Oviposition by Pierid Butterflies Triggers Defense Responses in Arabidopsis

Abstract

Insect eggs represent a threat for the plant as hatching larvae rapidly start with their feeding activity. Using a whole-genome microarray, we studied the expression profile of Arabidopsis (Arabidopsis thaliana) leaves after oviposition by two pierid butterflies. For Pieris brassicae, the deposition of egg batches changed the expression of hundreds of genes over a period of 3 d after oviposition. The transcript signature was similar to that observed during a hypersensitive response or in lesion-mimic mutants, including the induction of defense and stress-related genes and the repression of genes involved in growth and photosynthesis. Deposition of single eggs by Pieris rapae caused a similar although much weaker transcriptional response. Analysis of the jasmonic acid and salicylic acid mutants coi1-1 and sid2-1 indicated that the response to egg deposition is mostly independent of these signaling pathways. Histochemical analyses showed that egg deposition is causing a localized cell death, accompanied by the accumulation of callose, and the production of reactive oxygen species. In addition, activation of the pathogenesis-related1Tb-glucuronidase reporter gene correlated precisely with the site of egg deposition and was also triggered by crude egg extract. This study provides molecular evidence for the detection of egg deposition by Arabidopsis plants and suggests that oviposition causes a localized response with strong similarity to a hypersensitive response.

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

“…In a parallel experiment, oviposited plants were challenged with S. littoralis larvae for 10 d and larval performance assessed. Natural oviposition suppressed wound-induced VSP2 expression and stimulated S. littoralis larval growth to a These results are in line with our previous observations that SA accumulation, defense gene expression, and physiological changes occur in response to natural oviposition or application of egg extract (Little et al, 2007;Bruessow et al, 2010;Reymond, 2013).…”

“…SA accumulates upon oviposition and the expression of SA-and NPR1-dependent genes (e.g. PR1) is activated (Little et al, 2007;Bruessow et al, 2010, Gouhier-Darimont et al, 2013. In addition, egg-induced SA accumulation is known to inhibit larvae-induced expression of JAdependent genes (e.g.…”

“…We analyzed the expression of genes that are strongly upregulated by oviposition (Little et al, 2007). The SA marker gene PR1, a chitinase gene (CHIT), and a trypsin inhibitor gene (TI) were all markedly up-regulated by egg extract treatment or by a consecutive egg extract and wound treatment.…”

“…We previously noticed that WRKY75 was highly induced by P. brassicae oviposition (Little et al, 2007). Since several WRKYs have been reported to modulate SA/JA antagonism (Caarls et al, 2015), this prompted us to test the involvement of this factor in response to egg extract treatment.…”

“…In Arabidopsis, insect eggs trigger cellular and molecular changes that are very similar to those that are caused by infection with biotroph pathogens. Indeed, eggs from the specialist lepidopteran herbivore Pieris brassicae induce a hypersensitive-like response, callose and reactive oxygen species accumulation, and the induction of pathogenesis-related genes (Little et al, 2007;GouhierDarimont et al, 2013). Expression of PATHOGENESIS-RELATED1 (PR1) is strongly up-regulated at the site of oviposition in response to P. brassicae eggs but also in response to egg extracts from other insect species, including the generalist Spodoptera littoralis (Bruessow et al, 2010).…”