The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine

Abstract Background Bursaphelenchus xylophilus is the causal agent of pine wilt disease (PWD) that has caused enormous ecological and economic losses in China. The mechanism in the interaction between nematodes and pine remains unclear. Plant parasitic nematodes (PPNs) secrete effectors into host pl...

Full description

Bibliographic Details
Main Authors: Yan Zhang, Tong-Yue Wen, Xiao-Qin Wu, Long-Jiao Hu, Yi-Jun Qiu, Lin Rui
Format: Article
Language:English
Published: BMC 2022-04-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-03567-z
_version_ 1818014257037443072
author Yan Zhang
Tong-Yue Wen
Xiao-Qin Wu
Long-Jiao Hu
Yi-Jun Qiu
Lin Rui
author_facet Yan Zhang
Tong-Yue Wen
Xiao-Qin Wu
Long-Jiao Hu
Yi-Jun Qiu
Lin Rui
author_sort Yan Zhang
collection DOAJ
description Abstract Background Bursaphelenchus xylophilus is the causal agent of pine wilt disease (PWD) that has caused enormous ecological and economic losses in China. The mechanism in the interaction between nematodes and pine remains unclear. Plant parasitic nematodes (PPNs) secrete effectors into host plant tissues. However, it is poorly studied that role of effector in the infection of pine wood nematode (PWN). Results We cloned, characterized and functionally validated the B. xylophilus effector BxML1, containing an MD-2-related lipid-recognition (ML) domain. This protein inhibits immune responses triggered by the molecular pattern BxCDP1 of B. xylophilus. An insitu hybridization assay demonstrated that BxML1 was expressed mainly in the dorsal glands and intestine of B. xylophilus. Subcellular localization analysis showed the presence of BxML1 in the cytoplasm and nucleus. Furthermore, number of B. xylophilus and morbidity of pine were significantly reduced in Pinus thunbergii infected with B. xylophilus when BxML was silenced. Using yeast two-hybrid (Y2H) and coimmunoprecipitation (CoIP) assays, we found that the BxML1 interacts with cyclophilin protein PtCyP1 in P. thunbergii. Conclusions This study illustrated that BxML1 plays a critical role in the B. xylophilus–plant interaction and virulence of B. xylophilus.
first_indexed 2024-04-14T06:42:43Z
format Article
id doaj.art-3b13519f791e4f6ab1bc1bfabc27dd0c
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-04-14T06:42:43Z
publishDate 2022-04-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-3b13519f791e4f6ab1bc1bfabc27dd0c2022-12-22T02:07:17ZengBMCBMC Plant Biology1471-22292022-04-0122111310.1186/s12870-022-03567-zThe Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pineYan Zhang0Tong-Yue Wen1Xiao-Qin Wu2Long-Jiao Hu3Yi-Jun Qiu4Lin Rui5Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityCo-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry UniversityAbstract Background Bursaphelenchus xylophilus is the causal agent of pine wilt disease (PWD) that has caused enormous ecological and economic losses in China. The mechanism in the interaction between nematodes and pine remains unclear. Plant parasitic nematodes (PPNs) secrete effectors into host plant tissues. However, it is poorly studied that role of effector in the infection of pine wood nematode (PWN). Results We cloned, characterized and functionally validated the B. xylophilus effector BxML1, containing an MD-2-related lipid-recognition (ML) domain. This protein inhibits immune responses triggered by the molecular pattern BxCDP1 of B. xylophilus. An insitu hybridization assay demonstrated that BxML1 was expressed mainly in the dorsal glands and intestine of B. xylophilus. Subcellular localization analysis showed the presence of BxML1 in the cytoplasm and nucleus. Furthermore, number of B. xylophilus and morbidity of pine were significantly reduced in Pinus thunbergii infected with B. xylophilus when BxML was silenced. Using yeast two-hybrid (Y2H) and coimmunoprecipitation (CoIP) assays, we found that the BxML1 interacts with cyclophilin protein PtCyP1 in P. thunbergii. Conclusions This study illustrated that BxML1 plays a critical role in the B. xylophilus–plant interaction and virulence of B. xylophilus.https://doi.org/10.1186/s12870-022-03567-zBursaphelenchus xylophilusEffectorMD-2-related lipid-recognition domain proteinCyclophilin proteinPinus thunbergii
spellingShingle Yan Zhang
Tong-Yue Wen
Xiao-Qin Wu
Long-Jiao Hu
Yi-Jun Qiu
Lin Rui
The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
BMC Plant Biology
Bursaphelenchus xylophilus
Effector
MD-2-related lipid-recognition domain protein
Cyclophilin protein
Pinus thunbergii
title The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
title_full The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
title_fullStr The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
title_full_unstemmed The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
title_short The Bursaphelenchus xylophilus effector BxML1 targets the cyclophilin protein (CyP) to promote parasitism and virulence in pine
title_sort bursaphelenchus xylophilus effector bxml1 targets the cyclophilin protein cyp to promote parasitism and virulence in pine
topic Bursaphelenchus xylophilus
Effector
MD-2-related lipid-recognition domain protein
Cyclophilin protein
Pinus thunbergii
url https://doi.org/10.1186/s12870-022-03567-z
work_keys_str_mv AT yanzhang thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT tongyuewen thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT xiaoqinwu thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT longjiaohu thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT yijunqiu thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT linrui thebursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT yanzhang bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT tongyuewen bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT xiaoqinwu bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT longjiaohu bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT yijunqiu bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine
AT linrui bursaphelenchusxylophiluseffectorbxml1targetsthecyclophilinproteincyptopromoteparasitismandvirulenceinpine