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Plant immunity: plants are not defenceless

The outcome of an attempted infection of a plant depends on its ability to sense invading pathogens and rapidly mount defence reactions, and on the pathogen’s repertoire of virulence strategies to evade or subvert plant immunity.
Plants are permanently exposed to diverse classes of potentially pathogenic microbes. Despite, plants are mostly healthy as they have evolved efficient surveillance and defence systems to ward off microbial invaders. Pathogens, in turn, evolved virulence strategies to evade recognition or suppress defence responses, while plants evolve new recognition strategies. Hence, an evolutionary arms-race exists between pathogens and their potential host plants. We want to understand the molecular mechanisms of plant immune sensing and immune responses as well as microbial adaptation and virulence strategies to support plant breeding and biotechnology in keeping pace with the adaptation of pathogens and in strengthening plant health.

Innate immunity: a common concept in animals and plants

Conserved microbial signatures, so-called microbe-associated molecular patterns (MAMPs), betray the pathogen’s presence to the host. MAMP detection by specific host pattern-recognition receptors (PRRs) is an integral part of the immune system of animals and plants. Cell surface components such as bacterial lipopolysaccharide (LPS), peptidoglycan and flagellin are typical MAMPs as they are vital for microbial survival and common to whole microbial classes. In mammals, MAMPs are sensed by different classes of PRRs e.g. the Toll-like receptors (TLRs), and trigger inflammatory responses. Vertebrates additionally evolved an adaptive immune system employing highly specific antibodies. Plants do not possess specialized roaming immune cells like vertebrates and rely solely on genetically determined innate immune responses that can be executed by almost all plant cells. In plants, sensing of MAMPs by PRRs induces a common set of signalling and defence responses known as pattern-triggered immunity (PTI). Despite some conceptual similarities, MAMP sensing apparently evolved independently in animals and plants.

Functions of lipopolysaccharide in host-bacteria interactions

Scheme of Gram-negative bacterial cell envelope.
Our group studies the interaction between plants and Gram-negative bacterial pathogens such as Pseudomonas syringae. We are particularly interested in LPS, a heterogeneous and complex glycolipid macromolecule composed of several domains, that covers ~75% of the Gram-negative bacterial cell surface. LPS is not only vital for survival of bacteria but fulfils multiple roles in interaction with hosts. LPS is sensed in various ways by the mammalian as well as the plant immune system and triggers defence reactions. At the same time, LPS as a highly restrictive barrier, is vital for resistance against antimicrobial compounds released by the host. We want to understand LPS immune sensing and the role of LPS as virulence factor during plant infection on the molecular level by combining expertise in plant biochemistry, microbiology, structural biology as well as analytical chemistry.

Lipopolysaccharide immune sensing differs in animals and plants

In mammals, LPS is a strong agonist of the innate immune system and its lipid A domain is sensed in trace amounts by extra- and intracellular immune receptors. LPS is also sensed in different plant species, but the perception systems are not yet understood. In a genetic screen for LPS sensing components in the model plant Arabidopsis thaliana, we identified the lectin S-domain receptor kinase LORE (LipoOligosaccharide-specific Reduced Elicitation) (Ranf et al., Nature Immunology, 2015). Interestingly, LORE does not sense LPS itself but free 3-hydroxylated fatty acids of medium chain length, which apparently co-purify with LPS during extraction from bacterial cell material. In Pseudomonas, medium chain 3-hydroxy fatty acids are part of the lipid A moiety of LPS and released during synthesis of penta-acylated LPS in the outer membrane by the lipid A O-deacylase PagL. 3-hydroxy fatty acids are also building blocks of other bacterial compounds and are presumably produced through different metabolic pathways (Kutschera et al., Science, 2019). Hence, in contrast to mammals which sense complex structures such as the lipid A domain of LPS, Arabidopsis plants sense small, low-complexity 3-hydroxy fatty acid metabolites.

Currently known sensing systems of lipid A and lipid A-related metabolites in humans and cruciferous plants.

In humans (left panel), LPS is sensed by different immune cells through different extra- and intracellular receptors. LPS is disaggregated from the bacterial membrane by the serum protein LBP and transferred to CD14, which occurs as soluble (sCD14) and membrane-linked (mCD14) version. Dependent on the cell type, CD14 can trigger LPS signalling itself, or further transfers LPS to the membrane-resident TLR4/MD-2 receptor complex. Lipid A binding to a preformed TLR4/MD-2 hetero-dimer leads to association with another TLR4/MD-2-dimer and initiates intracellular signalling. Depending on the cellular localization (at the plasma membrane or in endosomes upon CD14-dependent endocytosis) TLR4/MD-2/LPS complexes activate production of either interferons or cytokines through distinct signalling adapters (TIRAP/MyD88 or TRIF/TRAM). Intracellular LPS leads to oligomerization of caspase-4, activation of the non-canonical inflammasome and pyroptotic cell death.

In Arabidopsis plants (right panel), the bulb-type lectin S-domain-1 receptor kinase LORE was identified in a genetic screen for LPS sensing components. LORE does not sense LPS directly but free medium-chain 3-hydroyx fatty acids, which are released from the LPS lipid A moiety and presumably other metabolic pathways. In analogy to other SD-RLKs, LORE likely forms dimers and is activated through mutual phosphorylation by the cytosolic kinase domain. (Figure adapted from Ranf et al. 2016, PLoS Pathogens)



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