Research ArticleApplication of methyl jasmonate and salicylic acid lead to contrasting effects on the plant’s metabolome and herbivory
Introduction
Plants have evolved different strategies, including chemical and mechanical defences, to cope with attacks from herbivores and pathogens [1,2]. Chemical defences are mainly based on secondary metabolites (SMs) derived from different chemical origins, often characteristic for certain plant taxa and effective at least against generalist herbivores [3]. Mostly shifts in chemical composition upon attack are herbivore-specific and depend to some degree on the feeding mode of the herbivore [4,5].
Induction of chemical defense after attack is mediated by phytohormones such as jasmonate (JA), ethylene (ET) and salicylic acid (SA). As a general rule, the JA pathway, which frequently acts synergistically with ET, is up-regulated if the plant is attacked by chewing-biting herbivores, cell-content feeders and necrotrophic pathogens [6,7], while the SA pathway is activated in response to piercing-sucking insects and biotrophic pathogens [7,8]. Therefore, it is predicted that the compounds activated by the JA pathway help the plant to resist chewing-biting herbivores and cell-content feeders while the compounds activated by the SA pathway help the plant to resist piercing-sucking herbivores. JA and SA pathways are not distinct from each other but interact by a complex network of regulatory interactions [9,10], including priming [11,12], complementary additive or synergistic effects [13,14] and mutual antagonism [15,16].
Direct exogenous application of phytohormones has been commonly used to simulate attack by herbivores and to analyse the plant responses to herbivory [17]. In Brassicae and Nicotiana species, glucosinolate and nicotine concentrations increased in response to JA application [18,19]. SA application induced resistance against rice stink bugs [20]. The artificial application of JA reduced thrips-associated damage in a whole plant no-choice bioassay of tomato [21]. Most of these studies showed the effects of JA or SA application on the production of SMs or the performance of herbivores. Only few studies aimed at coupling the changes in metabolic profiles upon hormone application with the changes in herbivore feeding [22,23]. In addition, most studies were targeted at one specific group of plant SMs while other chemical compounds, which might also be important to defense, were neglected [24,25].
In this study, we investigated how metabolic profiles were affected by exogenous application of methyl jasmonate (MeJA) and SA. We also examined how these induced metabolic profiles were associated with feeding by herbivores with different feeding modes. We addressed these questions with two plant species known for their pyrrolizidine alkaloids (PAs), common ragwort, Jacobaea vulgaris (syn. Senecio jacobaea) and marsh ragwort, Jacobaea aquatica (both Asteraceae). Previously, we showed that, while the total PA concentration in these plant species was not affected by root application of MeJA, the composition of PAs shifted significantly from senecionine- to erucifoline-like PAs [26]. However, it remained unclear to what extent other plant chemical components are affected by phytohormone application. A leaf-chewing herbivore, cabbage moth, Mamestra brassicae (Lepidoptera: Noctuidae), a leaf-mining herbivore, celery leafminer, Liriomyza trifolii (Diptera: Agromyzidae) and a piercing-sucking herbivore, western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) were used in this study. Our experiments were designed to answer the following questions: (1) How do the plant metabolic profiles change after MeJA and SA application to the leaves? (2) Is the feeding damage of the leaf-chewing herbivore and the leaf-mining herbivore reduced by MeJA application? (3) Is the feeding damage of the piercing-sucking herbivore reduced by SA application? (4) Are the changes in the plant metabolites related to the changes in herbivore feeding? (5) If so, which compounds are associated with reduced or increased feeding levels of these three herbivores? The compounds that potentially affected the feeding of F. occidentalis were further investigated by combining the results of the present experiment with those of two previous experiments [27,28].
