A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration
The migratory endoparasitic phytonematodes Bursaphelenchus xylophilus is the causal agent of pine wilt disease and causes significant economic damage to pine forests in China. Effectors play a key role in the successful parasitism of plants by phytonematodes. In this study, 210 genes obtained by tra...
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| Format: | Article |
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Frontiers Media S.A.
2024-02-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1357141/full |
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| author | Zhiwen Li Honghong Wang Yuqing Cao Xiaoling Shan Xiaoxian He Qiuling Huang Kan Zhuo Kan Zhuo Jinling Liao Jinling Liao Borong Lin Borong Lin |
| author_facet | Zhiwen Li Honghong Wang Yuqing Cao Xiaoling Shan Xiaoxian He Qiuling Huang Kan Zhuo Kan Zhuo Jinling Liao Jinling Liao Borong Lin Borong Lin |
| author_sort | Zhiwen Li |
| collection | DOAJ |
| description | The migratory endoparasitic phytonematodes Bursaphelenchus xylophilus is the causal agent of pine wilt disease and causes significant economic damage to pine forests in China. Effectors play a key role in the successful parasitism of plants by phytonematodes. In this study, 210 genes obtained by transcriptomics analyses were found to be upregulated in B. xylophilus infecting Pinus massoniana that were not functionally annotated nor reported previously in B. xylophilus infecting P. thunbergii. Among these differentially expressed genes, a novel effector, BxICD1, that could induce cell death in the extracellular space of Nicotiana benthamiana was identified. BxICD1 was upregulated in the early stages of infection, as shown by RT-qPCR analyses. In situ hybridization analysis showed that BxICD1 was expressed in the esophageal gland of nematodes. The yeast signal sequence trap system indicated that BxICD1 possessed an N-terminal signal peptide with secretion functionality. Using an Agrobacterium-mediated transient expression system, it was demonstrated that the cell death-inducing activity of BxICD1 was dependent on N. benthamiana brassinosteroid-insensitive 1-associated kinase 1 (NbBAK1). Finally, BxICD1 contributed to B. xylophilus virulence and migration in host pine trees, as demonstrated by RNAi silencing assays. These findings indicate that BxICD1 both induces plant cell death and also contributes to nematode virulence and migration in P. massonian. |
| first_indexed | 2024-03-07T20:06:13Z |
| format | Article |
| id | doaj.art-935adfd40d2f4bfd90fa22b560563a5b |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-07T20:06:13Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-935adfd40d2f4bfd90fa22b560563a5b2024-02-28T05:03:00ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-02-011510.3389/fpls.2024.13571411357141A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migrationZhiwen Li0Honghong Wang1Yuqing Cao2Xiaoling Shan3Xiaoxian He4Qiuling Huang5Kan Zhuo6Kan Zhuo7Jinling Liao8Jinling Liao9Borong Lin10Borong Lin11College of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollaborative Innovation Center of Plant Pest Management and Bioenvironmental Health Application Technology, Guangdong Eco-Engineering Polytechnic, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaCollaborative Innovation Center of Plant Pest Management and Bioenvironmental Health Application Technology, Guangdong Eco-Engineering Polytechnic, Guangzhou, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, ChinaThe migratory endoparasitic phytonematodes Bursaphelenchus xylophilus is the causal agent of pine wilt disease and causes significant economic damage to pine forests in China. Effectors play a key role in the successful parasitism of plants by phytonematodes. In this study, 210 genes obtained by transcriptomics analyses were found to be upregulated in B. xylophilus infecting Pinus massoniana that were not functionally annotated nor reported previously in B. xylophilus infecting P. thunbergii. Among these differentially expressed genes, a novel effector, BxICD1, that could induce cell death in the extracellular space of Nicotiana benthamiana was identified. BxICD1 was upregulated in the early stages of infection, as shown by RT-qPCR analyses. In situ hybridization analysis showed that BxICD1 was expressed in the esophageal gland of nematodes. The yeast signal sequence trap system indicated that BxICD1 possessed an N-terminal signal peptide with secretion functionality. Using an Agrobacterium-mediated transient expression system, it was demonstrated that the cell death-inducing activity of BxICD1 was dependent on N. benthamiana brassinosteroid-insensitive 1-associated kinase 1 (NbBAK1). Finally, BxICD1 contributed to B. xylophilus virulence and migration in host pine trees, as demonstrated by RNAi silencing assays. These findings indicate that BxICD1 both induces plant cell death and also contributes to nematode virulence and migration in P. massonian.https://www.frontiersin.org/articles/10.3389/fpls.2024.1357141/fullBursaphelenchus xylophilustranscriptomePinus massonianaeffectorplant cell death activation |
| spellingShingle | Zhiwen Li Honghong Wang Yuqing Cao Xiaoling Shan Xiaoxian He Qiuling Huang Kan Zhuo Kan Zhuo Jinling Liao Jinling Liao Borong Lin Borong Lin A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration Frontiers in Plant Science Bursaphelenchus xylophilus transcriptome Pinus massoniana effector plant cell death activation |
| title | A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration |
| title_full | A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration |
| title_fullStr | A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration |
| title_full_unstemmed | A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration |
| title_short | A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration |
| title_sort | bursaphelenchus xylophilus effector bxicd1 inducing plant cell death concurrently contributes to nematode virulence and migration |
| topic | Bursaphelenchus xylophilus transcriptome Pinus massoniana effector plant cell death activation |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1357141/full |
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