The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity
Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Journal Article |
| Language: | English |
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2020
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| Online Access: | https://hdl.handle.net/10356/145615 |
| _version_ | 1826120811509972992 |
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| author | Tran, Tuan Minh Ma, Zhiming Triebl, Alexander Nath, Sangeeta Cheng, Yingying Gong, Ben-Qiang Han, Xiao Wang, Junqi Li, Jian-Feng Wenk, Markus R. Torta, Federico Mayor, Satyajit Yang, Liang Miao, Yansong |
| author2 | School of Biological Sciences |
| author_facet | School of Biological Sciences Tran, Tuan Minh Ma, Zhiming Triebl, Alexander Nath, Sangeeta Cheng, Yingying Gong, Ben-Qiang Han, Xiao Wang, Junqi Li, Jian-Feng Wenk, Markus R. Torta, Federico Mayor, Satyajit Yang, Liang Miao, Yansong |
| author_sort | Tran, Tuan Minh |
| collection | NTU |
| description | Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern–triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern–triggered host immunity. |
| first_indexed | 2024-10-01T05:22:51Z |
| format | Journal Article |
| id | ntu-10356/145615 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T05:22:51Z |
| publishDate | 2020 |
| record_format | dspace |
| spelling | ntu-10356/1456152023-02-28T17:08:19Z The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity Tran, Tuan Minh Ma, Zhiming Triebl, Alexander Nath, Sangeeta Cheng, Yingying Gong, Ben-Qiang Han, Xiao Wang, Junqi Li, Jian-Feng Wenk, Markus R. Torta, Federico Mayor, Satyajit Yang, Liang Miao, Yansong School of Biological Sciences School of Chemical and Biomedical Engineering Singapore Centre for Environmental Life Sciences and Engineering (SCELSE) Science::Biological sciences Quorum Sensing Xanthomonas Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern–triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern–triggered host immunity. Nanyang Technological University Published version We are grateful to Kimberly Kline (Singapore Centre for Environmental Life Sciences Engineering, Singapore) for critical reading of the manuscript, Yuki Nakamura (Institute of Plant and Microbial Biology, Academia Sinica, Taiwan) for valuable discussion on the lipidomics data. We thank Lay Yin Tang and Alma Turšić-Wunder for helping in RNA preparation. We thank the following researchers for sharing the Arabidopsis seeds: Takashi Ueda (National Institute for Basic Biology, Japan) for the FLS2–GFP Arabidopsis, Jianwei Pan (Lanzhou University, China) for PIN2–GFP Arabidopsis, Liwen Jiang (Chinese University of Hongkong) for the VHAa1–GFP line, and Thomas Ott (University of Freiburg) for the pREM1.2::YFP:REM1.2 line; Kathrin Schrick (Kansas State University) and Jyan-Chyun Jang (Ohio State University) for the Arabidopsis sterol mutants; and Jinbo Shen (State Key Laboratory of Subtropical Silviculture, Zhejang A&F University, China) for the BOR1–GFP line. We also thank Yinyue Deng (South China Agricultural University, China) for sharing reagents; MK Mathew and Divya Rajagopal (National Centre for Biological Sciences-TIFR, India) for helping with Arabidopsis growth for the Homo-FRET experiments. S Mayor is supported by a Margdarshi Fellowship (IA/M/15/1/502018) from the Department of Biotechnology-Wellcome Trust Alliance. This study was supported by Nanyang Technological University NIMBELS grant (NIM/01/2016) and Nanyang Technological University startup grant (M4081533) to Y Miao in Singapore. 2020-12-30T03:33:49Z 2020-12-30T03:33:49Z 2020 Journal Article Tran, T. M., Ma, Z., Triebl, A., Nath, S., Cheng, Y., Gong, B.-Q., . . . Miao, Y. (2020). The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity. Life Science Alliance, 3(10), e202000720-. doi:10.26508/lsa.202000720 2575-1077 https://hdl.handle.net/10356/145615 10.26508/lsa.202000720 32788227 10 3 en NIM/01/2016 M4081533 Life Science Alliance © 2020 Tran et al. This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/). application/pdf |
| spellingShingle | Science::Biological sciences Quorum Sensing Xanthomonas Tran, Tuan Minh Ma, Zhiming Triebl, Alexander Nath, Sangeeta Cheng, Yingying Gong, Ben-Qiang Han, Xiao Wang, Junqi Li, Jian-Feng Wenk, Markus R. Torta, Federico Mayor, Satyajit Yang, Liang Miao, Yansong The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title | The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title_full | The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title_fullStr | The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title_full_unstemmed | The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title_short | The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| title_sort | bacterial quorum sensing signal dsf hijacks arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity |
| topic | Science::Biological sciences Quorum Sensing Xanthomonas |
| url | https://hdl.handle.net/10356/145615 |
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