Signatures of antagonistic pleiotropy in a bacterial flagellin epitope

Parys, Katarzyna; Colaianni, Nicholas R.; Lee, Hoseok; Hohmann, Ulrich; Edelbacher, Natalie; Trgovcevic, Alen; Blahovska, Zuzana; Lee, Du‐Hwa; Mechtler, Alexander; Muhari-Portik, Zsuzsanna; Madalinski, Mathias; Schandry, Niklas; Rodríguez‐Arévalo, Isaac; Becker, Claude; Sonnleitner, Elisabeth; Korte, Arthur; Bläsi, Udo; Geldner, Niko; Hothorn, Michael; Jones, Corbin D.; Dangl, Jeffery L.; Belkhadir, Youssef

doi:10.1016/j.chom.2021.02.008

Cited by 52 publications

(47 citation statements)

References 94 publications

(120 reference statements)

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“…This result might reflect the fact that phylogenetically diverse, A. thaliana root–colonizing fungi display higher pathogenic potential than that of root-derived bacteria in monoassociation with the host ( 27 , 39 , 61 – 63 ) and show more extensive, site-specific associations with A. thaliana roots than bacteria in nature ( 3 ). Furthermore, the reciprocal and complex interplay between bacterial root commensals and PTI reported recently corroborated that PTI outputs selectively modulate bacterial assembly, which in turn instructs the host immune system ( 13 , 14 , 64 , 65 ). Notably, a subset of bacterial root commensals was found to suppress a specific and evolutionarily conserved sector of the A. thaliana immune system, and cooccurrence of suppressive and nonsuppressive isolates in the root microbiome appears to be critical for the maintenance of host–microbial homeostasis ( 27 , 29 ).…”

Section: Discussionmentioning

confidence: 66%

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

Wolinska

Vannier

Thiergart

et al. 2021

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

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In nature, roots of healthy plants are colonized by multikingdom microbial communities that include bacteria, fungi, and oomycetes. A key question is how plants control the assembly of these diverse microbes in roots to maintain host–microbe homeostasis and health. Using microbiota reconstitution experiments with a set of immunocompromised Arabidopsis thaliana mutants and a multikingdom synthetic microbial community (SynCom) representative of the natural A. thaliana root microbiota, we observed that microbiota-mediated plant growth promotion was abolished in most of the tested immunocompromised mutants. Notably, more than 40% of between-genotype variation in these microbiota-induced growth differences was explained by fungal but not bacterial or oomycete load in roots. Extensive fungal overgrowth in roots and altered plant growth was evident at both vegetative and reproductive stages for a mutant impaired in the production of tryptophan-derived, specialized metabolites (cyp79b2/b3). Microbiota manipulation experiments with single- and multikingdom microbial SynComs further demonstrated that 1) the presence of fungi in the multikingdom SynCom was the direct cause of the dysbiotic phenotype in the cyp79b2/b3 mutant and 2) bacterial commensals and host tryptophan metabolism are both necessary to control fungal load, thereby promoting A. thaliana growth and survival. Our results indicate that protective activities of bacterial root commensals are as critical as the host tryptophan metabolic pathway in preventing fungal dysbiosis in the A. thaliana root endosphere.

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Section: Discussionmentioning

confidence: 66%

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

Wolinska

Vannier

Thiergart

et al. 2021

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

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“…In Pst DC3000, AlgU not only downregulates flagellar and chemotaxis genes in vitro ( Markel et al, 2016 ), but also negatively regulates fliC expression during infection ( Bao et al, 2020 ). fliC encodes the flagellin protein including the flg22 epitope which triggers PTI ( Felix et al, 1999 ; Zipfel et al, 2004 ; Parys et al, 2021 ; Colaianni et al, 2021 ). Recent studies reported the important role of AlgU in de-flagellation during the P. syringae -plant interaction to reduce PTI activation, and promote bacterial fitness in its host ( Bao et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Multiple virulence factors regulated by AlgU contribute to the pathogenicity of Pseudomonas savastanoi pv. glycinea in soybean

Nguyen

Sakata

Usuki

et al. 2021

PeerJ

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Pseudomonas savastanoi pv. glycinea (Psg) causes bacterial blight of soybean. To identify candidate virulence factors, transposon-mediated mutational analysis of Psg was carried out. We syringe-inoculated soybean leaves with Psg transposon mutants and identified 28 mutants which showed reduced virulence from 1,000 mutants screened. Next, we spray-inoculated soybean leaves with these mutants and demonstrated that the algU mutant showed significantly reduced virulence together with reduced bacterial populations in planta. Expression profiles comparison between the Psg wild-type (WT) and algU mutant in HSC broth revealed that expression of coronatine (COR)-related genes (including cmaA and corR) were down-regulated in the algU mutant compared with Psg WT. Moreover, we also showed that COR production were reduced in the algU mutant compared with WT. We also demonstrated that algD, which is related to alginate biosynthesis, showed reduced expression and biofilm formation was significantly suppressed in the algU mutant. Furthermore, hrpL also showed less expression in the algU mutant. These results indicate that AlgU plays a critical role in promoting Psg pathogenesis by regulating multiple virulence factors.

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“…Colaianni and coworkers screened 97 representative flg22 peptides from the three FliC clades for FLS2 interaction and downstream MTI-related production of reactive oxygen species (ROS) and inhibition of plant growth. Parys et al, (2021) similarly tested a set of synthetic flg22 variants with varying levels of FLS2 interaction and MTI responses. While most flg22 variants could interact with FLS2, there were variants that did not induce typical MTIrelated ROS production or cause growth inhibition.…”

Section: Llmentioning

confidence: 99%

“…While at the bacterial side the flg22 epitope evolved abundantly into diverse variants, at the plant-side FLS2 seems to be particularly prone to evolutionary selection pressure. Genome mining in >1,000 Arabidopsis accessions detected >100 amino acid changes in FLS2, but only one in BAK1 (Parys et al, 2021). FLS2 sequence variation may have evolved to allow for the detection of different flg22 variants to safeguard proper immune activation (Figure 1E).…”

Section: Llmentioning

confidence: 99%

“…Comparative analysis of all the flg22 variants revealed that Asp 14/15 residues are critical for both the interaction with FLS2 and motility. Phytopathogenic Pseudomonas associating with Arabidopsis contain selected mutations at the position of Asp 15 , yielding flg22 variants that prevent FLS2 interaction but do not affect motility Parys et al (2021). Hence, some bacterial pathogens seem to have selected the best of both worlds.…”

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confidence: 99%

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

Stringlis

Pieterse

2021

Cell Host & Microbe

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Signatures of antagonistic pleiotropy in a bacterial flagellin epitope

Cited by 52 publications

References 94 publications

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

Multiple virulence factors regulated by AlgU contribute to the pathogenicity of Pseudomonas savastanoi pv. glycinea in soybean

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

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