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Title: Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis

Abstract

Environmental conditions profoundly affect plant disease development; however, the underlying molecular bases are not well understood. Here we show that elevated temperature significantly increases the susceptibility of Arabidopsis to Pseudomonas syringae pv. tomato (Pst) DC3000 independently of the phyB/PIF thermosensing pathway. Instead, elevated temperature promotes translocation of bacterial effector proteins into plant cells and causes a loss of ICS1-mediated salicylic acid (SA) biosynthesis. Global transcriptome analysis reveals a major temperature-sensitive node of SA signalling, impacting ~60% of benzothiadiazole (BTH)-regulated genes, including ICS1 and the canonical SA marker gene, PR1. Remarkably, BTH can effectively protect Arabidopsis against Pst DC3000 infection at elevated temperature despite the lack of ICS1 and PR1 expression. Our results highlight the broad impact of a major climate condition on the enigmatic molecular interplay between temperature, SA defence and function of a central bacterial virulence system in the context of a widely studied susceptible plant–pathogen interaction.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [3];  [4];  [5]; ORCiD logo [4]; ORCiD logo [6];  [7];  [8]
  1. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab., Cell and Molecular Biology Program, and Plant Resilience Institute
  2. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab. and Plant Resilience Institute
  3. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.
  4. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology and Center for Genomics Enabled Plant Science
  5. Western Michigan Univ., Kalamazoo MI (United States). Dept. of Biological Sciences
  6. Max Planck Inst. for Plant Breeding Research, Cologne (Germany)
  7. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab., Cell and Molecular Biology Program, Department of Biochemistry and Molecular Biology and Department of Microbiology and Molecular Genetics
  8. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab., Cell and Molecular Biology Program, Plant Resilience Institute, Dept. of Plant Biology, Department of Microbiology and Molecular Genetics, and Howard Hughes Medical Inst.
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1529931
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Huot, Bethany, Castroverde, Christian Danve M., Velásquez, André C., Hubbard, Emily, Pulman, Jane A., Yao, Jian, Childs, Kevin L., Tsuda, Kenichi, Montgomery, Beronda L., and He, Sheng Yang. Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01674-2.
Huot, Bethany, Castroverde, Christian Danve M., Velásquez, André C., Hubbard, Emily, Pulman, Jane A., Yao, Jian, Childs, Kevin L., Tsuda, Kenichi, Montgomery, Beronda L., & He, Sheng Yang. Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. United States. doi:10.1038/s41467-017-01674-2.
Huot, Bethany, Castroverde, Christian Danve M., Velásquez, André C., Hubbard, Emily, Pulman, Jane A., Yao, Jian, Childs, Kevin L., Tsuda, Kenichi, Montgomery, Beronda L., and He, Sheng Yang. Mon . "Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis". United States. doi:10.1038/s41467-017-01674-2. https://www.osti.gov/servlets/purl/1529931.
@article{osti_1529931,
title = {Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis},
author = {Huot, Bethany and Castroverde, Christian Danve M. and Velásquez, André C. and Hubbard, Emily and Pulman, Jane A. and Yao, Jian and Childs, Kevin L. and Tsuda, Kenichi and Montgomery, Beronda L. and He, Sheng Yang},
abstractNote = {Environmental conditions profoundly affect plant disease development; however, the underlying molecular bases are not well understood. Here we show that elevated temperature significantly increases the susceptibility of Arabidopsis to Pseudomonas syringae pv. tomato (Pst) DC3000 independently of the phyB/PIF thermosensing pathway. Instead, elevated temperature promotes translocation of bacterial effector proteins into plant cells and causes a loss of ICS1-mediated salicylic acid (SA) biosynthesis. Global transcriptome analysis reveals a major temperature-sensitive node of SA signalling, impacting ~60% of benzothiadiazole (BTH)-regulated genes, including ICS1 and the canonical SA marker gene, PR1. Remarkably, BTH can effectively protect Arabidopsis against Pst DC3000 infection at elevated temperature despite the lack of ICS1 and PR1 expression. Our results highlight the broad impact of a major climate condition on the enigmatic molecular interplay between temperature, SA defence and function of a central bacterial virulence system in the context of a widely studied susceptible plant–pathogen interaction.},
doi = {10.1038/s41467-017-01674-2},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {11}
}

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