Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa

Rapicavoli, Jeannette N.; Blanco‐Ulate, Barbara; Muszyński, Artur; Figueroa‐Balderas, Rosa; Morales‐Cruz, Abraham; Azadi, Parastoo; Dobruchowska, Justyna M.; Castro, Claudia; Cantu, Dario; Roper, M. Caroline

doi:10.1038/s41467-018-02861-5

Cited by 98 publications

(107 citation statements)

References 72 publications

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“…A manual curation of each reaction was then performed using databases, literature, and simulations. Novel reactions were written to take into account the biosynthesis of EPS and lipopolysaccharides (LPS) (24)(25)(26). To represent the global cost of excreted proteins, which are crucial virulence factors, we included reactions for the biosynthesis and excretion of a proteic virulence factor through the type II secretion system (27).…”

Section: Resultsmentioning

confidence: 99%

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

et al. 2020

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High proliferation rate and robustness are vital characteristics of bacterial pathogens that successfully colonize their hosts. The observation of drastically slow growth in some pathogens is thus paradoxical and remains unexplained. In this study, we sought to understand the slow (fastidious) growth of the plant pathogen Xylella fastidiosa. Using genome-scale metabolic network reconstruction, modeling, and experimental validation, we explored its metabolic capabilities. Despite genome reduction and slow growth, the pathogen’s metabolic network is complete but strikingly minimalist and lacking in robustness. Most alternative reactions were missing, especially those favoring fast growth, and were replaced by less efficient paths. We also found that the production of some virulence factors imposes a heavy burden on growth. Interestingly, some specific determinants of fastidious growth were also found in other slow-growing pathogens, enriching the view that these metabolic peculiarities are a pathogenicity strategy to remain at a low population level. IMPORTANCE Xylella fastidiosa is one of the most important threats to plant health worldwide, causing disease in the Americas on a range of agricultural crops and trees, and recently associated with a critical epidemic affecting olive trees in Europe. A main challenge for the detection of the pathogen and the development of physiological studies is its fastidious growth, as the generation time can vary from 10 to 100 h for some strains. This physiological peculiarity is shared with several human pathogens and is poorly understood. We performed an analysis of the metabolic capabilities of X. fastidiosa through a genome-scale metabolic model of the bacterium. This model was reconstructed and manually curated using experiments and bibliographical evidence. Our study revealed that fastidious growth most probably results from different metabolic specificities such as the absence of highly efficient enzymes or a global inefficiency in virulence factor production. These results support the idea that the fragility of the metabolic network may have been shaped during evolution to lead to the self-limiting behavior of X. fastidiosa.

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Section: Resultsmentioning

confidence: 99%

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

et al. 2020

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“…Future studies should investigate whether pure LPS (without mc‐3‐OH‐FA contamination) can activate immune responses in other plants, although only free mc‐3‐OH‐FA activates immunity in Arabidopsis . Indeed, treatment with Xylella fastidiosa LPS O‐antigen delayed plant innate immune recognition in grapevine (Rapicavoli et al , ), implying that plants recognize LPS through other moiety in addition to mc‐3‐OH‐FAs.…”

Section: Discussionmentioning

confidence: 99%

Tyrosine phosphorylation of the lectin receptor‐like kinase LORE regulates plant immunity

Luo

Liang

et al. 2020

The EMBO Journal

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Plant pattern recognition receptors (PRRs) perceive pathogen‐associated molecular patterns (PAMPs) to activate immune responses. Medium‐chain 3‐hydroxy fatty acids (mc‐3‐OH‐FAs), which are widely present in Gram‐negative bacteria, were recently shown to be novel PAMPs in Arabidopsis thaliana. The Arabidopsis PRR LIPOOLIGOSACCHARIDE‐SPECIFIC REDUCED ELICITATION (LORE) is a G‐type lectin receptor‐like kinase that recognizes mc‐3‐OH‐FAs and subsequently mounts an immune response; however, the mechanisms underlying LORE activation and downstream signaling are unexplored. Here, we report that one of the mc‐3‐OH‐FAs, 3‐OH‐C10:0, induces phosphorylation of LORE at tyrosine residue 600 (Y600). Phosphorylated LORE subsequently trans‐phosphorylates the receptor‐like cytoplasmic kinase PBL34 and its close paralogs, PBL35 and PBL36, and therefore activates plant immunity. Phosphorylation of LORE Y600 is required for downstream phosphorylation of PBL34, PBL35, and PBL36. However, the Pseudomonas syringae effector HopAO1 targets LORE, dephosphorylating the tyrosine‐phosphorylated Y600 and therefore suppressing the immune response. These observations uncover the mechanism by which LORE mediates signaling in response to 3‐OH‐C10:0 in Arabidopsis.

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“…O-antigen is an essential virulence factor for P. aeruginosa in its colonization of animal tissues (52). While O-antigen is dispensable for growth in culture, it has been recently shown to delay the host immune response during Xylella fastidiosa colonization of grape xylem (53). Alternatively, glycosyltransferase activity may contribute to flagellar modifications in order to avoid plant recognition (54, 55).…”

Section: Discussionmentioning

confidence: 99%

Genome-wide identification ofPseudomonas syringaegenes required for competitive fitness during colonization of the leaf surface and apoplast

Helmann¹,

Deutschbauer

Lindow³

2019

Preprint

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The foliar plant pathogen Pseudomonas syringae can establish large epiphytic populations on leaf surfaces before infection. However, the bacterial genes that contribute to these lifestyles have not been completely defined. The fitness contributions of most genes in P. syringae pv. syringae B728a were determined by genome-wide fitness profiling with a randomly barcoded transposon mutant library that was grown on the leaf surface and in the apoplast of the susceptible plant Phaseolus vulgaris. Genes within the functional categories of amino acid and polysaccharide (including alginate) biosynthesis contributed most to fitness both on the leaf surface (epiphytic) or in the leaf interior (apoplast), while genes in the type III secretion system and syringomycin synthesis were primarily important in the apoplast. Numerous other genes that had not been previously associated with in planta growth were also required for maximum epiphytic or apoplastic fitness. Many hypothetical proteins and uncategorized glycosyltransferases were also required for maximum competitive fitness in and on leaves. For most genes, no relationship was seen between fitness in planta and either the magnitude of their expression in planta or degree of induction in planta compared to in vitro conditions measured in other studies. A lack of association of gene expression and fitness has important implications for the interpretation of transcriptional information and our broad understanding of plant-microbe interactions.Significance StatementMany plant pathogenic bacteria can extensively colonize leaf surfaces before entry and multiplication within the leaf to cause disease. While these habitats presumably require distinct adaptations, the genes required in these habitats and how they would differ was unknown. Using a genome-wide library of barcoded insertional mutants in the plant pathogen Pseudomonas syringae, we ascertained the common and unique genes required to colonize these habitats. A lack of association between gene expression and contribution to fitness suggests that many genes that are highly expressed or induced in planta are dispensable or redundant. As a model bacterium for plant pathogenesis and colonization, our comprehensive genetic dataset allows us to better understand the traits needed for association with leaves.

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Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa

Cited by 98 publications

References 72 publications

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

Genome-Scale Investigation of the Metabolic Determinants Generating Bacterial Fastidious Growth

Tyrosine phosphorylation of the lectin receptor‐like kinase LORE regulates plant immunity

Genome-wide identification ofPseudomonas syringaegenes required for competitive fitness during colonization of the leaf surface and apoplast

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