Phosphatidylcholines from Pieris brassicae eggs activate an immune response in Arabidopsis

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.

Insect egg‐killing: a new front on the evolutionary arms‐race between brassicaceous plants and pierid butterflies

“…In other plant species tested, occasionally a single plant showed a light HR‐like necrosis. These plants might be able to detect insect eggs and respond with a general immune response, as recently shown for A. thaliana (Gouhier‐Darimont et al ., 2013, 2019; Stahl et al ., 2020). Alternatively, it could be a false‐positive response due to a contamination or a general stress response, as in rare cases, also control wash induced a weak necrosis.…”

“…In A. thaliana , eggs from distantly related insect species were recently shown to release phosphatidylcholines (PCs) that induce a general immune response (i.e. pattern‐triggered immunity) involving salicylic acid and H 2 O 2 accumulation (Little et al ., 2007; Gouhier‐Darimont et al ., 2013, 2019; Stahl et al ., 2020). A lectin receptor kinase, LecRK‐I.8, might be involved in early perception of eggs from two widely divergent species, P. brassicae and Spodoptera littoralis (Gouhier‐Darimont et al ., 2019).…”

“…In this study, ROS accumulation and cell death were induced in all plant species tested, whereas the strong HR‐like necrosis and high PR1 expression was specific to B. nigra and to Pierinae insect species. It is possible that also in other species and accessions in the Brassicaceae that we have not investigated closely, a general immune response lacking a strong cell death is activated by Pieris eggs, as was shown for A. thaliana (Col‐0) (Gouhier‐Darimont et al ., 2013, 2019; Stahl et al ., 2020; Valsamakis et al . 2020).…”

“…Defence responses induced by cabbage white butterfly eggs have been studied mainly in A. thaliana and the black mustard Brassica nigra (Little et al ., 2007; Fatouros et al ., 2014; Pashalidou et al ., 2015b; Firtzlaff et al ., 2016; Paniagua Voirol et al ., 2020; Stahl et al ., 2020). In A. thaliana , Pieris brassicae and P. rapae eggs activate a plant immune response, that resembles pattern‐triggered immunity (PTI) against pathogens.…”

DecipheringBrassicaplant defence responses to cabbage white butterfly egg-associated molecular patterns

“…However, glands from unmated females induced HR-like, and therefore another female-derived elicitor is likely to play a role (Fatouros et al, 2015). In A. thaliana , egg-derived phosphatidylcholines were recently found to induce H 2 O 2 , SA and trypan blue staining (Stahl et al, 2020). It is thus still unclear which compounds from Pieris eggs are detected by Brassica spp.…”