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

• Published in: Current biology Vol. 31; no. 5; pp. 1012 - 1028.e7
• Main Authors: Emonet, Aurélia, Zhou, Feng, Vacheron, Jordan, Heiman, Clara Margot, Dénervaud Tendon, Valérie, Ma, Ka-Wai, Schulze-Lefert, Paul, Keel, Christoph, Geldner, Niko
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 08.03.2021
• Subjects: Arabidopsis; Arabidopsis Proteins; Bacteria - immunology; cell-specific response; commensal bacteria; flagellin; lignin; meristem; Meristem - immunology; Meristem - microbiology; microbe-associated molecular pattern; pattern recognition receptor; Plant Immunity; Plants - immunology; Plants - microbiology; Protein Kinases; root immune response; root immune response; meristem; microbe-associated molecular pattern; cell-specific response; Arabidopsis; flagellin; lignin; commensal bacteria; pattern recognition receptor
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.12.048

Plants restrict immune responses to vulnerable root parts. Spatially restricted responses are thought to be necessary to avoid constitutive responses to rhizosphere microbiota. To directly demonstrate the importance of spatially restricted responses, we expressed the plant flagellin receptor (FLS2) in different tissues, combined with fluorescent defense markers for immune readouts at cellular resolution. Our analysis distinguishes responses appearing cell autonomous from apparently non-cell-autonomous responses. It reveals lignification as a general immune response, contrasting suberization. Importantly, our analysis divides the root meristem into a central zone refractory to FLS2 expression and a cortex that is sensitized by FLS2 expression, causing meristem collapse upon stimulation. Meristematic epidermal expression generates super-competent lines that detect native bacterial flagellin and bypass the weak or absent response to commensals, providing a powerful tool for studying root immunity. Our manipulations and readouts demonstrate incompatibility of meristematic activity and defense and the importance of cell-resolved studies of plant immune responses. [Display omitted] •Cell-specific expression of an immune receptor reveals general and specific responses•Immune signaling appears to separate into autonomous and non-autonomous branches•Immune response in some meristem cells causes meristem collapse and growth arrest•Mis-localized immune perception interferes with accommodation of commensal bacteria By installing immune responsiveness specifically in peripheral root meristem cells, Emonet et al. generate hyperresponsive plants, showing flagellin-dependent root collapse and growth inhibition by commensal bacteria. This highlights the relevance of spatially resolved immune responses and their importance for bacterial accommodation by roots.