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

Recognition of microbe-associated molecular patterns (MAMPs) is crucial for the plant's immune response. How this sophisticated perception system can be usefully deployed in roots, continuously exposed to microbes, remains a mystery. By analyzing MAMP receptor expression and response at cellular resolution in Arabidopsis, we observed that differentiated outer cell layers show low expression of pattern-recognition receptors (PRRs) and lack MAMP responsiveness. Yet, these cells can be gated to become responsive by neighbor cell damage. Laser ablation of small cell clusters strongly upregulates PRR expression in their vicinity, and elevated receptor expression is sufficient to induce responsiveness in non-responsive cells. Finally, localized damage also leads to immune responses to otherwise non-immunogenic, beneficial bacteria. Damage-gating is overridden by receptor overexpression, which antagonizes colonization. Our findings that cellular damage can "switch on" local immune responses helps to conceptualize how MAMP perception can be used despite the presence of microbial patterns in the soil.

Danger-associate peptide regulates root immunity in Arabidopsis.

Plant elicitor peptides (Peps) are recognized by two receptor-like kinases, PEPR1 and PEPR2, and trigger plant immunity responses and root growth inhibition. In this study, we reveal that the Pep-PEPR system triggers root immunity responses in Arabidopsis. Pep1 incubation initiated callose and lignin deposition in roots of wild type but not in that of pepr1 pepr2 mutant seedlings. The plasma membrane-associated kinase BIK1, which serves downstream of the Pep-PEPR signaling pathway, was essential for Pep1-induced root immunity responses. Interestingly, disruption of PEPR1/2-associated coreceptor BAK1 enhanced the deposition of both callose and lignin induced by Pep1 in roots. Ethylene and salicylic acid signaling are involved in Pep1-induced root immunity responses. Furthermore, we showed that the successful phytopathogen, P. syringae (DC3000) could effectively suppress Pep1-trigged root callose and lignin accumulation. These results demonstrated the endogenous Pep-triggered root immunity responses and pathogenic suppression of the Pep-PEPR signaling pathway.

A screening of inhibitors targeting the receptor kinase FERONIA reveals small molecules that enhance plant root immunity.

Receptor-like kinases (RLKs) constitute the largest receptor family involved in the regulation of plant immunity and growth, but small-molecule inhibitors that target RLKs to improve agronomic traits remain unexplored. The RLK member FERONIA (FER) negatively regulates plant resistance to certain soil-borne diseases that are difficult to control and cause huge losses in crop yields and economy. Here, we identified 33 highly effective FER kinase inhibitors from 1494 small molecules by monitoring FER autophosphorylation in vitro. Four representative inhibitors (reversine, cenisertib, staurosporine and lavendustin A) inhibited the kinase activity of FER and its homologues in several crops by targeting the conserved ATP pocket in the kinase structure. FER contributes to the physiological impact of representative inhibitors in plants. The treatment of roots with reversine, staurosporine and lavendustin A enhanced innate immunity in plant roots and thus alleviated soil-borne diseases in tobacco, tomato and rice without growth penalties. Consistently, RNA sequencing assays showed that lavendustin A and reversine exert profound impacts on immunity-related gene expression. Our results will set a new milestone in the development of the plant RLK kinase regulation theory and provide a novel strategy for the prevention and control of plant soil-borne diseases without growth penalties.

Uncoupling root hair formation and defence activation from growth inhibition in response to damage-associated Pep peptides in Arabidopsis thaliana.

