Phosphatidylcholines from Pieris brassicae eggs activate an immune response in Arabidopsis.

Elia Stahl,Emerson Ferreira Queiroz,Théo Brillatz,Isabelle Riezman,Howard Riezman,Philippe Reymond,Laurence Marcourt,André Schmiesing,Jean-Luc Wolfender,Olivier Hilfiker

doi:10.7554/elife.60293

Abstract

Recognition of conserved microbial molecules activates immune responses in plants, a process termed pattern-triggered immunity (PTI). Similarly, insect eggs trigger defenses that impede egg development or attract predators, but information on the nature of egg-associated elicitors is scarce. We performed an unbiased bioactivity-guided fractionation of eggs of the butterfly Pieris brassicae. Nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry of active fractions led to the identification of phosphatidylcholines (PCs). PCs are released from insect eggs, and they induce salicylic acid and H2O2 accumulation, defense gene expression and cell death in Arabidopsis, all of which constitute a hallmark of PTI. Active PCs contain primarily C16 to C18-fatty acyl chains with various levels of desaturation, suggesting a relatively broad ligand specificity of cell-surface receptor(s). The finding of PCs as egg-associated molecular patterns (EAMPs) illustrates the acute ability of plants to detect conserved immunogenic patterns from their enemies, even from seemingly passive structures such as eggs.

Highlights

In nature, plants are frequently confronted with microbial pathogens or herbivores, and have evolved an efficient immune response that mainly relies on initial detection of the attacker, followed by production of defense proteins and toxic metabolites (Jones and Dangl, 2006; Schuman and Baldwin, 2016)
In order to find marker genes that we could robustly use to identify defense-inducing compounds in eggs, we performed an RNA sequencing experiment using Arabidopsis plants on which eggs were naturally oviposited by P. brassicae butterflies and compared it with plants treated with egg extract (EE)
Amongst the most highly upregulated genes, we selected PATHOGENESIS-RELATED PROTEIN1 (PR1, At2g14610), SENESCENCE-ASSOCIATED GENE 13 (SAG13, At2g29350), and KUNITZ INHIBITOR PROTEIN 1 (TI, At1g73260), which were induced by oviposition and EE treatment (Figure 1—figure supplement 1, Supplementary file 1) and which were initially found to be strongly responsive to P. brassicae oviposition and to treatment by EE from different insect species (Bruessow et al, 2010)

Summary

Introduction

Plants are frequently confronted with microbial pathogens or herbivores, and have evolved an efficient immune response that mainly relies on initial detection of the attacker, followed by production of defense proteins and toxic metabolites (Jones and Dangl, 2006; Schuman and Baldwin, 2016). What plants perceive is the presence of conserved microbe-associated molecular patterns (MAMPs) and activate pattern-triggered immunity (PTI) (Ranf, 2017). Flagellin, peptidoglycan or medium-chain 3-hydroxy-fatty acids constitute well-studied sources of MAMPs that are sensed by specific plant cell-surface receptor-like kinases; the same is true for chitin, a structural component of fungal cell walls (Boutrot and Zipfel, 2017; Ranf, 2017; Kutschera et al, 2019). Oral secretions (OS) from feeding insect larvae contain herbivore-associated molecular patterns (HAMPs) that trigger defense responses (Wu and Baldwin, 2010; Erb and Reymond, 2019). For example, is a fatty acidamino acid conjugate from several chewing herbivores OS and triggers the release of plant volatile organic compounds that attract parasitic wasps (Alborn et al, 1997). Contrary to MAMPs, receptors for HAMPs have not yet been described

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Conclusion