Section snippets
Plants and insects
Jacobaea vulgaris and Jacobaea aquatica individuals used in this study are the parental genotypes of a well-studied hybrid cross [29]. J. vulgaris was derived from seeds collected at the Meijendel Nature Reserve (52°7′54″N, 4°19′46″E, The Netherlands), and J. aquatica was derived from seeds collected at the Zwanenwater Nature Reserve (52°48′38″N, 4°41′7″E, The Netherlands). J. vulgaris is attacked by over 60 species of herbivores and grows in dry and sandy soils while J. aquatica is fed on by
Effects of phytohormone treatments on the NMR metabolite profile of leaf tissue
A principle component analysis (PCA) of the 1H-NMR peaks from J. vulgaris showed that, 63.1 % of the variation was explained by the first two axes (Fig. 1a) while the third axis explained 9.2 %. In J. aquatica, 64.7 % of the variances was explained by the first two axes (Fig. 1b) and another 10.0 % was explained by the third axis. PCA plots of the first two components showed that the plants treated with MeJA were separated from the control and SA treated plants for both plant species. Although
Discussion
The metabolic profiles of both plant species showed similar shifts after application of phytohormones. The peak area of more NMR bins was affected by phytohormone treatments in J. aquatica than in J. vulgaris. The latter was especially true for the SA treatment, in which the NMR signals of 76 bins (Table 1) were affected significantly in J. aquatica while only seven bins were affected in J. vulgaris. Apparently, there was a strong species-specific effect in the strength of the response but not
Conclusions
The metabolites in the two Jacobaea species showed a similar response pattern: the MeJA treatment induced more metabolites to be upregulated while the SA treatment showed more metabolites that were downregulated compared to the control. However, the up and down regulation was more pronounced in J. aquatica. The feeding of leaf-chewing (M. brassicae) and leaf-mining (L. trifolii) herbivores was significantly reduced in the MeJA treated leaves while the piercing-sucking herbivore (F. occidentalis
Author contributions
Klaas Vrieling, Peter G. L. Klinkhamer and Xianqin Wei conceived and designed the research. Xianqin Wei performed the experiments. Hye Kyong Kim and Patrick P. J. Mulder did the chemical analysis. All the authors participated in the data analysis. Xianqin Wei wrote the manuscript. Klaas Vrieling, Peter G. L. Klinkhamer and Patrick P. J. Mulder revised the manuscript.
Declaration of Competing Interest
The authors declare no conflict of interest.
Acknowledgements
We thank Karin van der Veen-van Wijk and Yan Yan for the technical help. We thank Harald van Mil for his help in statistical analysis. We thank Dr. Saskia Klumpers for her efforts on English polishing. We also thank two anonymous reviewers for their valuable comments. This research was supported by “the Fundamental Research Funds for the Central Universities”, Nankai University (Grant Number 63191404).
References (53)
- et al.
The study of hormonal metabolism of Trincadeira and Syrah cultivars indicates new roles of salicylic acid, jasmonates, ABA and IAA during grape ripening and upon infection with Botrytis cinerea
Plant Sci.
(2019) - et al.
Type VI glandular trichome density and their derived volatiles are differently induced by jasmonic acid in developing and fully developed tomato leaves: implications for thrips resistance
Plant Sci.
(2018) - et al.
Metabolomic analysis of methyl jasmonate treated Brassica rapa leaves by 2-dimensional NMR spectroscopy
Phytochemistry
(2006) - et al.
The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida
Enzyme Microb. Technol.
(2000) - et al.
Interplant communication: airborne methyl jasmonate is essentially converted into JA and JA-Ile activating jasmonate signaling pathway and VOCs emission
Biochem. Biophys. Res. Commun.
(2008) - et al.
Glucose, some amino acids and a plant secondary metabolite, chlorogenic acid induce the secretion of a regulatory hormone, tachykinin-related peptide, from the silkworm midgut
Peptides
(2018) - et al.
Plant defense against insect herbivores
Int. J. Mol. Sci.
(2013) Transgenerational effects alter plant defence and resistance in nature
J. Evol. Biol.
(2017)- et al.
Insect-Plant Biology
(2005) - et al.
Induced Responses to Herbivory
(2007)