In Arabidopsis thaliana, PROPEPs and their derived elicitor-active Pep epitopes provide damage-associated molecular patterns (DAMPs), which trigger defence responses through cell-surface receptors PEPR1 and PEPR2. In addition, Pep peptides induce root growth inhibition and root hair formation, however their relationships and coordinating mechanisms are poorly understood. Here, we reveal that Pep1-mediated root hair formation requires PEPR-associated kinases BAK1/BKK1 and BIK1/PBL1, ethylene, auxin and root hair differentiation regulators, in addition to PEPR2. Our analysis on 69 accessions unravels intraspecies variations in Pep1-induced root hair formation and growth inhibition. The absence of a positive correlation between the two traits suggests their separate regulation and diversification in natural populations of A. thaliana. Restricted PEPR2 expression to certain root tissues is sufficient to induce root hair formation and growth inhibition in response to Pep1, indicating the capacity of non-cell-autonomous receptor signalling in different root tissues. Of particular note, root hair cell-specific PEPR2 expression uncouples defence activation from root growth inhibition and root hair formation, suggesting a unique property of root hairs in root defence activation following Pep1 recognition.

Cell-type-specific transcriptomics reveals that root hairs and endodermal barriers play important roles in beneficial plant-rhizobacterium interactions.

Growth- and health-promoting bacteria can boost crop productivity in a sustainable way. Pseudomonas simiae WCS417 is such a bacterium that efficiently colonizes roots, modifies the architecture of the root system to increase its size, and induces systemic resistance to make plants more resistant to pests and pathogens. Our previous work suggested that WCS417-induced phenotypes are controlled by root cell-type-specific mechanisms. However, it remains unclear how WCS417 affects these mechanisms. In this study, we transcriptionally profiled five Arabidopsis thaliana root cell types following WCS417 colonization. We found that the cortex and endodermis have the most differentially expressed genes, even though they are not in direct contact with this epiphytic bacterium. Many of these genes are associated with reduced cell wall biogenesis, and mutant analysis suggests that this downregulation facilitates WCS417-driven root architectural changes. Furthermore, we observed elevated expression of suberin biosynthesis genes and increased deposition of suberin in the endodermis of WCS417-colonized roots. Using an endodermal barrier mutant, we showed the importance of endodermal barrier integrity for optimal plant-beneficial bacterium association. Comparison of the transcriptome profiles in the two epidermal cell types that are in direct contact with WCS417-trichoblasts that form root hairs and atrichoblasts that do not-implies a difference in potential for defense gene activation. While both cell types respond to WCS417, trichoblasts displayed both higher basal and WCS417-dependent activation of defense-related genes compared with atrichoblasts. This suggests that root hairs may activate root immunity, a hypothesis that is supported by differential immune responses in root hair mutants. Taken together, these results highlight the strength of cell-type-specific transcriptional profiling to uncover "masked" biological mechanisms underlying beneficial plant-microbe associations.

Root cap-derived cells and mucilage: a protective network at the root tip.

Root cap-derived cells and mucilage provide the first line of defense of the plant against soil microbial pathogens. These cells form a mucilaginous root extracellular trap (RET), which also harbors a range of molecules including exDNA and defensive peptides and proteins much like the neutrophil extracellular trap (NET) of mammalians. Plant RETs resemble mucus structures found in mammalian systems and are rich in arabinogalactan proteins that have similarities to highly glycosylated human mucins. Human mucus and mucins regulate the intestinal flora microbiome through recruiting certain species of microbes and it is plausible that the arabinogalactan protein-rich mucilage found in plant roots fulfills a similar function by attracting specific microbes to the rhizosphere. The role of RETs in root defense functioning is highlighted.

Plant Immunity Is Compartmentalized and Specialized in Roots.

Roots are important organs for plant survival. In recent years, clear differences between roots and shoots in their respective plant defense strategies have been highlighted. Some putative gene markers of defense responses usually used in leaves are less relevant in roots and are sometimes not even expressed. Immune responses in roots appear to be tissue-specific suggesting a compartmentalization of defense mechanisms in root systems. Furthermore, roots are able to activate specific defense mechanisms in response to various elicitors including Molecular/Pathogen Associated Molecular Patterns, (MAMPs/PAMPs), signal compounds (e.g., hormones) and plant defense activator (e.g., ß-aminobutyric acid, BABA). This review discusses recent findings in root defense mechanisms and illustrates the necessity to discover new root specific biomarkers. The development of new strategies to control root disease and improve crop quality will also be reviewed.