<i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle

Plants harbor various beneficial bacteria that modulate their innate immunity, resulting in induced systemic resistance (ISR) against various pathogens. However, the immune mechanisms underlying ISR triggered by Bacillus spp. and Pseudomonas spp. against pathogens with different lifestyles are not y...

Full description

Bibliographic Details
Main Authors: Ngoc Huu Nguyen, Patricia Trotel-Aziz, Sandra Villaume, Fanja Rabenoelina, Adrian Schwarzenberg, Eric Nguema-Ona, Christophe Clément, Fabienne Baillieul, Aziz Aziz
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Vaccines
Subjects:
Online Access:https://www.mdpi.com/2076-393X/8/3/503
_version_ 1827706881905262592
author Ngoc Huu Nguyen
Patricia Trotel-Aziz
Sandra Villaume
Fanja Rabenoelina
Adrian Schwarzenberg
Eric Nguema-Ona
Christophe Clément
Fabienne Baillieul
Aziz Aziz
author_facet Ngoc Huu Nguyen
Patricia Trotel-Aziz
Sandra Villaume
Fanja Rabenoelina
Adrian Schwarzenberg
Eric Nguema-Ona
Christophe Clément
Fabienne Baillieul
Aziz Aziz
author_sort Ngoc Huu Nguyen
collection DOAJ
description Plants harbor various beneficial bacteria that modulate their innate immunity, resulting in induced systemic resistance (ISR) against various pathogens. However, the immune mechanisms underlying ISR triggered by Bacillus spp. and Pseudomonas spp. against pathogens with different lifestyles are not yet clearly elucidated. Here, we show that root drenching of Arabidopsis plants with <i>Pseudomonas fluorescens</i><span style="font-variant: small-caps;">PTA-CT</span>2 and <i>Bacillus subtilis</i> PTA-271 can induce ISR against the necrotrophic fungus <i>B. cinerea</i> and the hemibiotrophic bacterium <i>Pseudomonas syringae Pst</i> DC3000. In the absence of pathogen infection, both beneficial bacteria do not induce any consistent change in systemic immune responses. However, ISR relies on priming faster and robust expression of marker genes for the salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) signaling pathways upon pathogen challenge. These responses are also associated with increased levels of SA, JA, and abscisic acid (ABA) in the leaves of bacterized plants after infection. The functional study also points at priming of the JA/ET and NPR1-dependent defenses as prioritized immune pathways in ISR induced by both beneficial bacteria against <i>B. cinerea</i>. However, <i>B. subtilis</i>-triggered ISR against <i>Pst</i> DC3000 is dependent on SA, JA/ET, and NPR1 pathways, whereas <i>P. fluorescens</i>-induced ISR requires JA/ET and NPR1 signaling pathways. The use of ABA-insensitive mutants also pointed out the crucial role of ABA signaling, but not ABA concentration, along with JA/ET signaling in primed systemic immunity by beneficial bacteria against <i>Pst</i> DC3000, but not against <i>B. cinerea</i>. These results clearly indicate that ISR is linked to priming plants for enhanced common and distinct immune pathways depending on the beneficial strain and the pathogen lifestyle.
first_indexed 2024-03-10T16:34:00Z
format Article
id doaj.art-7996655327ff487fa3dc782991f01089
institution Directory Open Access Journal
issn 2076-393X
language English
last_indexed 2024-03-10T16:34:00Z
publishDate 2020-09-01
publisher MDPI AG
record_format Article
series Vaccines
spelling doaj.art-7996655327ff487fa3dc782991f010892023-11-20T12:35:18ZengMDPI AGVaccines2076-393X2020-09-018350310.3390/vaccines8030503<i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen LifestyleNgoc Huu Nguyen0Patricia Trotel-Aziz1Sandra Villaume2Fanja Rabenoelina3Adrian Schwarzenberg4Eric Nguema-Ona5Christophe Clément6Fabienne Baillieul7Aziz Aziz8Induced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceCentre Mondial de l’Innovation, Groupe Roullier, 35401 Saint-Malo, FranceCentre Mondial de l’Innovation, Groupe Roullier, 35401 Saint-Malo, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FranceInduced Resistance and Plant Bioprotection EA 4707, SFR Condorcet FR-CNRS 3417, UFR Sciences, Campus Moulin de