Receptor-like protein-mediated sensing of cysteinerich patterns in plants

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Dokumentart: PhDThesis
Date: 2024-01-04
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Biochemie
Advisor: Gust, Andrea (PD Dr.)
Day of Oral Examination: 2023-11-29
DDC Classifikation: 580 - Plants (Botany)
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Plants deploy pattern recognition receptors (PRRs) to detect microbe or damaged-self-derived molecular patterns, thereby responding to biotic stresses. Arabidopsis Lysine-Rich Repeat Receptor Like Protein (LRR-RLP) RLP30 contributes to immunity against the necrotrophic fungus Sclerotinia sclerotiorum by recognizing a so far unknown pattern within Sclerotinia Culture Filtrate Elicitor 1 (SCFE1). Here we identify the RLP30-ligand as a small cysteine-rich protein (SCP) that occurs in many fungi and oomycetes. RLP30 specifically binds SCP and forms a tripartite complex with co-receptor kinases SOBIR1 and BAK1 to mediate signaling. RE02 (Response to VmE02), an LRR-RLP non-homologous to RLP30, mediates SCP recognition in Nicotiana benthamiana. However, RLP30 and RE02 share little sequence similarity and respond to different parts of the native/folded protein. Moreover, some Brassicaceae other than Arabidopsis also respond to a linear SCP peptide instead of the folded protein, suggesting that SCP is an eminent immune target that led to the convergent evolution of distinct immune receptors in plants. Surprisingly, RLP30 shows a second ligand specificity for a SCP nonhomologous protein secreted by bacterial Pseudomonads. Stable and ectopic expression of RLP30 in Nicotiana tabacum thus not only results in quantitatively lower susceptibility to fungal and oomycete pathogens, but also to bacterial infection, demonstrating that detection of immunogenic patterns by Arabidopsis RLP30 is involved in defense against pathogens from three microbial kingdoms. Our study therefore reveals an intricate network of plant immune recognition: a single PRR can monitor immune alerts derived from three microbial kingdoms and distinct immune-sensing mechanisms for one molecular pattern exist in Brassicaceae and Solanaceae. Formerly, pattern-triggered immunity (PTI) on the plant surface and intracellular effector-triggered immunity (ETI) have been regarded as two separate branches of the plant immune system. However, it is now known that both pathways are interconnected and interdependent. As shown for other Arabidopsis RLPs, RLP30-mediated immune signaling depends on the lipase-like proteins EDS1 (enhanced disease susceptibility 1) and PAD4 (phytoalexin-deficient 4) and helper NLR (helper nucleotide-binding LRR receptor, RNL) ADR1, further solidifying the fact that PTI mediated by RLPs requires ETI components in Arabidopsis. However, EDS1 and RNLs are dispensable for SCP-triggered defenses in N. benthamiana, suggesting that the dependence of RLP signaling on EDS1-RNL modules is not conserved in Arabidopsis and N. benthamiana. Instead, the coiled coil-type helper NLR (CNL) NRCs (NLR Required for Cell death) are involved in the hypersensitive cell death induced by SCP and a few other RLP-ligands. In addition, nicotinamide, which inhibits TIR (Toll-interleukin 1 receptor) enzymatic activity, abolishes RLP-mediated cell death in N. benthamiana, implicating that a TNL (TIR-NLR receptor) and its derived small signaling molecules are required for RLP signaling. We thus speculate that a TNL-CNL tandem regulates RLP signaling in N. benthamiana.

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