IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44724-2.html
   My bibliography  Save this article

Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS

Author

Listed:
  • Frederickson Entila

    (Huazhong Agricultural University
    Max Planck Institute for Plant Breeding Research)

  • Xiaowei Han

    (Huazhong Agricultural University
    Huazhong Agricultural University
    Chinese Academy of Agricultural Sciences)

  • Akira Mine

    (JST PRESTO
    Kyoto University)

  • Paul Schulze-Lefert

    (Max Planck Institute for Plant Breeding Research)

  • Kenichi Tsuda

    (Huazhong Agricultural University
    Max Planck Institute for Plant Breeding Research
    Huazhong Agricultural University
    Chinese Academy of Agricultural Sciences)

Abstract

Despite the plant health-promoting effects of plant microbiota, these assemblages also comprise potentially detrimental microbes. How plant immunity controls its microbiota to promote plant health under these conditions remains largely unknown. We find that commensal bacteria isolated from healthy Arabidopsis plants trigger diverse patterns of reactive oxygen species (ROS) production dependent on the immune receptors and completely on the NADPH oxidase RBOHD that selectively inhibited specific commensals, notably Xanthomonas L148. Through random mutagenesis, we find that L148 gspE, encoding a type II secretion system (T2SS) component, is required for the damaging effects of Xanthomonas L148 on rbohD mutant plants. In planta bacterial transcriptomics reveals that RBOHD suppresses most T2SS gene expression including gspE. L148 colonization protected plants against a bacterial pathogen, when gspE was inhibited by ROS or mutation. Thus, a negative feedback loop between Arabidopsis ROS and the bacterial T2SS tames a potentially detrimental leaf commensal and turns it into a microbe beneficial to the host.

