Differential Costs of Two Distinct Resistance Mechanisms Induced by Different Herbivore Species in Arabidopsis

Abstract

Plants respond to herbivory with the induction of resistance, mediated by distinct phytohormonal signaling pathways and their interactions. Phloem feeders are known to induce plant resistance via the salicylic acid pathway, whereas biting-chewing herbivores induce plant resistance mainly via the jasmonate pathway. Here, we show that a specialist caterpillar (biting-chewing herbivore) and a specialist aphid (phloem feeder) differentially induce resistance against Pieris brassicae caterpillars in Arabidopsis (Arabidopsis thaliana) plants. Caterpillar feeding induces resistance through the jasmonate signaling pathway that is associated with the induction of kaempferol 3,7-dirhamnoside, whereas aphid feeding induces resistance via a novel mechanism involving sinapoyl malate. The role of sinapoyl malate is confirmed through the use of a mutant compromised in the biosynthesis of this compound. Caterpillar-induced resistance is associated with a lower cost in terms of plant growth reduction than aphid-induced resistance. A strong constitutive resistance against P. brassicae caterpillars in combination with a strong growth attenuation in plants of a transfer DNA (T-DNA) insertion mutant of WRKY70 (wrky70) suggest that the WRKY70 transcription factor, a regulator of downstream responses mediated by jasmonate-salicylic acid signaling cross talk, is involved in the negative regulation of caterpillar resistance and in the tradeoff between growth and defense. In conclusion, different mechanisms of herbivore-induced resistance come with different costs, and a functional WRKY70 transcription factor is required for the induction of low-cost resistance.

Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra

“…As postulated previously [80], other defense compounds may play a crucial role in influencing P. brassicae performance on Brassicaceous plant species . The recent identification of flavonoid compounds that negatively impact P. brassicae caterpillar performance in Arabidopsis supports this conclusion [81, 82]. In addition, since ET is an important regulator associated with Xcr in Arabidopsis [47], local ET signaling may be involved in the local effect of Xcr on P. brassicae performance.…”

The plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclodiphosphate modulates defence responses against aphids

“…Unlike generalist aphids, many studies show that SA signalling does not have a significant role in mediating plant defences against B. brassicae aphids. SA‐deficient Arabidopsis mutant plants ( sid2‐1 ) exhibited a similar level of resistance to B. brassicae as WT plants (Onkokesung et al, ). Hence, an elevation of the expression of marker genes in SA‐biosynthesis ( ICS1 ) and SA‐response ( PR1 ) pathways of hds3 plants (Figure ) cannot fully explain an enhanced resistance against B. brassicae aphids in the mutant plants.…”

“…Plant defence responses to caterpillar feeding are mediated by the JA-signalling pathway (Reymond et al, 2004), and the antagonistic crosstalk of the SA and JA-signalling pathways is known to influence plant responses to caterpillar feeding (Mewis et al, 2005;Kroes, van Loon, & Dicke, 2015;Walling, 2008). For instance, 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). Furthermore, high relative transcript expression of JA-responsive genes corresponds with increased resistance to P. brassicae caterpillar in wrky70 mutants (Onkokesung et al, 2016).…”

Earthworms affect plant growth and resistance against herbivores: A meta‐analysis

“…auxin, ethylene, jasmonic acids or salicylic acid), known to respond to biotic and abiotic stresses (Puga‐Freitas, Barot, Taconnat, Renou, & Blouin, ; Puga‐Freitas et al., ). Generally, plants activate the jasmonic acid (JA)‐dependent signalling pathways in response to tissue‐chewing herbivores such as caterpillars and cell‐content‐feeding herbivores such as thrips (Howe & Jander, ), whereas salicylic acid (SA)‐dependent defences are activated in response to phloem‐feeders such as aphids (Onkokesung, Reichelt, van Doorn, Schuurink, & Dicke, ; Stam et al., ). We therefore hypothesised that earthworms could enhance plant resistance against a variety of herbivore types by simultaneously activating several phytohormonal pathways.…”