Herbivore-specific induction of indirect and direct defensive responses in leaves and roots.

Li Xiao,Evan Siemann,Jianqing Ding,Juli Carrillo

doi:10.1093/aobpla/plz003

Abstract

Herbivory can induce both general and specific responses in plants that modify direct and indirect defence against subsequent herbivory. The type of induction (local versus systemic induction, single versus multiple defence induction) likely depends both on herbivore identity and relationships among different responses. We examined the effects of two above-ground chewing herbivores (caterpillar, weevil) and one sucking herbivore (aphid) on indirect defence responses in leaves and direct defence responses in both leaves and roots of tallow tree, Triadica sebifera. We also included foliar applications of methyl jasmonate (MeJA) and salicylic acid (SA). We found that chewing herbivores and MeJA increased above-ground defence chemicals but SA only increased below-ground total flavonoids. Herbivory or MeJA increased above-ground indirect defence response (extrafloral nectar) but SA decreased it. Principal component analysis showed there was a trade-off between increasing total root phenolics and tannins (MeJA, chewing) versus latex and total root flavonoids (aphid, SA). For individual flavonoids, there was evidence for systemic induction (quercetin), trade-offs between compounds (quercetin versus kaempferitrin) and trade-offs between above-ground versus below-ground production (isoquercetin). Our results suggest that direct and indirect defence responses in leaves and roots depend on herbivore host range and specificity along with feeding mode. We detected relationships among some defence response types, while others were independent. Including multiple types of insects to examine defence inductions in leaves and roots may better elucidate the complexity and specificity of defence responses of plants.

Highlights

Herbivory-induced defensive responses in plants can be direct or indirect(Howe and Jander 2008; Hagenbucher et al 2013; Kaplan et al 2016; Aljbory and Chen 2018)
Leaf total flavonoids increased with methyl jasmonate (MeJA) (Fig. 1C) and root total flavonoids increased with salicylic acid (SA) (Fig. 1F)
Antagonistic interactions are thought to be common between the jasmonic acid (JA) and SA signalling pathways, which can result in trade-offs among JA- and SA-mediated defence traits (Caillaud et al 2013; Haney et al 2018)

Summary

Introduction

Herbivory-induced defensive responses in plants can be direct (e.g. secondary chemicals suppressing herbivory) or indirect (e.g. extrafloral nectar [EFN] attracting ants)(Howe and Jander 2008; Hagenbucher et al 2013; Kaplan et al 2016; Aljbory and Chen 2018). Since plant resources are limited, theory suggests that plants face allocation trade-offs in generating induced defensive responses, and that the expression of response traits will depend on allocational, evolutionary and ecological costs (Heil 2002; Bekaert et al 2012; van Velzen and Etienne 2015; Züst et al 2015). These relationships are complex, including synergistic interactions among defensive responses (Agrawal and Fishbein 2006), antagonistic trade-offs (Koricheva et al 2004; Kempel et al 2011; Koricheva and Romero 2012; Moles et al 2013; Haak et al 2014) or some combination of positive and negative interactions (Agrawal 2011; Agrawal et al 2014). Such studies are rare (Huang et al 2014)

Methods

Results

Conclusion