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

Zhou, Feng; Emonet, Aurélia; Tendon, Valérie Dénervaud; Marhavý, Peter; Wu, Dousheng; Lahaye, Thomas; Geldner, Niko

doi:10.1016/j.cell.2020.01.013

Cited by 211 publications

(235 citation statements)

References 77 publications

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“…The observed redundancy of Fo effectors targeting the same process implied that interference with this process is a crucial element in host colonisation by this vascular pathogen. Intriguingly, a recent study revealed highly localised and damage-dependent activation of PTI in Arabidopsis roots (Zhou et al, 2020). Initial root surface colonisation by Fo is followed by its invasion of the xylem vessels that is likely to result in plant tissue damage and thus PTI activation, explaining the necessity for these PTI-suppressing effectors.…”

Section: Discussionmentioning

confidence: 99%

“…The concept of PTI and its suppression by intracellularly acting effectors is largely based on the study of foliar pathogens. Roots are exposed to both beneficial and pathogenic microbes, a condition that has likely shaped the immune system in roots (De Coninck et al, 2015;Hacquard et al, 2017;Zhou et al, 2020). Currently, it is poorly understood which type of defence responses are activated in roots, and whether root pathogens use similar mechanisms for their suppression as those employed in aboveground interactions.…”

Section: Introductionmentioning

confidence: 99%

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The root‐invading pathogen Fusarium oxysporum targets pattern‐triggered immunity using both cytoplasmic and apoplastic effectors

et al. 2020

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Plant pathogens use effector proteins to promote host colonisation. The mode of action of effectors from root-invading pathogens, such as Fusarium oxysporum (Fo), is poorly understood. Here, we investigated whether Fo effectors suppress pattern-triggered immunity (PTI), and whether they enter host cells during infection. Eight candidate effectors of an Arabidopsis-infecting Fo strain were expressed with and without signal peptide for secretion in Nicotiana benthamiana and their effect on flg22-triggered and chitin-triggered reactive oxidative species (ROS) burst was monitored. To detect uptake, effector biotinylation by an intracellular Arabidopsis-produced biotin ligase was examined following root infection. Four effectors suppressed PTI signalling; two acted intracellularly and two apoplastically. Heterologous expression of a PTI-suppressing effector in Arabidopsis enhanced bacterial susceptibility. Consistent with an intracellular activity, host cell uptake of five effectors, but not of the apoplastically acting ones, was detected in Fo-infected Arabidopsis roots. Multiple Fo effectors targeted PTI signalling, uncovering a surprising overlap in infection strategies between foliar and root pathogens. Extracellular targeting of flg22 signalling by a microbial effector provides a new mechanism on how plant pathogens manipulate their host. Effector translocation appears independent of protein size, charge, presence of conserved motifs or the promoter driving its expression.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The root‐invading pathogen Fusarium oxysporum targets pattern‐triggered immunity using both cytoplasmic and apoplastic effectors

et al. 2020

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“…3b). Recent work showed that MAMP responsiveness in germ-free roots was gated by the expression of damage-induced PRRs 35 . However, the sustained expression of FLS2 (c1) in the presence of SynComs indicates that RGI suppression is not due to FLS2 downregulation ( Fig.…”

Section: Root Transcriptomic Changes and Dampening Of Immunity By Supmentioning

confidence: 99%

Coordination of microbe-host homeostasis via a crosstalk with plant innate immunity

Schulze‐Lefert

Garrido‐Oter

et al. 2020

Preprint

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Asymptomatic plants grown in natural soil are colonized by phylogenetically structured communities of microbes known as the microbiota. Individual microbes can activate microbe-associated molecular pattern (MAMP)-triggered immunity (MTI), which limits pathogen proliferation but curtails plant growth, a phenomenon known as the growth-defense trade-off. We report that in mono-associations, 41% (62/151) of taxonomically diverse root bacterial commensals suppress Arabidopsis thaliana root growth inhibition (RGI) triggered by immune-stimulating MAMPs or damage-associated molecular patterns. Amplicon sequencing of bacteria 16S rRNA genes reveal that immune activation alters the profile of synthetic communities (SynComs) comprised of RGI-non-suppressive strains, while the presence of RGI-suppressive strains attenuates this effect. Root colonization by SynComs with different complexities and RGI-suppressive activities alters the expression of 174 core host genes with functions related to root development and nutrient transport. Further, RGI-suppressive SynComs specifically downregulate a subset of immune-related genes. Pre-colonization with RGI-suppressive SynComs, or mutation of one commensal-downregulated transcription factor, MYB15, render plants more susceptible to opportunistic Pseudomonas pathogens. Our results suggest that RGI-non-suppressive and suppressive root commensals modulate host susceptibility to pathogens by either eliciting or dampening MTI responses, respectively. This interplay buffers the plant immune system against pathogen perturbation and defense-associated growth inhibition, ultimately leading to commensal-host homeostasis.

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“…If pathogens can overcome preformed plant barriers (cuticle, cell wall) or even be sensed before [1], the so-called first line of defense is activated. Here, Pattern Recognition Receptors (PRRs) at the plasma membrane (PM) recognize conserved pathogen or microbial signatures (Pathogen-Associated Molecular Patterns (PAMPs)).…”

Section: Introductionmentioning

confidence: 99%

Plant Cells under Attack: Unconventional Endomembrane Trafficking during Plant Defense

Ruano

Scheuring

2020

Plants

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Since plants lack specialized immune cells, each cell has to defend itself independently against a plethora of different pathogens. Therefore, successful plant defense strongly relies on precise and efficient regulation of intracellular processes in every single cell. Smooth trafficking within the plant endomembrane is a prerequisite for a diverse set of immune responses. Pathogen recognition, signaling into the nucleus, cell wall enforcement, secretion of antimicrobial proteins and compounds, as well as generation of reactive oxygen species, all heavily depend on vesicle transport. In contrast, pathogens have developed a variety of different means to manipulate vesicle trafficking to prevent detection or to inhibit specific plant responses. Intriguingly, the plant endomembrane system exhibits remarkable plasticity upon pathogen attack. Unconventional trafficking pathways such as the formation of endoplasmic reticulum (ER) bodies or fusion of the vacuole with the plasma membrane are initiated and enforced as the counteraction. Here, we review the recent findings on unconventional and defense-induced trafficking pathways as the plant´s measures in response to pathogen attack. In addition, we describe the endomembrane system manipulations by different pathogens, with a focus on tethering and fusion events during vesicle trafficking.

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

Cited by 211 publications

References 77 publications

The root‐invading pathogen Fusarium oxysporum targets pattern‐triggered immunity using both cytoplasmic and apoplastic effectors

The root‐invading pathogen Fusarium oxysporum targets pattern‐triggered immunity using both cytoplasmic and apoplastic effectors

Coordination of microbe-host homeostasis via a crosstalk with plant innate immunity

Plant Cells under Attack: Unconventional Endomembrane Trafficking during Plant Defense

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