la Housse, University of Reims, CEDEX 02, 51687 Reims, FrancePlants harbor various beneficial bacteria that modulate their innate immunity, resulting in induced systemic resistance (ISR) against various pathogens. However, the immune mechanisms underlying ISR triggered by Bacillus spp. and Pseudomonas spp. against pathogens with different lifestyles are not yet clearly elucidated. Here, we show that root drenching of Arabidopsis plants with <i>Pseudomonas fluorescens</i><span style="font-variant: small-caps;">PTA-CT</span>2 and <i>Bacillus subtilis</i> PTA-271 can induce ISR against the necrotrophic fungus <i>B. cinerea</i> and the hemibiotrophic bacterium <i>Pseudomonas syringae Pst</i> DC3000. In the absence of pathogen infection, both beneficial bacteria do not induce any consistent change in systemic immune responses. However, ISR relies on priming faster and robust expression of marker genes for the salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) signaling pathways upon pathogen challenge. These responses are also associated with increased levels of SA, JA, and abscisic acid (ABA) in the leaves of bacterized plants after infection. The functional study also points at priming of the JA/ET and NPR1-dependent defenses as prioritized immune pathways in ISR induced by both beneficial bacteria against <i>B. cinerea</i>. However, <i>B. subtilis</i>-triggered ISR against <i>Pst</i> DC3000 is dependent on SA, JA/ET, and NPR1 pathways, whereas <i>P. fluorescens</i>-induced ISR requires JA/ET and NPR1 signaling pathways. The use of ABA-insensitive mutants also pointed out the crucial role of ABA signaling, but not ABA concentration, along with JA/ET signaling in primed systemic immunity by beneficial bacteria against <i>Pst</i> DC3000, but not against <i>B. cinerea</i>. These results clearly indicate that ISR is linked to priming plants for enhanced common and distinct immune pathways depending on the beneficial strain and the pathogen lifestyle.https://www.mdpi.com/2076-393X/8/3/503<i>Arabidopsis</i><i>Bacillus subtilis</i>induced immunitypathogenspriming<i>Pseudomonas</i> <i>fluorescens</i>
spellingShingle Ngoc Huu Nguyen
Patricia Trotel-Aziz
Sandra Villaume
Fanja Rabenoelina
Adrian Schwarzenberg
Eric Nguema-Ona
Christophe Clément
Fabienne Baillieul
Aziz Aziz
<i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
Vaccines
<i>Arabidopsis</i>
<i>Bacillus subtilis</i>
induced immunity
pathogens
priming
<i>Pseudomonas</i> <i>fluorescens</i>
title <i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
title_full <i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
title_fullStr <i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
title_full_unstemmed <i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
title_short <i>Bacillus subtilis</i> and <i>Pseudomonas fluorescens</i> Trigger Common and Distinct Systemic Immune Responses in <i>Arabidopsis thaliana</i> Depending on the Pathogen Lifestyle
title_sort i bacillus subtilis i and i pseudomonas fluorescens i trigger common and distinct systemic immune responses in i arabidopsis thaliana i depending on the pathogen lifestyle
topic <i>Arabidopsis</i>
<i>Bacillus subtilis</i>
induced immunity
pathogens
priming
<i>Pseudomonas</i> <i>fluorescens</i>
url https://www.mdpi.com/2076-393X/8/3/503
work_keys_str_mv AT ngochuunguyen ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT patriciatrotelaziz ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT sandravillaume ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT fanjarabenoelina ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT adrianschwarzenberg ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT ericnguemaona ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT christopheclement ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT fabiennebaillieul ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle
AT azizaziz ibacillussubtilisiandipseudomonasfluorescensitriggercommonanddistinctsystemicimmuneresponsesiniarabidopsisthalianaidependingonthepathogenlifestyle