TY - JOUR
T1 - Rhizosphere-associated Pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH
AU - Yu, Ke
AU - Liu, Yang
AU - Tichelaar, Ramon
AU - Savant, Niharika
AU - Lagendijk, Ellen
AU - van Kuijk, Sanne J L
AU - Stringlis, Ioannis A
AU - van Dijken, Anja J H
AU - Pieterse, Corné M J
AU - Bakker, Peter A H M
AU - Haney, Cara H
AU - Berendsen, Roeland L
N1 - Copyright © 2019 Elsevier Ltd. All rights reserved.
PY - 2019/11/18
Y1 - 2019/11/18
N2 - The root microbiome consists of commensal, pathogenic, and plant-beneficial microbes [1]. Most members of the root microbiome possess microbe-associated molecular patterns (MAMPs) similar to those of plant pathogens [2]. Their recognition can lead to the activation of host immunity and suppression of plant growth due to growth-defense tradeoffs [3, 4]. We found that 42% of the tested root microbiota, including the plant growth-promoting rhizobacteria Pseudomonas capeferrum WCS358 [5, 6] and Pseudomonas simiae WCS417 [6, 7], are able to quench local Arabidopsis thaliana root immune responses that are triggered by flg22 [8], an immunogenic epitope of the MAMP flagellin [9], suggesting that this is an important function of the root microbiome. In a screen for WCS358 mutants that lost their capacity to suppress flg22-induced CYP71A12pro:GUS MAMP-reporter gene expression, we identified the bacterial genes pqqF and cyoB in WCS358, which are required for the production of gluconic acid and its derivative 2-keto gluconic acid. Both WCS358 mutants are impaired in the production of these organic acids and consequently lowered their extracellular pH to a lesser extent than wild-type WCS358. Acidification of the plant growth medium similarly suppressed flg22-induced CYP71A12pro:GUS and MYB51pro:GUS expression, and the flg22-mediated oxidative burst, suggesting a role for rhizobacterial gluconic acid-mediated modulation of the extracellular pH in the suppression of root immunity. Rhizosphere population densities of the mutants were significantly reduced compared to wild-type. Collectively, these findings show that suppression of immune responses is an important function of the root microbiome, as it facilitates colonization by beneficial root microbiota.
AB - The root microbiome consists of commensal, pathogenic, and plant-beneficial microbes [1]. Most members of the root microbiome possess microbe-associated molecular patterns (MAMPs) similar to those of plant pathogens [2]. Their recognition can lead to the activation of host immunity and suppression of plant growth due to growth-defense tradeoffs [3, 4]. We found that 42% of the tested root microbiota, including the plant growth-promoting rhizobacteria Pseudomonas capeferrum WCS358 [5, 6] and Pseudomonas simiae WCS417 [6, 7], are able to quench local Arabidopsis thaliana root immune responses that are triggered by flg22 [8], an immunogenic epitope of the MAMP flagellin [9], suggesting that this is an important function of the root microbiome. In a screen for WCS358 mutants that lost their capacity to suppress flg22-induced CYP71A12pro:GUS MAMP-reporter gene expression, we identified the bacterial genes pqqF and cyoB in WCS358, which are required for the production of gluconic acid and its derivative 2-keto gluconic acid. Both WCS358 mutants are impaired in the production of these organic acids and consequently lowered their extracellular pH to a lesser extent than wild-type WCS358. Acidification of the plant growth medium similarly suppressed flg22-induced CYP71A12pro:GUS and MYB51pro:GUS expression, and the flg22-mediated oxidative burst, suggesting a role for rhizobacterial gluconic acid-mediated modulation of the extracellular pH in the suppression of root immunity. Rhizosphere population densities of the mutants were significantly reduced compared to wild-type. Collectively, these findings show that suppression of immune responses is an important function of the root microbiome, as it facilitates colonization by beneficial root microbiota.
KW - plant microbiome
KW - plant immunity
KW - beneficial microbes
KW - rhizosphere competence
KW - induced systemic resistance
KW - immune suppression
KW - gluconic acid
U2 - 10.1016/j.cub.2019.09.015
DO - 10.1016/j.cub.2019.09.015
M3 - Article
C2 - 31668625
SN - 0960-9822
VL - 29
SP - 3913
EP - 3920
JO - Current Biology
JF - Current Biology
ER -