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Genome-wide identification and characterization of putative effectors in Heterodera schachtii that suppress plant immune response

Ke Yao1Menghan Zhang1Jianjun Xu2Deliang Peng1Wenkun Huang1Ling’an Kong1,3Shiming Liu1Guangkuo Li2( )Huan Peng1,2( )
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
Key Laboratory of Integrated Pest Management on Crop in Northwestern Oasis, Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences/Scientific Observing and Experimental Station of Korla, Ministry of Agriculture and Rural Affairs, Urumqi 830013, China
Zhongyuan Research Center, Chinese Academy of Agricultural Sciences, Xinxiang 453000, China
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Highlights

• We analyzed the genome and transcriptome data of Heterodera schachtii, and finally identified 51 potential predicted proteins after a series of screens.

• Functional validation of 37 successfully cloned putative effectors revealed 13 effectors that inhibited Bax-induced cell death, and 9 effectors that inhibited both Bax- and GPA2/RBP1-induced cell death.

• The 13 effector-triggered immunity suppressor genes are specifically expressed in esophageal gland cells and have the ability to significantly downregulate one or more defense genes in plant.

Abstract

The sugar beet cyst nematode (Heterodera schachtii) is one of the most destructive pathogens in sugar beet production, which causes serious economic losses every year. Few molecular details of effectors of H. schachtii parasitism are known. We analyzed the genome and transcriptome data of H. schachtii and identified multiple potential predicted proteins. After filtering out predicted proteins with high homology to other plant-parasitic nematodes, we performed functional validation of the remaining effector proteins. 37 putative effectors of H. schachtii were screened based on the Nicotiana benthamiana system for identifying the effectors that inhibit plant immune response, eventually determines 13 candidate effectors could inhibit cell death caused by Bax. Among the 13 effectors, nine have the ability to inhibit GPA2/RBP1-induced cell death. All 13 effector-triggered immunity (ETI) suppressor genes were analyzed by qRT-PCR and confirmed to result in a significant downregulation of one or more defense genes during infection compared to empty vector. For in situ hybridization, 13 effectors were specifically expressed and located in esophageal gland cells. These data and functional analysis set the stage for further studies on the interaction of H. schachtii with host and H. schachtii parasitic control.

References

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Journal of Integrative Agriculture (JIA)
Pages 196-208

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Cite this article:
Yao K, Zhang M, Xu J, et al. Genome-wide identification and characterization of putative effectors in Heterodera schachtii that suppress plant immune response. Journal of Integrative Agriculture (JIA), 2025, 24(1): 196-208. https://doi.org/10.1016/j.jia.2023.09.028

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Received: 06 June 2023
Accepted: 11 August 2023
Published: 20 January 2025
© 2025, Chinese Academy of Agricultural Sciences (CAAS). All rights reserved.