Dual herbivore attack and herbivore density affect metabolic profiles of Brassica nigra leaves

Abstract

Plant responses to dual herbivore attack are increasingly studied, but effects on the metabolome have largely been restricted to volatile metabolites and defence-related non-volatile metabolites. However, plants subjected to stress, such as herbivory, undergo major changes in both primary and secondary metabolism. Using a naturally occurring system, we investigated metabolome-wide effects of single or dual herbivory on Brassica nigra plants by Brevicoryne brassicae aphids and Pieris brassicae caterpillars, while also considering the effect of aphid density. Metabolomicanalysis of leaf material showed that single and dual herbivory had strong effects on the plant metabolome, with caterpillar feeding having the strongest influence. Additionally, aphid-density-dependent effects were found in both the single and dual infestation scenarios. Multivariate analysis revealed treatment-specific metabolomic profiles, and effects were largely driven by alterations in the glucosinolate and sugar pools. Our work shows that analysing the plant metabolome as a single entity rather than as individual metabolites provides new insights into the subcellular processes underlying plant defence against multiple herbivore attackers. These processes appear to be importantly influenced by insect density.

Influence of Belowground Herbivory on the Dynamics of Root and Rhizosphere Microbial Communities

“…Insect herbivory can modify plant physiology (Bolton, 2009) and alter metabolite concentrations in plant tissues (Griffiths et al, 1994;Hopkins et al, 1995;Ponzio et al, 2017) as well as nutrient uptake (Katayama et al, 2014;Aziz et al, 2016). It can also modify the release of organic matter by plant roots (rhizodeposition), a major driver of soil microbial communities (Singh et al, 2004;Paterson et al, 2007).…”

Dual‐guild herbivory disrupts predator‐prey interactions in the field

“…When we manipulated single and dual-guild herbivory in our open-field experiments, we found that foliar concentrations of gluconapin were reduced by 30% in B. oleracea plants fed upon by both caterpillars and aphids rather than aphids alone (Fig. Indeed, recent greenhouse work in this system has shown that both the glucosinolate profile (Ponzio et al 2017), and the volatile chemical profile (Ponzio et al 2016) are distinct in single and dual infestations of aphids and caterpillars. A hydrolyzed volatile product of gluconapin, 3-butenyl isothiocyanate, is innately attractive to dominant aphid parasitoid species at our sites, D. rapae (Blande et al 2007, Pope et al 2008.…”

“…Still, while suggestive, our estimates of volatile precursors in a single species are only a proxy for examining volatile-mediated plant signaling in diverse communities. Indeed, recent greenhouse work in this system has shown that both the glucosinolate profile (Ponzio et al 2017), and the volatile chemical profile (Ponzio et al 2016) are distinct in single and dual infestations of aphids and caterpillars. Important next steps will be to test these mechanisms by combining field experiments that quantify parasitoid behavior with field-collection of volatile profiles of single and dual infested plants, across a variety of plant species and cultivars.…”

“…Gluconapin (3-butenyl glucosinolate) is a glucosinolate whose volatile products include 3-butenyl isothiocyanate, a known attractant for the aphid parasitoid D. rapae (Bradburne andMithen 2000, Blande et al 2007). Therefore, we focused our analyses on this particular compound, and samples were collected at an optimal time point (72 h) for examining aphid-induced secondary metabolites (Ponzio et al 2017). Foliar tissue samples were processed from only two of the four farms in the field experiment.…”

Plant ontogeny determines strength and associated plant fitness consequences of plant‐mediated interactions between herbivores and flower visitors

“…Simultaneous colonization by nematodes and aphids on vegetative plants can thereby negatively or positively influence the effects that aphids have on seed production. Simultaneous herbivory can induce different plant responses as compared to induction by a single herbivore (Pierre, Jansen, et al, ; Ponzio, Papazian, Albrectsen, Dicke, & Gols, ). This can have consequences for plant‐mediated interactions (Chrétien et al, ; Soler et al, ; Stam, Chrétien, Dicke, & Poelman, ; Stam et al, ) and plant seed production (Stam et al, ).…”