Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH

Yu, Ke; Liu, Yang; Tichelaar, Ramon; Savant, Niharika; Lagendijk, Ellen; Kuijk, Sanne J.L. van; Stringlis, Ioannis A.; Dijken, Anja J.H. Van; Pieterse, Corné M. J.; Bakker, Peter A. H. M.; Haney, Cara H.; Berendsen, Roeland L.

doi:10.1016/j.cub.2019.09.015

Cited by 134 publications

(107 citation statements)

References 53 publications

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“…SR80 inoculation tends to suppress the expression of PR-related defense genes in wheat shoots without Fp presence in soils. Consistent with this finding, suppression of the plant root immunity by non-pathogenic Pseudomonas species has recently been observed in Arabidopsis thaliana, which may have facilitated the bacterial colonization on roots (Yu et al, 2019). These suggest that quenching plant immune responses is an emerging strategy for plant-associated bacteria to prevent constitutive activation of plant immune responses.…”

Section: Sr80 Intimately Interacts With Plant Immune Systems and Medisupporting

confidence: 66%

Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogen

Liu

Cavalhais

et al. 2020

Preprint

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SummaryEmerging experimental framework suggests that plants under biotic stress may actively seek help from soil microbes, but empirical evidence underlying such a ‘cry for help’ strategy is limited.We used integrated microbial community profiling, pathogen and plant transcriptive gene quantification and culture-based methods to systematically investigate a three-way interaction between the wheat plant, wheat-associated microbiomes and Fusarium pseudograminearum (Fp).A clear enrichment of a dominant bacterium, Stenotrophomonas rhizophila (SR80), was observed in both the rhizosphere and root endosphere of Fp-infected wheat. SR80 reached 3.7×107 cells g-1 in the rhizosphere and accounted for up to 11.4% of the microbes in the root endosphere. Its abundance had a positive linear correlation with the pathogen load at base stems and expression of multiple defense genes in top leaves. Upon re-introduction in soils, SR80 enhanced plant growth, both the below- and above-ground, and induced strong disease resistance by priming plant defense in the aboveground plant parts, but only when the pathogen was presentTogether, the bacterium SR80 seems to have acted as an early warning system for plant defense. This work provides novel evidence for the potential protection of plants against pathogens by an enriched beneficial microbe via modulation of the plant immune system.

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Section: Sr80 Intimately Interacts With Plant Immune Systems and Medisupporting

confidence: 66%

Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogen

Liu

Cavalhais

et al. 2020

Preprint

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“…During colonization of plant roots, beneficial Pseudomonas spp. both suppress 45,46 and induce 23 distinct subsets of defence-related genes indicating that beneficial microbes can induce and suppress PTI. To test whether L. bicolor induces PTI, Arabidopsis seedlings were treated with live and heat-killed L. bicolor and MAP Kinase phosphorylation was used as a readout for PTI.…”

Section: Resultsmentioning

confidence: 99%

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Vishwanathan

Zienkiewicz²,

Liu

et al. 2019

Preprint

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20Below-ground microbes can induce systemic resistance (ISR) against foliar pests and 21 pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems 22 raises the question of host specificity in microbial induction of ISR. To test whether ISR is 23 limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus 24 Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation 25 with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic 26 susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 27 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid 28 (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. 29 bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the 30 chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. 31Collectively our findings suggest that some ISR responses might not require intimate co-32 evolution of host and microbe, but rather might be the result of root perception of conserved 33 microbial signals. 34 35 Plants associate with complex communities of microorganisms. Interplay of host and 36 microbial genotype determine whether the outcome of specific plant-microbe interactions is 37 beneficial or detrimental to plant health 1-3 . Plants possess receptors to sense potential 38 pathogens including transmembrane pattern-recognition receptors that recognize conserved 39 microbe-associated molecular patterns (MAMPs), and intracellular receptors that directly or 40 indirectly recognize effectors to help limit pathogen growth 4,5 . MAMP perception by plant 41 receptors triggers pattern-triggered immunity (PTI) responses including a reactive oxygen 42 species (ROS) burst, Mitogen-Activated Protein Kinase (MAPK) signaling, ion influx and 43 callose deposition 6-9 . In addition to local immune mechanisms, root-associated microbes can 44 induce systemic resistance (ISR) against a diverse spectrum of above-ground threats 2,10 . While 45 the mechanisms by which plants perceive MAMPs and effectors are well understood, there is 46 a more limited understanding of the mechanisms by which plant perceive the microbes that 47 trigger ISR. 48 In response to perception of microbes or pathogens, plants activate systemic defense 49 mechanisms including commensal-triggered ISR and pathogen-triggered systemic acquired 50 resistance (SAR) 11,12 . While both SAR and ISR confer resistance to pests and pathogens, they 51 promote resistance through distinct mechanisms 2 . SAR occurs upon local perception of a 52 pathogen, MAMP, or effector and results in systemic induction of SA-dependent gene 53 expression and accumulation of secondary metabolites 13,14 . Unlike SAR, ISR is associated with 54 small or no changes in systemic gene expression and phytohormone levels 15,16 . Additionally, 55while SAR is dependent...

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“…One important function that promotes colonization is thought to be the ability of some bacteria to suppress MAMP responses, thus avoiding production of anti-microbial compounds and inhibition of root growth. Suppression of MAMP perception by non-pathogenic colonizers has been reported, but is just starting to be understood in mechanistic terms (Garrido-Oter et al, 2018;Pel and Pieterse, 2013;Yu et al, 2019). Type III secretion system (T3SS) effectors are known to suppress MAMP perception (Chisholm et al, 2006), yet appear to be associated with a pathogenic (or symbiotic) life-style, with commensal/beneficial bacteria either not possessing a T3SS or containing only few recognizable T3SS proteins whose functions remain enigmatic (Loper et al, 2012;Stringlis et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…This is especially apparent in the microbe-rich soil environment of roots, whose outer cell layers do not possess protective barriers comparable to leaves. Recent breakthroughs in root microbiome research have heightened the interest in understanding how constitutive activation of PRRs by non-pathogenic microbes is avoided, while maintaining their effectiveness in defense Finkel et al, 2017;Garrido-Oter et al, 2018;Yu et al, 2019). The molecular outlines of microbe-associated molecular pattern (MAMP) perception were characterized in systems allowing for quantitative, time-resolved measurements of early responses .…”

Section: Introductionmentioning

confidence: 99%

Co-incidence of Damage and Microbial Patterns Controls Localized Immune Responses in Roots

Zhou

Emonet

Tendon

et al. 2020

Cell

208

200

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Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH

Abstract: Highlights d 42% of the tested root microbiota are able to quench local root immune responses d Beneficial Pseudomonas can suppress root immunity by lowering environmental pH d Suppression of immunity facilitates root colonization by these beneficial microbes

Cited by 134 publications

References 53 publications

Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogen

Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogen

Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Co-incidence of Damage and Microbial Patterns Controls Localized Immune Responses in Roots

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