The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus
The NLR (nucleotide-binding leucine-rich repeat) class immune receptor Sw-5b confers resistance to Tomato spotted wilt orthotospovirus (TSWV). Although Sw-5b is known to activate immunity upon recognition of the TSWV movement protein NSm, we know very little about the downstream events that lead to...
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2023-11-01
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| Series: | Molecular Plant-Microbe Interactions |
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| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-03-23-0032-R |
| _version_ | 1797435720837627904 |
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| author | Norma A. Ordaz Ugrappa Nagalakshmi Leonardo S. Boiteux Hagop S. Atamian Diane E. Ullman Savithramma P. Dinesh-Kumar |
| author_facet | Norma A. Ordaz Ugrappa Nagalakshmi Leonardo S. Boiteux Hagop S. Atamian Diane E. Ullman Savithramma P. Dinesh-Kumar |
| author_sort | Norma A. Ordaz |
| collection | DOAJ |
| description | The NLR (nucleotide-binding leucine-rich repeat) class immune receptor Sw-5b confers resistance to Tomato spotted wilt orthotospovirus (TSWV). Although Sw-5b is known to activate immunity upon recognition of the TSWV movement protein NSm, we know very little about the downstream events that lead to resistance. Here, we investigated the Sw-5b–mediated early transcriptomic changes that occur in response to mechanical and thrips-mediated inoculation of TSWV, using near-isogenic tomato lines CNPH-LAM 147 (Sw5b+/+) and Santa Clara (Sw-5b−/−). We observed earlier Sw-5b–mediated transcriptional changes in response to thrips-mediated inoculation compared with that in response to mechanical inoculation of TSWV. With thrips-mediated inoculation, differentially expressed genes (DEGs) were observed at 12, 24, and 72 h postinoculation (hpi). Whereas with mechanical inoculation, DEGs were observed only at 72 hpi. Although some DEGs were shared between the two methods of inoculation, many DEGs were specific to either thrips-mediated or mechanical inoculation of TSWV. In response to thrips-mediated inoculation, an NLR immune receptor, cysteine-rich receptor-like kinase, G-type lectin S-receptor-like kinases, the ethylene response factor 1, and the calmodulin-binding protein 60 were induced. Fatty acid desaturase 2-9, cell death genes, DCL2b, RIPK/PBL14-like, ERF017, and WRKY75 were differentially expressed in response to mechanical inoculation. Our findings reveal Sw-5b responses specific to the method of TSWV inoculation. Although TSWV is transmitted in nature primarily by the thrips, Sw-5b responses to thrips inoculation have not been previously studied. Therefore, the DEGs we have identified in response to thrips-mediated inoculation provide a new foundation for understanding the mechanistic roles of these genes in the Sw-5b–mediated resistance. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-03-09T10:51:21Z |
| format | Article |
| id | doaj.art-5732721c668b45f0977ab69c587b0433 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-03-09T10:51:21Z |
| publishDate | 2023-11-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-5732721c668b45f0977ab69c587b04332023-12-01T06:06:27ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062023-11-01361170571510.1094/MPMI-03-23-0032-RThe Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirusNorma A. Ordaz0Ugrappa Nagalakshmi1Leonardo S. Boiteux2Hagop S. Atamian3Diane E. Ullman4Savithramma P. Dinesh-Kumar5Department of Plant Pathology, College of Agricultural and Environmental Sciences, University of California, Davis, CA 95616, U.S.A.Department of Plant Biology, College of Biological Sciences, University of California, Davis, CA 95616, U.S.A.National Center for Vegetable Crops Research (CNPH), Embrapa Hortaliças, Brasilia–DF, BrazilBiological Sciences program, Schmid College of Science & Technology, Chapman University, Orange, CA 92866, U.S.A.Department of Entomology and Nematology, College of Agricultural and Environmental Sciences, University of California, Davis, CA 95616, U.S.A.Department of Plant Biology, College of Biological Sciences, University of California, Davis, CA 95616, U.S.A.The NLR (nucleotide-binding leucine-rich repeat) class immune receptor Sw-5b confers resistance to Tomato spotted wilt orthotospovirus (TSWV). Although Sw-5b is known to activate immunity upon recognition of the TSWV movement protein NSm, we know very little about the downstream events that lead to resistance. Here, we investigated the Sw-5b–mediated early transcriptomic changes that occur in response to mechanical and thrips-mediated inoculation of TSWV, using near-isogenic tomato lines CNPH-LAM 147 (Sw5b+/+) and Santa Clara (Sw-5b−/−). We observed earlier Sw-5b–mediated transcriptional changes in response to thrips-mediated inoculation compared with that in response to mechanical inoculation of TSWV. With thrips-mediated inoculation, differentially expressed genes (DEGs) were observed at 12, 24, and 72 h postinoculation (hpi). Whereas with mechanical inoculation, DEGs were observed only at 72 hpi. Although some DEGs were shared between the two methods of inoculation, many DEGs were specific to either thrips-mediated or mechanical inoculation of TSWV. In response to thrips-mediated inoculation, an NLR immune receptor, cysteine-rich receptor-like kinase, G-type lectin S-receptor-like kinases, the ethylene response factor 1, and the calmodulin-binding protein 60 were induced. Fatty acid desaturase 2-9, cell death genes, DCL2b, RIPK/PBL14-like, ERF017, and WRKY75 were differentially expressed in response to mechanical inoculation. Our findings reveal Sw-5b responses specific to the method of TSWV inoculation. Although TSWV is transmitted in nature primarily by the thrips, Sw-5b responses to thrips inoculation have not been previously studied. Therefore, the DEGs we have identified in response to thrips-mediated inoculation provide a new foundation for understanding the mechanistic roles of these genes in the Sw-5b–mediated resistance. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-03-23-0032-Rdifferentially expressed genesNLR immune receptorRNA-seqSw-5btomatoTomato spotted wilt orthotospovirus (TSWV) |
| spellingShingle | Norma A. Ordaz Ugrappa Nagalakshmi Leonardo S. Boiteux Hagop S. Atamian Diane E. Ullman Savithramma P. Dinesh-Kumar The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus Molecular Plant-Microbe Interactions differentially expressed genes NLR immune receptor RNA-seq Sw-5b tomato Tomato spotted wilt orthotospovirus (TSWV) |
| title | The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus |
| title_full | The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus |
| title_fullStr | The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus |
| title_full_unstemmed | The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus |
| title_short | The Sw-5b NLR Immune Receptor Induces Early Transcriptional Changes in Response to Thrips and Mechanical Modes of Inoculation of Tomato spotted wilt orthotospovirus |
| title_sort | sw 5b nlr immune receptor induces early transcriptional changes in response to thrips and mechanical modes of inoculation of tomato spotted wilt orthotospovirus |
| topic | differentially expressed genes NLR immune receptor RNA-seq Sw-5b tomato Tomato spotted wilt orthotospovirus (TSWV) |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-03-23-0032-R |
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