Evolutionary “hide and seek” between bacterial flagellin and the plant immune system

Bacterial flagellin is a potent host immune activator. Parys et al., 2021Parys K. Colaianni N.R. Lee H.-K. Hohmann U. Edelbacher N. Trgovcevic A. Blahovska Z. D. Mechtler Muhari-Portik al.Signatures of antagonistic pleiotropy in bacterial epitope.Cell Host Microbe. 2021; 29 (this issue): 620-634Google Scholar and 2021Colaianni H.-S. Conway J.M. Kim N.H. Mucyn T.S. Madalinski M. Law T.F. Jones C.D. al.A complex response to epitope variation commensal communities.Cell 635-649Abstract Full Text PDF PubMed Scopus (16) Google dissected effects variants on detection motility. They report this issue Cell & Microbe that Arabidopsis-associated microbiota differentially evolved flg22 allow tunability between motility defense activation. Plants are sessile organisms interact fixed position with plethora microorganisms their roots leaves. These plant-associated termed plant microbiota, while collective genomes functional repertoire referred as the microbiome (Trivedi 2020Trivedi P. Leach J.E. Tringe S.G. Sa T. Singh B.K. Plant-microbiome interactions: from community assembly health.Nat. Rev. Microbiol. 2020; 18: 607-621https://doi.org/10.1038/s41579-020-0412-1Crossref (308) Scholar). members can cause devastating diseases, but majority have lifestyle or even provide life-supporting benefits by promoting growth, enhancing nutrient uptake, stimulating plant’s system (Pascale 2020Pascale Proietti S. Pantelides I.S. Stringlis I.A. Modulation root molecules: The basis for targeted disease suppression growth promotion.Front. Plant Sci. 10: 1741https://doi.org/10.3389/fpls.2019.01741Crossref (129) dominated phyla Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, Acidobacteria. Their relative abundances vary greatly, depending soil type, species, compartment actively select microbial partners via exudation primary secondary metabolites activating specific defenses From side, evade responses, tolerate plant-released antimicrobial compounds, competitively colonize nutrient-rich niches (Yu 2019aYu Pieterse C.M.J. Bakker P.A.H.M. Berendsen R.L. Beneficial microbes going underground immunity.Plant Environ. 2019; 42: 2860-2870https://doi.org/10.1111/pce.13632Crossref (61) This balancing act at both side represents one top questions plant-microbe interactions research: how do plants engage beneficial, bacteria, warding off pathogenic ones? In two elegant tour-de-force studies Belkhadir Dangl groups, sought an answer question dissecting co-evolutionary principles receptor FLAGELLIN SENSING 2 (FLS2). Flagellin building block flagellum, locomotory organ almost all flagellated bacteria. As such, essential motility, fundamental function needed colonization pathogens symbionts alike (Raina 2019Raina J.B. Fernandez V. Lambert B. Stocker R. Seymour J.R. role chemotaxis symbiosis.Nat. 17: 284-294https://doi.org/10.1038/s41579-019-0182-9Crossref (71) At same time, ubiquitous microbe-associated molecular pattern (MAMP) be recognized its cognate FLS2 (Couto Zipfel, 2016Couto Zipfel C. Regulation recognition signalling plants.Nat. Immunol. 2016; 16: 537-552https://doi.org/10.1038/nri.2016.77Crossref (516) detects beneficial bacteria 22-amino-acid (Stringlis 2018Stringlis Hickman Van Verk M.C. Zamioudis Root transcriptional dynamics induced rhizobacteria elicitors reveal signatures adaptation mutualists.Plant J. 2018; 93: 166-180https://doi.org/10.1111/tpj.13741Crossref (97) Upon FLS2-flg22 pairing, forms co-receptor BRI1-ASSOCIATED RECEPTOR KINASE 1 (BAK1) (Figure 1A). activates number well-defined MAMP-triggered immunity (MTI) responses form first line against colonizing microbes, also comes fitness costs due tradeoffs Hence, immunogenic potentially mediates opposing fitness, concept called pleiotropy. To investigate single amino acid changes motif affect interaction Arabidopsis thaliana