SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato
Bri1-associated kinase 1 (BAK1)-interacting receptor-like kinase (BIR) proteins have been shown to play important roles in regulating growth and development, pathogen associated molecular pattern (PAMP)-triggered immunity (PTI) responses, and cell death in the model plant, Arabidopsis thaliana. We i...
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| Format: | Article |
| Language: | English |
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MDPI AG
2017-09-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/18/9/1966 |
| _version_ | 1811344967331741696 |
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| author | Shuhua Huang Shuming Nie Shufen Wang Jianwei Liu Yanfeng Zhang Xiaofeng Wang |
| author_facet | Shuhua Huang Shuming Nie Shufen Wang Jianwei Liu Yanfeng Zhang Xiaofeng Wang |
| author_sort | Shuhua Huang |
| collection | DOAJ |
| description | Bri1-associated kinase 1 (BAK1)-interacting receptor-like kinase (BIR) proteins have been shown to play important roles in regulating growth and development, pathogen associated molecular pattern (PAMP)-triggered immunity (PTI) responses, and cell death in the model plant, Arabidopsis thaliana. We identified four BIR family members in tomato (Solanum lycopersicum), including SlBIR3, an ortholog of AtBIR3 from A. thaliana. SlBIR3 is predicted to encode a membrane localized non-arginine-aspartate (non-RD) kinase that, based on protein sequence, does not have autophosphorylation activity but that can be phosphorylated in vivo. We established that SlBIR3 interacts with SlBAK1 and AtBAK1 using yeast two-hybrid assays and co-immunoprecipitation and maltose-binding protein pull down assays. We observed that SlBIR3 overexpression in tomato (cv. micro-tom) and A. thaliana has weak effect on growth and development through brassinosteroid (BR) signaling. SlBIR3 overexpression in A. thaliana suppressed flg22-induced defense responses, but did not affect infection with the bacterial pathogen Pseudomonas syringae (PstDC3000). This result was confirmed using virus-induced gene silencing (VIGS) in tomato in conjunction with PstDC3000 infection. Overexpression of SlBIR3 in tomato (cv. micro-tom) and A. thaliana resulted in enhanced susceptibility to the necrotrophic fungus Botrytis cinerea. In addition, co-silencing SlBIR3 with SlSERK3A or SlSERK3B using VIGS and the tobacco rattle virus (TRV)-RNA2 vector containing fragments of both the SlSERK3 and SlBIR3 genes induced spontaneous cell death, indicating a cooperation between the two proteins in this process. In conclusion, our study revealed that SlBIR3 is the ortholog of AtBIR3 and that it participates in BR, PTI, and cell death signaling pathways. |
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| language | English |
| last_indexed | 2024-04-13T19:56:02Z |
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| spelling | doaj.art-f867e34592704de4b6b40f73000029332022-12-22T02:32:20ZengMDPI AGInternational Journal of Molecular Sciences1422-00672017-09-01189196610.3390/ijms18091966ijms18091966SlBIR3 Negatively Regulates PAMP Responses and Cell Death in TomatoShuhua Huang0Shuming Nie1Shufen Wang2Jianwei Liu3Yanfeng Zhang4Xiaofeng Wang5State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, ChinaBri1-associated kinase 1 (BAK1)-interacting receptor-like kinase (BIR) proteins have been shown to play important roles in regulating growth and development, pathogen associated molecular pattern (PAMP)-triggered immunity (PTI) responses, and cell death in the model plant, Arabidopsis thaliana. We identified four BIR family members in tomato (Solanum lycopersicum), including SlBIR3, an ortholog of AtBIR3 from A. thaliana. SlBIR3 is predicted to encode a membrane localized non-arginine-aspartate (non-RD) kinase that, based on protein sequence, does not have autophosphorylation activity but that can be phosphorylated in vivo. We established that SlBIR3 interacts with SlBAK1 and AtBAK1 using yeast two-hybrid assays and co-immunoprecipitation and maltose-binding protein pull down assays. We observed that SlBIR3 overexpression in tomato (cv. micro-tom) and A. thaliana has weak effect on growth and development through brassinosteroid (BR) signaling. SlBIR3 overexpression in A. thaliana suppressed flg22-induced defense responses, but did not affect infection with the bacterial pathogen Pseudomonas syringae (PstDC3000). This result was confirmed using virus-induced gene silencing (VIGS) in tomato in conjunction with PstDC3000 infection. Overexpression of SlBIR3 in tomato (cv. micro-tom) and A. thaliana resulted in enhanced susceptibility to the necrotrophic fungus Botrytis cinerea. In addition, co-silencing SlBIR3 with SlSERK3A or SlSERK3B using VIGS and the tobacco rattle virus (TRV)-RNA2 vector containing fragments of both the SlSERK3 and SlBIR3 genes induced spontaneous cell death, indicating a cooperation between the two proteins in this process. In conclusion, our study revealed that SlBIR3 is the ortholog of AtBIR3 and that it participates in BR, PTI, and cell death signaling pathways.https://www.mdpi.com/1422-0067/18/9/1966tomatoSlBIR3BR signalingPTI responsesBotrytis cinereacell death |
| spellingShingle | Shuhua Huang Shuming Nie Shufen Wang Jianwei Liu Yanfeng Zhang Xiaofeng Wang SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato International Journal of Molecular Sciences tomato SlBIR3 BR signaling PTI responses Botrytis cinerea cell death |
| title | SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato |
| title_full | SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato |
| title_fullStr | SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato |
| title_full_unstemmed | SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato |
| title_short | SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato |
| title_sort | slbir3 negatively regulates pamp responses and cell death in tomato |
| topic | tomato SlBIR3 BR signaling PTI responses Botrytis cinerea cell death |
| url | https://www.mdpi.com/1422-0067/18/9/1966 |
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