Spatially Restricted Immune Responses Are Required for Maintaining Root Meristematic Activity upon Detection of Bacteria

Emonet, Aurélia; Vacheron, Jordan; Heiman, Clara Margot; Tendon, Valérie Dénervaud; Ma, Ka‐Wai; Schulze‐Lefert, Paul; Keel, Christoph; Geldner, Niko

doi:10.1016/j.cub.2020.12.048

Cited by 54 publications

(47 citation statements)

References 86 publications

(129 reference statements)

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“…To facilitate the screening of individual root commensals of the At- RSPHERE culture collection, we took advantage of a flg22-hypersensitive line, pWER :: FLS2-GFP 25 , 26 , in which the flg22 receptor FLS2 is overexpressed but restricted to the root epidermis. This hypersensitivity leads to an enhanced signal-to-noise ratio for flg22-mediated RGI (Extended Data Fig.…”

Section: Resultsmentioning

confidence: 99%

Coordination of microbe–host homeostasis by crosstalk with plant innate immunity

et al. 2021

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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–defence trade-off. Here, we report that, in monoassociations, 41% (62 out of 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 bacterial 16S rRNA genes reveals that immune activation alters the profile of synthetic communities (SynComs) comprising RGI-non-suppressive strains, whereas 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. Furthermore, RGI-suppressive SynComs specifically downregulate a subset of immune-related genes. Precolonization of plants with RGI-suppressive SynComs, or mutation of one commensal-downregulated transcription factor, MYB15, renders the plants more susceptible to opportunistic Pseudomonas pathogens. Our results suggest that RGI-non-suppressive and RGI-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 defence-associated growth inhibition, ultimately leading to commensal–host homeostasis.

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Section: Resultsmentioning

confidence: 99%

Coordination of microbe–host homeostasis by crosstalk with plant innate immunity

et al. 2021

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“…Suberin plasticity in response to abiotic stresses such as drought, salt, waterlogging, or cadmium, while observed in roots in many species ( 20 , 47 – 49 ), only recently started to be characterized at the molecular level. This topic gained increasing interest in the past few years after observing that endodermal suberin is even more plastic than previously thought, and not only overproduced in toxic environments but also tightly modulated in response to mineral deficiencies ( 6 , 14 , 21 – 25 ), to Casparian strip defects ( 9 , 10 , 12 , 14 , 16 , 17 ), and during biotic interactions ( 25 – 28 ). In light of the plethora of signals controlling suberization, understanding the interaction between these pathways is critical.…”

Section: Discussionmentioning

confidence: 99%

“…Suberin, however, is not only regulated by endogenous developmental factors surveilling Casparian strip integrity. Pointing toward a very central role of suberin in plants’ adaptation to their environment, endodermal suberization is also highly regulated by nutrient availability and the hormones ethylene and abscisic acid (ABA) ( 6 , 14 , 20 – 25 ), as well as during biotic interactions ( 25 – 28 ). How suberin is regulated in response to developmental and exogenous clues remains poorly understood.…”

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confidence: 99%

Suberin plasticity to developmental and exogenous cues is regulated by a set of MYB transcription factors

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Cléard

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Suberin is a hydrophobic biopolymer that can be deposited at the periphery of cells, forming protective barriers against biotic and abiotic stress. In roots, suberin forms lamellae at the periphery of endodermal cells where it plays crucial roles in the control of water and mineral transport. Suberin formation is highly regulated by developmental and environmental cues. However, the mechanisms controlling its spatiotemporal regulation are poorly understood. Here, we show that endodermal suberin is regulated independently by developmental and exogenous signals to fine-tune suberin deposition in roots. We found a set of four MYB transcription factors (MYB41, MYB53, MYB92, and MYB93), each of which is individually regulated by these two signals and is sufficient to promote endodermal suberin. Mutation of these four transcription factors simultaneously through genome editing leads to a dramatic reduction in suberin formation in response to both developmental and environmental signals. Most suberin mutants analyzed at physiological levels are also affected in another endodermal barrier made of lignin (Casparian strips) through a compensatory mechanism. Through the functional analysis of these four MYBs, we generated plants allowing unbiased investigation of endodermal suberin function, without accounting for confounding effects due to Casparian strip defects, and were able to unravel specific roles of suberin in nutrient homeostasis.

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“…In this regard, plant signaling research has made important progress in recent years, and thus is poised for many exciting discoveries in the future. It will be particularly informative to examine PTI signaling at the network level, and map protein-protein interactions and kinase-substrate phosphorylation at a larger scale, as well as determine potential cell-or tissue-specific interactions/responses (Emonet et al, 2021). Recent progress has been made in identifying kinase substrates (Figure 4); however, the bulk of substrates for even well-characterized RLCKs are likely unknown.…”

Section: Discussionmentioning

confidence: 99%

Molecular mechanisms of early plant pattern-triggered immune signaling

2021

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Spatially Restricted Immune Responses Are Required for Maintaining Root Meristematic Activity upon Detection of Bacteria

Cited by 54 publications

References 86 publications

Coordination of microbe–host homeostasis by crosstalk with plant innate immunity

Coordination of microbe–host homeostasis by crosstalk with plant innate immunity

Suberin plasticity to developmental and exogenous cues is regulated by a set of MYB transcription factors

Molecular mechanisms of early plant pattern-triggered immune signaling

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