A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism
<i>Radopholus similis</i> is a migratory endoparasitic nematode that is extremely harmful to host plants. Venom allergen-like proteins (VAPs) are members of the cysteine-rich secretory protein family that are widely present in plants and animals. In this study, we cloned a VAP gene from...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-04-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/22/9/4782 |
| _version_ | 1797535640078778368 |
|---|---|
| author | Junyi Li Chunling Xu Sihua Yang Chun Chen Shiqiao Tang Jiafeng Wang Hui Xie |
| author_facet | Junyi Li Chunling Xu Sihua Yang Chun Chen Shiqiao Tang Jiafeng Wang Hui Xie |
| author_sort | Junyi Li |
| collection | DOAJ |
| description | <i>Radopholus similis</i> is a migratory endoparasitic nematode that is extremely harmful to host plants. Venom allergen-like proteins (VAPs) are members of the cysteine-rich secretory protein family that are widely present in plants and animals. In this study, we cloned a VAP gene from <i>R. similis</i>, designated as RsVAP. RsVAP contains an open reading frame of 1089 bp encoding 362 amino acids. RsVAP is specifically expressed in the esophageal gland, and the expression levels of RsVAP are significantly higher in juveniles than in other life stages of <i>R. similis</i>. This expression pattern of RsVAP was consistent with the biological characteristics of juveniles of <i>R. similis</i>, which have the ability of infection and are the main infection stages of <i>R. similis</i>. The pathogenicity and reproduction rate of <i>R. similis</i> in tomato was significantly attenuated after RsVAP was silenced. In tobacco leaves transiently expressing RsVAP, the pathogen-associated molecular pattern-triggered immunity (PTI) induced by a bacterial flagellin fragment (flg22) was inhibited, while the cell death induced by two sets of immune elicitors (BAX and Gpa2/RBP-1) was repressed. The RsVAP-interacting, ras-related protein RABA1d (LeRabA1d) was identified in tomato hosts by yeast two-hybrid and co-immunoprecipitation assays. RsVAP may interact with LeRabA1d to affect the host defense response, which in turn facilitates nematode infection. This study provides the first evidence for the inhibition of plant defense response by a VAP from migratory plant-parasitic nematodes, and, for the first time, the target protein of <i>R. similis</i> in its host was identified. |
| first_indexed | 2024-03-10T11:47:19Z |
| format | Article |
| id | doaj.art-87a187a7099f46b1b325f5502ad5afc0 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T11:47:19Z |
| publishDate | 2021-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-87a187a7099f46b1b325f5502ad5afc02023-11-21T17:58:01ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-04-01229478210.3390/ijms22094782A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates ParasitismJunyi Li0Chunling Xu1Sihua Yang2Chun Chen3Shiqiao Tang4Jiafeng Wang5Hui Xie6Research Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaResearch Center of Nematodes of Plant Quarantine, Laboratory of Plant Nematology, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou 510642, China<i>Radopholus similis</i> is a migratory endoparasitic nematode that is extremely harmful to host plants. Venom allergen-like proteins (VAPs) are members of the cysteine-rich secretory protein family that are widely present in plants and animals. In this study, we cloned a VAP gene from <i>R. similis</i>, designated as RsVAP. RsVAP contains an open reading frame of 1089 bp encoding 362 amino acids. RsVAP is specifically expressed in the esophageal gland, and the expression levels of RsVAP are significantly higher in juveniles than in other life stages of <i>R. similis</i>. This expression pattern of RsVAP was consistent with the biological characteristics of juveniles of <i>R. similis</i>, which have the ability of infection and are the main infection stages of <i>R. similis</i>. The pathogenicity and reproduction rate of <i>R. similis</i> in tomato was significantly attenuated after RsVAP was silenced. In tobacco leaves transiently expressing RsVAP, the pathogen-associated molecular pattern-triggered immunity (PTI) induced by a bacterial flagellin fragment (flg22) was inhibited, while the cell death induced by two sets of immune elicitors (BAX and Gpa2/RBP-1) was repressed. The RsVAP-interacting, ras-related protein RABA1d (LeRabA1d) was identified in tomato hosts by yeast two-hybrid and co-immunoprecipitation assays. RsVAP may interact with LeRabA1d to affect the host defense response, which in turn facilitates nematode infection. This study provides the first evidence for the inhibition of plant defense response by a VAP from migratory plant-parasitic nematodes, and, for the first time, the target protein of <i>R. similis</i> in its host was identified.https://www.mdpi.com/1422-0067/22/9/4782<i>Radopholus similis</i>venom allergen-like proteinplant defenseinteracting protein |
| spellingShingle | Junyi Li Chunling Xu Sihua Yang Chun Chen Shiqiao Tang Jiafeng Wang Hui Xie A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism International Journal of Molecular Sciences <i>Radopholus similis</i> venom allergen-like protein plant defense interacting protein |
| title | A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism |
| title_full | A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism |
| title_fullStr | A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism |
| title_full_unstemmed | A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism |
| title_short | A Venom Allergen-Like Protein, RsVAP, the First Discovered Effector Protein of <i>Radopholus similis</i> That Inhibits Plant Defense and Facilitates Parasitism |
| title_sort | venom allergen like protein rsvap the first discovered effector protein of i radopholus similis i that inhibits plant defense and facilitates parasitism |
| topic | <i>Radopholus similis</i> venom allergen-like protein plant defense interacting protein |
| url | https://www.mdpi.com/1422-0067/22/9/4782 |
| work_keys_str_mv | AT junyili avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT chunlingxu avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT sihuayang avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT chunchen avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT shiqiaotang avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT jiafengwang avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT huixie avenomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT junyili venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT chunlingxu venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT sihuayang venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT chunchen venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT shiqiaotang venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT jiafengwang venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism AT huixie venomallergenlikeproteinrsvapthefirstdiscoveredeffectorproteinofiradopholussimilisithatinhibitsplantdefenseandfacilitatesparasitism |