AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis
Abstract Background N-3-oxo-tetradecanoyl-L-homoserine lactone (oxo-C14-HSL) is one of the N-acyl homoserine lactones (AHL) that mediate quorum sensing in Gram-negative bacteria. In addition to bacterial communication, AHL are involved in interactions with eukaryotes. Short-chain AHL are easily take...
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| Format: | Article |
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BMC
2022-12-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01464-3 |
| _version_ | 1828170143870484480 |
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| author | Abhishek Shrestha Casandra Hernández-Reyes Maja Grimm Johannes Krumwiede Elke Stein Sebastian T. Schenk Adam Schikora |
| author_facet | Abhishek Shrestha Casandra Hernández-Reyes Maja Grimm Johannes Krumwiede Elke Stein Sebastian T. Schenk Adam Schikora |
| author_sort | Abhishek Shrestha |
| collection | DOAJ |
| description | Abstract Background N-3-oxo-tetradecanoyl-L-homoserine lactone (oxo-C14-HSL) is one of the N-acyl homoserine lactones (AHL) that mediate quorum sensing in Gram-negative bacteria. In addition to bacterial communication, AHL are involved in interactions with eukaryotes. Short-chain AHL are easily taken up by plants and transported over long distances. They promote root elongation and growth. Plants typically do not uptake hydrophobic long sidechain AHL such as oxo-C14-HSL, although they prime plants for enhanced resistance to biotic and abiotic stress. Many studies have focused on priming effects of oxo-C14-HSL for enhanced plant resistance to stress. However, specific plant factors mediating oxo-C14-HSL responses in plants remain unexplored. Here, we identify the Arabidopsis protein ALI1 as a mediator of oxo-C14-HSL-induced priming in plants. Results We compared oxo-C14-HSL-induced priming between wild-type Arabidopsis Col-0 and an oxo-C14-HSL insensitive mutant ali1. The function of the candidate protein ALI1 was assessed through biochemical, genetic, and physiological approaches to investigate if the loss of the ALI1 gene resulted in subsequent loss of AHL priming. Through different assays, including MAP kinase activity assay, gene expression and transcriptome analysis, and pathogenicity assays, we revealed a loss of AHL priming in ali1. This phenomenon was reverted by the reintroduction of ALI1 into ali1. We also investigated the interaction between ALI1 protein and oxo-C14-HSL using biochemical and biophysical assays. Although biophysical assays did not reveal an interaction between oxo-C14-HSL and ALI1, a pull-down assay and an indirect method employing biosensor E. coli LuxCDABE support such interaction. We expressed fluorescently tagged ALI1 in tobacco leaves to assess the localization of ALI1 and demonstrate that ALI1 colocalizes with the plasma membrane, tonoplast, and endoplasmic reticulum. Conclusions These results suggest that the candidate protein ALI1 is indispensable for oxo-C14-HSL-dependent priming for enhanced resistance in Arabidopsis and that the ALI1 protein may interact with oxo-C14-HSL. Furthermore, ALI1 protein is localized in the cell periphery. Our findings advance the understanding of interactions between plants and bacteria and provide an avenue to explore desired outcomes such as enhanced stress resistance, which is useful for sustainable crop protection. |
| first_indexed | 2024-04-12T03:03:54Z |
| format | Article |
| id | doaj.art-5c0d9744c65743b09a92cc17d1b929d8 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T03:03:54Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-5c0d9744c65743b09a92cc17d1b929d82022-12-22T03:50:33ZengBMCBMC Biology1741-70072022-12-0120111910.1186/s12915-022-01464-3AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in ArabidopsisAbhishek Shrestha0Casandra Hernández-Reyes1Maja Grimm2Johannes Krumwiede3Elke Stein4Sebastian T. Schenk5Adam Schikora6Julius Kühn Institute (JKI)—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsCell Biology, Faculty of Biology, University of FreiburgJulius Kühn Institute (JKI)—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsJulius Kühn Institute (JKI)—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsJustus Liebig University Giessen, Institute for Phytopathology,Cell Biology, Faculty of Biology, University of FreiburgJulius Kühn Institute (JKI)—Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsAbstract Background N-3-oxo-tetradecanoyl-L-homoserine lactone (oxo-C14-HSL) is one of the N-acyl homoserine lactones (AHL) that mediate quorum sensing in Gram-negative bacteria. In addition to bacterial communication, AHL are involved in interactions with eukaryotes. Short-chain AHL are easily taken up by plants and transported over long distances. They promote root elongation and growth. Plants typically do not uptake hydrophobic long sidechain AHL such as oxo-C14-HSL, although they prime plants for enhanced resistance to biotic and abiotic stress. Many studies have focused on priming effects of oxo-C14-HSL for enhanced plant resistance to stress. However, specific plant factors mediating oxo-C14-HSL responses in plants remain unexplored. Here, we identify the Arabidopsis protein ALI1 as a mediator of oxo-C14-HSL-induced priming in plants. Results We compared oxo-C14-HSL-induced priming between wild-type Arabidopsis Col-0 and an oxo-C14-HSL insensitive mutant ali1. The function of the candidate protein ALI1 was assessed through biochemical, genetic, and physiological approaches to investigate if the loss of the ALI1 gene resulted in subsequent loss of AHL priming. Through different assays, including MAP kinase activity assay, gene expression and transcriptome analysis, and pathogenicity assays, we revealed a loss of AHL priming in ali1. This phenomenon was reverted by the reintroduction of ALI1 into ali1. We also investigated the interaction between ALI1 protein and oxo-C14-HSL using biochemical and biophysical assays. Although biophysical assays did not reveal an interaction between oxo-C14-HSL and ALI1, a pull-down assay and an indirect method employing biosensor E. coli LuxCDABE support such interaction. We expressed fluorescently tagged ALI1 in tobacco leaves to assess the localization of ALI1 and demonstrate that ALI1 colocalizes with the plasma membrane, tonoplast, and endoplasmic reticulum. Conclusions These results suggest that the candidate protein ALI1 is indispensable for oxo-C14-HSL-dependent priming for enhanced resistance in Arabidopsis and that the ALI1 protein may interact with oxo-C14-HSL. Furthermore, ALI1 protein is localized in the cell periphery. Our findings advance the understanding of interactions between plants and bacteria and provide an avenue to explore desired outcomes such as enhanced stress resistance, which is useful for sustainable crop protection.https://doi.org/10.1186/s12915-022-01464-3AHL primingEnhanced resistanceN-acyl homoserine lactonePlant immunityPlant–microbe interactionQuorum sensing |
| spellingShingle | Abhishek Shrestha Casandra Hernández-Reyes Maja Grimm Johannes Krumwiede Elke Stein Sebastian T. Schenk Adam Schikora AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis BMC Biology AHL priming Enhanced resistance N-acyl homoserine lactone Plant immunity Plant–microbe interaction Quorum sensing |
| title | AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis |
| title_full | AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis |
| title_fullStr | AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis |
| title_full_unstemmed | AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis |
| title_short | AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis |
| title_sort | ahl priming protein 1 mediates n 3 oxo tetradecanoyl homoserine lactone priming in arabidopsis |
| topic | AHL priming Enhanced resistance N-acyl homoserine lactone Plant immunity Plant–microbe interaction Quorum sensing |
| url | https://doi.org/10.1186/s12915-022-01464-3 |
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