Abstract
Feeding by insect herbivores such as caterpillars and aphids induces plant resistance mechanisms that are mediated by the phytohormones jasmonic acid (JA) and salicylic acid (SA). These phytohormonal pathways often crosstalk. Besides phytohormones, methyl‐D‐erythriol‐2,4‐cyclodiphosphate (MEcPP), the penultimate metabolite in the methyl‐D‐erythritol‐4‐phosphate pathway, has been speculated to regulate transcription of nuclear genes in response to biotic stressors such as aphids. Here, we show that MEcPP uniquely enhances the SA pathway without attenuating the JA pathway. Arabidopsis mutant plants that accumulate high levels of MEcPP (hds3) are highly resistant to the cabbage aphid (Brevicoryne brassicae), whereas resistance to the large cabbage white caterpillar (Pieris brassicae) remains unaltered. Thus, MEcPP is a distinct signalling molecule that acts beyond phytohormonal crosstalk to induce resistance against the cabbage aphid in Arabidopsis. We dissect the molecular mechanisms of MEcPP mediating plant resistance against the aphid B. brassicae. This shows that MEcPP induces the expression of genes encoding enzymes involved in the biosynthesis of several primary and secondary metabolic pathways contributing to enhanced resistance against this aphid species. A unique ability to regulate multifaceted molecular mechanisms makes MEcPP an attractive target for metabolic engineering in Brassica crop plants to increase resistance to cabbage aphids.
Highlights
Half a million insect herbivore species are known, and phloem‐sucking species including aphids are among the major causes of yield losses in agriculture around the world (Oerke, 2006)
The present study aims to gain detailed insight into the molecular mechanisms from signalling to biosynthesis of defence metabolites underlying the effects of MEcPP on resistance to the cabbage aphid (B. brassicae)
These results indicate that a significant increase in relative expression of genes in the salicylic acid (SA)‐signalling pathway in hds3 plants does not interfere with P. brassicae caterpillar‐induced expression of genes in the jasmonic acid (JA) biosynthetic and responsive pathways
Summary
Half a million insect herbivore species are known, and phloem‐sucking species including aphids are among the major causes of yield losses in agriculture around the world (Oerke, 2006). An increased transcript expression of genes in the SA biosynthetic and responsive pathways in ceh and hds mutant plants suggests a role of MEcPP as a positive regulator of the SA‐signalling pathway, mediating plant resistance to biotrophic pathogens and aphids (Gil et al, 2005; González‐Cabanelas et al, 2015; Xiao et al, 2012). The Arabidopsis T‐DNA‐insertion mutant plants that are silenced in the expression of the gene encoding the WRKY70 transcription factor (wrky70), an important transcription regulator involved in antagonistic effects of SA on the JA‐signalling pathway, are resistant to P. brassicae caterpillars (Onkokesung, Reichelt, van Doorn, Schuurink, & Dicke, 2016). These analyses have been complemented with investigations of a mutant overexpressing HDS in the hds background: 35S:HDS (hds3)
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