Lipopolysaccharide functions in plant-bacteria interactions
Plant Breeding and Plant Pathology
Final Report Abstract
Infestations of plants with pathogenic gram-negative bacteria such as Pseudomonas and Xanthomonas cause significant crop yield losses every year. The outcome of attempted pathogen infection of a host depends on its ability to sense the invading pathogen and rapidly mount a defence response and on the repertoire of evasion strategies and virulence factors employed by a pathogen to circumvent the host’s defence systems. Detection of conserved microbial signatures, so-called Microbe-Associated Molecular Patterns (MAMPs), by specific host Pattern-Recognition Receptors (PRRs) is an integral part of the immune system of animals and plants. Lipopolysaccharide (LPS), a complex glycolipid macromolecule composed of several domains covering the cell surface of gram-negative bacteria, is not only vital for the survival of bacteria but further fulfils multiple roles in interaction with hosts. LPS is a strong agonist of the mammalian innate immune system and its lipid A (LA) moiety is sensed by extracellular and intracellular immune receptors. As a highly restrictive barrier, LPS is also vital for resistance against host antimicrobial compounds and an important virulence factor. In mammals, dynamic remodelling of the LPS structure evolved as a strategy of adapted bacteria to evade immune sensing, adjust to hostile host environments and withstand host defence measures. LPS is also sensed by plants and triggers defence reactions, but the perception systems are not understood. We have recently shown that the LA domain of LPS is sensitively perceived as a MAMP in the model plant Arabidopsis thaliana and identified a key component of LPS signalling, the receptor-like kinase LORE (LipoOligosaccharide-specific Reduced Elicitation). This project studied the molecular details of the complex role of LPS in plant-bacteria interactions. LPS is an important bacterial virulence factor but is also sensed by the plant’s immune system. We identified and characterized LPS structures which perform both of these apparently opposing tasks. Specifically, we show (1) which structural motifs derived from LPS and other microbial components exactly activate immune responses in plants and how recognition specificity is achieved at the molecular level, (2) which LPS structures contribute to bacterial virulence, and finally (3) that alterations of bacterial LA structures occur during colonization of host plants and promote plant infection. Hence, remodelling of LA structures is a common virulence strategy promoting infection of mammalian and plant hosts.
Publications
- Challenges in the identification of microbe-associated molecular patterns in plant and animal innate immunity: a case study with bacterial lipopolysaccharide. Mol Plant Pathol 17: 1165-1169
Ranf S, Scheel D, and Lee J
(See online at https://doi.org/10.1111/mpp.12452) - Immune Sensing of Lipopolysaccharide in Plants and Animals: Same but Different. PLoS Pathog 12 e1005596
Ranf S
(See online at https://doi.org/10.1371/journal.ppat.1005596) - Bacterial medium chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364:178
Kutschera A, Dawid C, Gisch N, Schmid C, Raasch L, Gerster T, Schäffer M, Smakowska-Luzan E, Belkhadir Y, Vlot AC, Chandler CE, Schellenberger R, Schwudke D, Ernst RK, Dorey S, Hückelhoven R, Hofmann T, and Ranf S
(See online at https://doi.org/10.1126/science.aau1279) - Loss of wbpL disrupts O-polysaccharide synthesis and impairs virulence of plant-associated Pseudomonas strains. Mol Plant Pathol 20: 1535-1549
Kutschera A, Schombel U, Wrobel M, Gisch N, and Ranf S
(See online at https://doi.org/10.1111/mpp.12864) - The multifaceted functions of lipopolysaccharide in plant-bacteria interactions. Biochimie 159: 93-98
Kutschera A, and Ranf S
(See online at https://doi.org/10.1016/j.biochi.2018.07.028) - Analysis of the Structure and Biosynthesis of the Lipopolysaccharide Core Oligosaccharide of Pseudomonas syringae pv. tomato DC3000. Int J Mol Sci 22: 3250
Kutschera A, Schombel U, Schwudke D, Ranf S, and Gisch N
(See online at https://doi.org/10.3390/ijms22063250) - Bacterial rhamnolipids and their 3-hydroxyalkanoate precursors activate Arabidopsis innate immunity through two independent mechanisms. Proc Natl Acad Sci U S A 118 (39) e2101366118
Schellenberger R, Crouzet J, Nickzad A, Shu L-J, Kutschera A, Gerster T, Borie N, Dawid C, Cloutier M, Villaume S, Dhondt-Cordelier S, Hubert J, Cordelier S, Mazeyrat-Gourbeyre F, Schmid C, Ongena M, Renault J-H, Haudrechy A, Hofmann T, Baillieul F, Clément C, Zipfel C, Gauthier C, Déziel E, Ranf S, and Dorey S
(See online at https://doi.org/10.1073/pnas.2101366118) - Remodeling of Lipid A in Pseudomonas syringae pv. phaseolicola In Vitro. Int J Mol Sci 23: 1996
Gerster T, Wröbel M, Hofstaedter CE, Schwudke D, Ernst RK, Ranf S, Gisch N
(See online at https://doi.org/10.3390/ijms23041996)
