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Title: Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa

Abstract

Lipopolysaccharides (LPS) are among the known pathogen-associated molecular patterns (PAMPs). LPSs are potent elicitors of PAMP-triggered immunity (PTI), and bacteria have evolved intricate mechanisms to dampen PTI. Here we demonstrate that Xylella fastidiosa (Xf), a hemibiotrophic plant pathogenic bacterium, possesses a long chain O-antigen that enables it to delay initial plant recognition, thereby allowing it to effectively skirt initial elicitation of innate immunity and establish itself in the host. Lack of the O-antigen modifies plant perception of Xf and enables elicitation of hallmarks of PTI, such as ROS production specifically in the plant xylem tissue compartment, a tissue not traditionally considered a spatial location of PTI. To explore translational applications of our findings, we demonstrate that pre-treatment of plants with Xf LPS primes grapevine defenses to confer tolerance to Xf challenge.

Authors:
 [1];  [2]; ORCiD logo [3];  [4]; ORCiD logo [4];  [3];  [3];  [1]; ORCiD logo [4];  [1]
+ Show Author Affiliations
  1. Univ. of California, Riverside, CA (United States). Dept. of Microbiology and Plant Pathology
  2. Univ. of California, Davis, CA (United States). Dept. of Viticulture and Enology and Dept. of Plant Sciences
  3. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  4. Univ. of California, Davis, CA (United States). Dept. of Viticulture and Enology
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1523394
Grant/Contract Number:  
SC0015662
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Rapicavoli, Jeannette N., Blanco-Ulate, Barbara, Muszyński, Artur, Figueroa-Balderas, Rosa, Morales-Cruz, Abraham, Azadi, Parastoo, Dobruchowska, Justyna M., Castro, Claudia, Cantu, Dario, and Roper, M. Caroline. Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa. United States: N. p., 2018. Web. doi:10.1038/s41467-018-02861-5.
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Rapicavoli, Jeannette N., Blanco-Ulate, Barbara, Muszyński, Artur, Figueroa-Balderas, Rosa, Morales-Cruz, Abraham, Azadi, Parastoo, Dobruchowska, Justyna M., Castro, Claudia, Cantu, Dario, & Roper, M. Caroline. Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa. United States. https://doi.org/10.1038/s41467-018-02861-5
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Rapicavoli, Jeannette N., Blanco-Ulate, Barbara, Muszyński, Artur, Figueroa-Balderas, Rosa, Morales-Cruz, Abraham, Azadi, Parastoo, Dobruchowska, Justyna M., Castro, Claudia, Cantu, Dario, and Roper, M. Caroline. Fri . "Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa". United States. https://doi.org/10.1038/s41467-018-02861-5. https://www.osti.gov/servlets/purl/1523394.
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@article{osti_1523394,
title = {Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa},
author = {Rapicavoli, Jeannette N. and Blanco-Ulate, Barbara and Muszyński, Artur and Figueroa-Balderas, Rosa and Morales-Cruz, Abraham and Azadi, Parastoo and Dobruchowska, Justyna M. and Castro, Claudia and Cantu, Dario and Roper, M. Caroline},
abstractNote = {Lipopolysaccharides (LPS) are among the known pathogen-associated molecular patterns (PAMPs). LPSs are potent elicitors of PAMP-triggered immunity (PTI), and bacteria have evolved intricate mechanisms to dampen PTI. Here we demonstrate that Xylella fastidiosa (Xf), a hemibiotrophic plant pathogenic bacterium, possesses a long chain O-antigen that enables it to delay initial plant recognition, thereby allowing it to effectively skirt initial elicitation of innate immunity and establish itself in the host. Lack of the O-antigen modifies plant perception of Xf and enables elicitation of hallmarks of PTI, such as ROS production specifically in the plant xylem tissue compartment, a tissue not traditionally considered a spatial location of PTI. To explore translational applications of our findings, we demonstrate that pre-treatment of plants with Xf LPS primes grapevine defenses to confer tolerance to Xf challenge.},
doi = {10.1038/s41467-018-02861-5},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Fri Jan 26 00:00:00 EST 2018},
month = {Fri Jan 26 00:00:00 EST 2018}
}
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https://doi.org/10.1038/s41467-018-02861-5
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Figures / Tables:

Fig. 1 Fig. 1: O-antigen-modulated ROS production by extracted LPS and intact bacterial cells ex vivo. Discs of V. vinifera ‘Cabernet Sauvignon’ leaves were treated with 20 μL of a 50 μg/mL solution of purified LPS elicitors (either wzy or wild type LPS) equal to a final amount of 10 μg (basedmore » on Kdo content) of LPS, 20 μL of a 108 CFU/mL suspension of X&#402; wild type or wzy cells, or diH20 or 1× PBS-inoculated controls, respectively. a The amplitude of ROS production remained similar for both wild type and wzy LPS, reaching max production at ~4min, and plateaued starting around 30 min. b Total ROS production is reported as area under the curve (AUC) for plot of luminescence intensity over time. Total ROS production was not significantly different between discs treated with wild type or wzy extracted LPS. c Intact wzy cells induced a significantly stronger oxidative burst that persisted nearly 20 min longer than leaves inoculated with wild type bacteria (which contained fully polymerized O-antigens). Graphs represent the mean of 24 replicates per treatment ± standard error of the mean. d Total ROS production is reported as area under the curve (AUC) for plot of luminescence intensity over time. Discs treated with wzy cells produced significantly more ROS than discs treated with wild type cells. Graphs represent the mean of 24 replicates per treatment ± standard error of the mean. Treatments with different letters over the bars are statistically different (P < 0.05, Mann–Whitney U test, n = 24 per treatment)« less
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