sort Hui Yang
collection DOAJ
description Abstract Plasmodiophora brassicae is one of the biggest threats to cruciferous plants and one of the most economically significant diseases worldwide. However, our current understanding of its pathogenic mechanisms remains limited. In this study, we have identified an effector, Pb257, which plays a crucial role in the virulence of P. brassicae. The expression pattern analysis revealed continuous induction of Pb257 during both primary and secondary infections. Ectopic expression of Pb257 strongly triggered cell death in Nicotiana benthamiana and several other plants, which was dependent on SOBIR1 and the salicylic acid pathway but not BAK1, a central molecular regulator, to mediate classical defense pathways. Overexpression of Pb257 increased susceptibility of Brassica rapa to P. brassicae. Silencing of the Pb257-encoding gene led to reduce root swelling. Further investigation showed that the conserved GOLD domain within Pb257 was essential for inducing root enlargement, which is similar to the mild symptoms of clubroot, indicating that it is an important effector for promoting root cell enlargement. GOLD domain-containing family proteins were widely present in the kingdoms of protozoa, fungi, and animalia, and Pb257 was clustered into a clade of protozoa, suggesting the encoding gene as a potential marker gene for classification of P. brassicae. The GOLD domain-containing proteins are known regulators involved in human cell proliferation and immune system disruption, however, no previous reports have described a pathogen-derived GOLD domain protein with elicitor activity. Our findings demonstrate that Pb257 functions as a crucial effector contributing to the virulence of P. brassicae and could be used as a potential molecular target for controlling clubroot disease.
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spelling doaj.art-4a019b8ad94448ceb2ca4f7292c308922024-03-31T11:11:54ZengBMCPhytopathology Research2524-41672024-03-016111310.1186/s42483-024-00236-xThe conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swellingHui Yang0Rong Liao1Chuang Jin2Xiaoya Feng3Yang Zhang4Xinyue Wang5Yuge Zhang6Liang Yu7Wenming Wang8State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityThe Agricultural Comprehensive Service Center, Agriculture and Rural Bureau of Xindu DistrictState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural UniversityAbstract Plasmodiophora brassicae is one of the biggest threats to cruciferous plants and one of the most economically significant diseases worldwide. However, our current understanding of its pathogenic mechanisms remains limited. In this study, we have identified an effector, Pb257, which plays a crucial role in the virulence of P. brassicae. The expression pattern analysis revealed continuous induction of Pb257 during both primary and secondary infections. Ectopic expression of Pb257 strongly triggered cell death in Nicotiana benthamiana and several other plants, which was dependent on SOBIR1 and the salicylic acid pathway but not BAK1, a central molecular regulator, to mediate classical defense pathways. Overexpression of Pb257 increased susceptibility of Brassica rapa to P. brassicae. Silencing of the Pb257-encoding gene led to reduce root swelling. Further investigation showed that the conserved GOLD domain within Pb257 was essential for inducing root enlargement, which is similar to the mild symptoms of clubroot, indicating that it is an important effector for promoting root cell enlargement. GOLD domain-containing family proteins were widely present in the kingdoms of protozoa, fungi, and animalia, and Pb257 was clustered into a clade of protozoa, suggesting the encoding gene as a potential marker gene for classification of P. brassicae. The GOLD domain-containing proteins are known regulators involved in human cell proliferation and immune system disruption, however, no previous reports have described a pathogen-derived GOLD domain protein with elicitor activity. Our findings demonstrate that Pb257 functions as a crucial effector contributing to the virulence of P. brassicae and could be used as a potential molecular target for controlling clubroot disease.https://doi.org/10.1186/s42483-024-00236-xPlasmodiophora brassicaeEffectorPb257GOLD domainHIGS
spellingShingle Hui Yang
Rong Liao
Chuang Jin
Xiaoya Feng
Yang Zhang
Xinyue Wang
Yuge Zhang
Liang Yu
Wenming Wang
The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
Phytopathology Research
Plasmodiophora brassicae
Effector
Pb257
GOLD domain
HIGS
title The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
title_full The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
title_fullStr The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
title_full_unstemmed The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
title_short The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling
title_sort conserved gold domain in the plasmodiophora brassicae effector pb257 is required for triggering cell death and root swelling
topic Plasmodiophora brassicae
Effector
Pb257
GOLD domain
HIGS
url https://doi.org/10.1186/s42483-024-00236-x
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