Suggested Citation

  • Frederickson Entila & Xiaowei Han & Akira Mine & Paul Schulze-Lefert & Kenichi Tsuda, 2024. "Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44724-2
    DOI: 10.1038/s41467-024-44724-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44724-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44724-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yan Wang & Yuanpeng Xu & Yujing Sun & Huibin Wang & Jiaming Qi & Bowen Wan & Wenwu Ye & Yachun Lin & Yuanyuan Shao & Suomeng Dong & Brett M. Tyler & Yuanchao Wang, 2018. "Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    3. Xiu-Fang Xin & Kinya Nomura & Kyaw Aung & André C. Velásquez & Jian Yao & Freddy Boutrot & Jeff H. Chang & Cyril Zipfel & Sheng Yang He, 2016. "Bacteria establish an aqueous living space in plants crucial for virulence," Nature, Nature, vol. 539(7630), pages 524-529, November.
    4. Charrad, Malika & Ghazzali, Nadia & Boiteau, Véronique & Niknafs, Azam, 2014. "NbClust: An R Package for Determining the Relevant Number of Clusters in a Data Set," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 61(i06).
    5. Cyril Zipfel & Silke Robatzek & Lionel Navarro & Edward J. Oakeley & Jonathan D. G. Jones & Georg Felix & Thomas Boller, 2004. "Bacterial disease resistance in Arabidopsis through flagellin perception," Nature, Nature, vol. 428(6984), pages 764-767, April.
    6. Tao Chen & Kinya Nomura & Xiaolin Wang & Reza Sohrabi & Jin Xu & Lingya Yao & Bradley C. Paasch & Li Ma & James Kremer & Yuti Cheng & Li Zhang & Nian Wang & Ertao Wang & Xiu-Fang Xin & Sheng Yang He, 2020. "A plant genetic network for preventing dysbiosis in the phyllosphere," Nature, Nature, vol. 580(7805), pages 653-657, April.
    7. Struyf, Anja & Hubert, Mia & Rousseeuw, Peter, 1997. "Clustering in an Object-Oriented Environment," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 1(i04).
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Li Fan & Katja Fröhlich & Eric Melzer & Rory N. Pruitt & Isabell Albert & Lisha Zhang & Anna Joe & Chenlei Hua & Yanyue Song & Markus Albert & Sang-Tae Kim & Detlef Weigel & Cyril Zipfel & Eunyoung Ch, 2022. "Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Xin Zhou & Jinting Wang & Fang Liu & Junmin Liang & Peng Zhao & Clement K. M. Tsui & Lei Cai, 2022. "Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Mamoru Matsumura & Mika Nomoto & Tomotaka Itaya & Yuri Aratani & Mizuki Iwamoto & Takakazu Matsuura & Yuki Hayashi & Tsuyoshi Mori & Michael J. Skelly & Yoshiharu Y. Yamamoto & Toshinori Kinoshita & I, 2022. "Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Bolívar, Fernando & Duran, Miguel A. & Lozano-Vivas, Ana, 2023. "Bank business models, size, and profitability," Finance Research Letters, Elsevier, vol. 53(C).
    5. Reder, Maik & Yürüşen, Nurseda Y. & Melero, Julio J., 2018. "Data-driven learning framework for associating weather conditions and wind turbine failures," Reliability Engineering and System Safety, Elsevier, vol. 169(C), pages 554-569.
    6. Marcin Gąsior, 2021. "Environmental Attitudes and Willingness to Purchase Online—Classification Approach," Sustainability, MDPI, vol. 13(15), pages 1-17, August.
    7. Sayaka Matsui & Saki Noda & Keiko Kuwata & Mika Nomoto & Yasuomi Tada & Hidefumi Shinohara & Yoshikatsu Matsubayashi, 2024. "Arabidopsis SBT5.2 and SBT1.7 subtilases mediate C-terminal cleavage of flg22 epitope from bacterial flagellin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Jiahui Liu & Xiaoyun Wu & Yue Fang & Ye Liu & Esther Oreofe Bello & Yong Li & Ruyi Xiong & Yinzi Li & Zheng Qing Fu & Aiming Wang & Xiaofei Cheng, 2023. "A plant RNA virus inhibits NPR1 sumoylation and subverts NPR1-mediated plant immunity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Shikai La & Jiafan Li & Si Ma & Xingqun Liu & Lihong Gao & Yongqiang Tian, 2024. "Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Roopam Shukla & Ankit Agarwal & Kamna Sachdeva & Juergen Kurths & P. K. Joshi, 2019. "Climate change perception: an analysis of climate change and risk perceptions among farmer types of Indian Western Himalayas," Climatic Change, Springer, vol. 152(1), pages 103-119, January.
    11. Saemi Shin & Won Suck Yoon & Sang-Hoon Byeon, 2022. "Trends in Occupational Infectious Diseases in South Korea and Classification of Industries According to the Risk of Biological Hazards Using K-Means Clustering," IJERPH, MDPI, vol. 19(19), pages 1-19, September.
    12. Kauffmann, Albrecht, 2012. "Delineation of City Regions Based on Commuting Interrelations: The Example of Large Cities in Germany," IWH Discussion Papers 4/2012, Halle Institute for Economic Research (IWH).
    13. Song He & Xinyu Song & Xiaoxi Yang & Jijun Yu & Yuqi Wen & Lianlian Wu & Bowei Yan & Jiannan Feng & Xiaochen Bo, 2021. "COMSUC: A web server for the identification of consensus molecular subtypes of cancer based on multiple methods and multi-omics data," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-10, March.
    14. Du-Hwa Lee & Ho-Seok Lee & Min-Soo Choi & Katarzyna Parys & Kaori Honda & Yasumitsu Kondoh & Jung-Min Lee & Natalie Edelbacher & Geon Heo & Balaji Enugutti & Hiroyuki Osada & Ken Shirasu & Youssef Bel, 2024. "Reprogramming of flagellin receptor responses with surrogate ligands," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Jihane El Ouadi & Hanae Errousso & Nicolas Malhene & Siham Benhadou & Hicham Medromi, 2022. "A machine-learning based hybrid algorithm for strategic location of urban bundling hubs to support shared public transport," Quality & Quantity: International Journal of Methodology, Springer, vol. 56(5), pages 3215-3258, October.
    16. Cyril Atkinson-Clement & Eléonore Pigalle, 2021. "What can we learn from Covid-19 pandemic’s impact on human behaviour? The case of France’s lockdown," Palgrave Communications, Palgrave Macmillan, vol. 8(1), pages 1-12, December.
    17. Kreitmair, Ursula & Bower-Bir, Jacob, 2021. "Too different to solve climate change? Experimental evidence on the effects of production and benefit heterogeneity on collective action," Ecological Economics, Elsevier, vol. 184(C).
    18. Getaneh Addis Tessema & Jan van der Borg & Anton Van Rompaey & Steven Van Passel & Enyew Adgo & Amare Sewnet Minale & Kerebih Asrese & Amaury Frankl & Jean Poesen, 2022. "Benefit Segmentation of Tourists to Geosites and Its Implications for Sustainable Development of Geotourism in the Southern Lake Tana Region, Ethiopia," Sustainability, MDPI, vol. 14(6), pages 1-25, March.
    19. Wu, Tong & Rocha, Juan C. & Berry, Kevin & Chaigneau, Tomas & Hamann, Maike & Lindkvist, Emilie & Qiu, Jiangxiao & Schill, Caroline & Shepon, Alon & Crépin, Anne-Sophie & Folke, Carl, 2024. "Triple Bottom Line or Trilemma? Global Tradeoffs Between Prosperity, Inequality, and the Environment," World Development, Elsevier, vol. 178(C).
    20. Petricli, Gulcan & Inkaya, Tulin & Gokay Emel, Gul, 2024. "Identifying green citizen typologies by mining household-level survey data," Renewable and Sustainable Energy Reviews, Elsevier, vol. 189(PA).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44724-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.