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AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis

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...

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Autores principales: Shrestha, Abhishek, Hernández-Reyes, Casandra, Grimm, Maja, Krumwiede, Johannes, Stein, Elke, Schenk, Sebastian T., Schikora, Adam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721052/
https://www.ncbi.nlm.nih.gov/pubmed/36464707
http://dx.doi.org/10.1186/s12915-022-01464-3
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author Shrestha, Abhishek
Hernández-Reyes, Casandra
Grimm, Maja
Krumwiede, Johannes
Stein, Elke
Schenk, Sebastian T.
Schikora, Adam
author_facet Shrestha, Abhishek
Hernández-Reyes, Casandra
Grimm, Maja
Krumwiede, Johannes
Stein, Elke
Schenk, Sebastian T.
Schikora, Adam
author_sort Shrestha, Abhishek
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01464-3.
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spelling pubmed-97210522022-12-06 AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis Shrestha, Abhishek Hernández-Reyes, Casandra Grimm, Maja Krumwiede, Johannes Stein, Elke Schenk, Sebastian T. Schikora, Adam BMC Biol Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01464-3. BioMed Central 2022-12-05 /pmc/articles/PMC9721052/ /pubmed/36464707 http://dx.doi.org/10.1186/s12915-022-01464-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Shrestha, Abhishek
Hernández-Reyes, Casandra
Grimm, Maja
Krumwiede, Johannes
Stein, Elke
Schenk, Sebastian T.
Schikora, Adam
AHL-Priming Protein 1 mediates N-3-oxo-tetradecanoyl-homoserine lactone priming in Arabidopsis
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9721052/
https://www.ncbi.nlm.nih.gov/pubmed/36464707
http://dx.doi.org/10.1186/s12915-022-01464-3
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