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Title: Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor

Abstract

In the past decade, characterization of the host targets of pathogen virulence factors took a center stage in the study of pathogenesis and disease susceptibility in plants and humans. However, the impressive knowledge of host targets has not been broadly exploited to inhibit pathogen infection. In this paper, we show that host target modification could be a promising new approach to “protect” the disease-vulnerable components of plants. In particular, recent studies have identified the plant hormone jasmonate (JA) receptor as one of the common targets of virulence factors from highly evolved biotrophic/hemibiotrophic pathogens. Strains of the bacterial pathogen Pseudomonas syringae, for example, produce proteinaceous effectors, as well as a JA-mimicking toxin, coronatine (COR), to activate JA signaling as a mechanism to promote disease susceptibility. Guided by the crystal structure of the JA receptor and evolutionary clues, we succeeded in modifying the JA receptor to allow for sufficient endogenous JA signaling but greatly reduced sensitivity to COR. Transgenic Arabidopsis expressing this modified receptor not only are fertile and maintain a high level of insect defense, but also gain the ability to resist COR-producing pathogens Pseudomonas syringae pv. tomato and P. syringae pv. maculicola. Finally, our results provide a proof-of-concept demonstration thatmore » host target modification can be a promising new approach to prevent the virulence action of highly evolved pathogens.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [3];  [7];  [6];  [8];  [9]
  1. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Plant Biology, Michigan State University, East Lansing, MI 48824,
  2. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Biological Sciences, Western Michigan University, Kalamazoo, MI 49008,
  3. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
  4. Department of Chemistry, Michigan State University, East Lansing, MI 48824,
  5. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Botany, Aligarh Muslim University, Aligarh, 202002, India,
  6. Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany,
  7. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824,
  8. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824,
  9. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Plant Biology, Michigan State University, East Lansing, MI 48824,, Howard Hughes Medical Institute, Michigan State University, East Lansing, MI 48824
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1235190
Alternate Identifier(s):
OSTI ID: 1348905
Grant/Contract Number:  
DE FG02 91ER20021; FG02-91ER20021
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 46; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plant hormone; plant immunity; bacterial virulence; coronatine; jasmonate

Citation Formats

Zhang, Li, Yao, Jian, Withers, John, Xin, Xiu-Fang, Banerjee, Rahul, Fariduddin, Qazi, Nakamura, Yoko, Nomura, Kinya, Howe, Gregg A., Boland, Wilhelm, Yan, Honggao, and He, Sheng Yang. Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor. United States: N. p., 2015. Web. doi:10.1073/pnas.1510745112.
Zhang, Li, Yao, Jian, Withers, John, Xin, Xiu-Fang, Banerjee, Rahul, Fariduddin, Qazi, Nakamura, Yoko, Nomura, Kinya, Howe, Gregg A., Boland, Wilhelm, Yan, Honggao, & He, Sheng Yang. Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor. United States. https://doi.org/10.1073/pnas.1510745112
Zhang, Li, Yao, Jian, Withers, John, Xin, Xiu-Fang, Banerjee, Rahul, Fariduddin, Qazi, Nakamura, Yoko, Nomura, Kinya, Howe, Gregg A., Boland, Wilhelm, Yan, Honggao, and He, Sheng Yang. Mon . "Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor". United States. https://doi.org/10.1073/pnas.1510745112.
@article{osti_1235190,
title = {Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor},
author = {Zhang, Li and Yao, Jian and Withers, John and Xin, Xiu-Fang and Banerjee, Rahul and Fariduddin, Qazi and Nakamura, Yoko and Nomura, Kinya and Howe, Gregg A. and Boland, Wilhelm and Yan, Honggao and He, Sheng Yang},
abstractNote = {In the past decade, characterization of the host targets of pathogen virulence factors took a center stage in the study of pathogenesis and disease susceptibility in plants and humans. However, the impressive knowledge of host targets has not been broadly exploited to inhibit pathogen infection. In this paper, we show that host target modification could be a promising new approach to “protect” the disease-vulnerable components of plants. In particular, recent studies have identified the plant hormone jasmonate (JA) receptor as one of the common targets of virulence factors from highly evolved biotrophic/hemibiotrophic pathogens. Strains of the bacterial pathogen Pseudomonas syringae, for example, produce proteinaceous effectors, as well as a JA-mimicking toxin, coronatine (COR), to activate JA signaling as a mechanism to promote disease susceptibility. Guided by the crystal structure of the JA receptor and evolutionary clues, we succeeded in modifying the JA receptor to allow for sufficient endogenous JA signaling but greatly reduced sensitivity to COR. Transgenic Arabidopsis expressing this modified receptor not only are fertile and maintain a high level of insect defense, but also gain the ability to resist COR-producing pathogens Pseudomonas syringae pv. tomato and P. syringae pv. maculicola. Finally, our results provide a proof-of-concept demonstration that host target modification can be a promising new approach to prevent the virulence action of highly evolved pathogens.},
doi = {10.1073/pnas.1510745112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 46,
volume = 112,
place = {United States},
year = {Mon Nov 02 00:00:00 EST 2015},
month = {Mon Nov 02 00:00:00 EST 2015}
}

Journal Article:
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https://doi.org/10.1073/pnas.1510745112

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