FLS2, generated massive library 412 gene fliC pathogen Pseudomonas aeruginosa (Pa). Transformation into immotile ?fliC Pa mutant demonstrated 80% did not restore indicating mutations impacted locomotive flagellum. Mutations 17 acids peptide, representing “address” segment important 1B), had strongest impact function. last five acids, “message” BAK1 docking Interestingly, systematic analysis variant showed more than 70% retained FLS2. suggests much less likely 1C). Comparative revealed Asp14/15 residues critical Phytopathogenic associating contain selected Asp15, yielding prevent Scholar. some seem best worlds. approached problem different angle. investigated potential naturally occurring epitopes trigger FLS2-mediated MTI consequently inhibit growth. 779 predicted FliC protein sequences 627 flagellar were classified three clades 268 unique sequences. Flg22 clade (mainly ?- ?-Proteobacteria FliC) Bacillus Actinobacteria resembled sequence, 3 Rhizobiales Caulobacterales divergent. coworkers screened 97 representative peptides downstream MTI-related production reactive oxygen species (ROS) inhibition similarly tested set synthetic varying levels responses. While most could there induce typical ROS inhibition. points natural occurrence polymorphs without generating Immunogenic ROS-inducing growth-inhibiting mostly derived 1, immune-evading 3. “deviant” types identified However, they led differential marker genes. deviant mainly occurred 2. A striking observation was evading suggesting non-canonical 1D). Using CYP71A12, it shown triggered suppressed 42% root-dwelling 2019bYu Liu Y. Tichelaar Savant Lagendijk E. van Kuijk S.J.L. Dijken A.J.H. al.Rhizosphere-associated suppress local gluconic acid-mediated lowering environmental pH.Curr. Biol. 29: 3913-3920.e4https://doi.org/10.2139/ssrn.3396501Crossref (0) al. found non-immunogenic antagonize CYP71A12 expression Considering presence these antagonist among reasonable expect context, competition might activation success message 1B) often displayed reduced activation, when introduced restored fact present 85% benefit during prioritize stay undetected over abundantly diverse variants, plant-side seems particularly prone evolutionary selection pressure. Genome mining >1,000 accessions detected >100 only (Parys sequence may safeguard proper 1E). On other hand, polymorphism help avoid recruitment therewith further abundance prevalence previously defined (Finkel 2020Finkel O.M. Salas-González I. Castrillo G. Teixeira P.J.P.L. Wilson E.D. Fitzpatrick C.R. J.L. genus maintains microbiome.Nature. 587: 103-108https://doi.org/10.1038/s41586-020-2778-7Crossref (63) Scholar) after shoots. shoots enriched FliCs (carrying variants), (representing variants) depleted. host, became dominant, ones depleted 1F). balance flg22-carrying shifted favor exposed salt stress (Colaianni abiotic condition lowered capacity activate functioning disease, required flg22-mediated monitoring symbiotic microbiota. significant us deep mechanistic understanding interplay numerous circumvent maintaining It tempting speculate similar arms races take place immune-receptor-MAMP pairs communities consisting Collectively, contribute coordinated activity immune-suppressing mechanisms employed ultimate challenge field decipher associated harness optimize health under conditions. work supported Dutch Research Council ( NWO/OCW ), part MiCRop Consortium programme, Harnessing second genome (grant 024.004.014 ). figure created BioRender (https://biorender.com/). communitiesColaianni al.Cell MicrobeMarch 12, 2021In BriefAt interface surveillance, small produced produce dynamic modulate functionality, propose monitor proportion each type peptide identify pathogens. Full-Text Open ArchiveSignatures epitopeParys BriefA has constrained influencing evolution epitope. demonstrate this, interrogated thousands physical mutated hundreds strains assess Archive