Leaf metabolic signatures induced by real and simulated herbivory in black mustard (Brassica nigra)

Abstract

Introduction The oxylipin methyl jasmonate (MeJA) is a plant hormone active in response signalling and defence against herbivores. Although MeJA is applied experimentally to mimic herbivory and induce plant defences, its downstream effects on the plant metabolome are largely uncharacterized, especially in the context of primary growth and tissue-specificity of the response. Objectives We investigated the effects of MeJA-simulated and real caterpillar herbivory on the foliar metabolome of the wild plant Brassica nigra and monitored the herbivore-induced responses in relation to leaf ontogeny. Methods As single or multiple herbivory treatments, MeJA- and mock-sprayed plants were consecutively exposed to caterpillars or left untreated. Gas chromatography (GC) and liquid chromatography (LC) time-of-flight mass-spectrometry (TOF-MS) were combined to analyse foliar compounds, including central primary and specialized defensive plant metabolites. Results Plant responses were stronger in young leaves, which simultaneously induced higher chlorophyll levels. Both MeJA and caterpillar herbivory induced similar, but not identical, accumulation of tricarboxylic acids (TCAs), glucosinolates (GSLs) and phenylpropanoids (PPs), but only caterpillar feeding led to depletion of amino acids. MeJA followed by caterpillars caused higher induction of defence compounds, including a three-fold increase in the major defence compound allyl-GSL (sinigrin). When feeding on MeJA-treated plants, caterpillars gained less weight indicative of the reduced host-plant quality and enhanced resistance. Conclusions The metabolomics approach showed that plant responses induced by herbivory extend beyond the regulation of defence metabolism and are tightly modulated throughout leaf development. This leads to a new understanding of the plant metabolic potential that can be exploited for future plant protection strategies.

Profiling of Altered Metabolomic States in Bidens pilosa Leaves in Response to Treatment by Methyl Jasmonate and Methyl Salicylate

“…Most metabolites identified in leaf extracts treated with MeSA and MeJA play vital roles in the SAR/ISR responses of plants. Apart from the metabolites mentioned above, treatment with the hormones also affected the primary metabolism as citric acid/isocitric acid, a tri-carboxylic acid (TCA), was also identified as a significant ion, upregulated in MeJA-treated leaves harvested after 12 h. This corresponds to a study performed on Brassica nigra where, in response to stress induced by MeJA, regulation of the TCA cycle supported energy requirements for biosynthesis of defense molecules [ 58 ]. This indicated upregulation of a primary metabolite showing energy requirements in plants during biosynthesis of defense molecules.…”

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“…However, most amino acids identified in our study were downregulated during the high infestation period (April-June; Table 2 and Figure 6), as similarly observed by Papazian et al (2019) in response to insect herbivory. The depletion in amino acids could be partially attributed to the infestation-induced stomatal closure, which may have resulted in impaired N supply to the foliage, as indicated by the declining needle N content of attacked pines during the intense infestation period (Figure 5B).…”

“…In addition to ecophysiological approaches, metabolic profiling is essential to understand the mechanisms mediating physiological changes in Aleppo pine upon attack by M. hellenica. Plant-insect interactions are known to induce the biosynthesis of defense compounds depending on central metabolic pathways for energy demands; thus, diverse changes in both primary and secondary plant metabolism can be expected (e.g., Tian et al, 2012;Nishida, 2014;López-Goldar et al, 2018;Kortbeek et al, 2019;Papazian et al, 2019). However, to date, metabolite abundances and their changes upon infestation by M. hellenica were studied only for Aleppo pine resin terpenoides (Roussis et al, 2001;Mita et al, 2002).…”

Cell Wall Acetylation in Hybrid Aspen Affects Field Performance, Foliar Phenolic Composition and Resistance to Biological Stress Factors in a Construct-Dependent Fashion

“…Finally, we compared the effects of two fungal enzymes belonging to the different CE families. We monitored growth over five years, and determined foliar biotic damage and foliar concentrations of phenylpropanoid compounds, which are indicators of stress induction and stress resistance (Dixon and Paiva, 1995;Papazian et al, 2019). In Populus spp., biotic stress has commonly been associated with levels of condensed tannins (CTs) (Bandau et al, 2015;Lindroth and Madritch, 2015; and salicinoid phenolic glucosides (SPGs) (Albrectsen et al, 2010;Robinson et al, 2012;Lindroth and St. Clair, 2013;Lindroth and Madritch, 2015), and these phenylpropanoid compounds are often related to environmental stress responses and performance (Lindroth et al, 2011;Robinson et al, 2012;Keefover-Ring et al, 2014;Bandau et al, 2015;Decker et al, 2016).…”