Elsevier

Plant Science

Volume 303, February 2021, 110784
Plant Science

Research Article
Application of methyl jasmonate and salicylic acid lead to contrasting effects on the plant’s metabolome and herbivory

https://doi.org/10.1016/j.plantsci.2020.110784Get rights and content

Highlights

  • Overall, MeJA treatments increased small molecule concentrations.

  • Overall, SA treatments reduced small molecule concentrations.

  • MeJA reduced feeding by a chewing and a mining herbivore.

  • SA reduced feeding by a piercing-sucking herbivore.

  • Candidate compounds involved in resistance and susceptibility were identified.

Abstract

Phytohormone applications are used to mimic herbivory and can induce plant defences. This study investigated (i) metabolomic changes in leaf tissues of Jacobaea vulgaris and J. aquatica after methyl jasmonate (MeJA) and salicylic acid (SA) applications and (ii) the effects on a leaf-chewing, a leaf-mining and a piercing-sucking herbivore. MeJA treated leaves showed clearly different metabolomic profiles than control leaves, while the differences in metabolomic profiles between SA treated leaves and control leaves were less clear. More NMR peaks increased than decreased after MeJA treatment while this pattern was reversed after SA treatment. The leaf-chewing (Mamestra brassicae) and the leaf-mining herbivores (Liriomyza trifolii) fed less on MeJA-treated leaves compared to control and SA-treated leaves while they fed equally on the latter two. In J. aquatica but not in J. vulgaris, SA treatment reduced feeding damage by the piercing-sucking herbivore (Frankliniella occidentalis). Based on the herbivory and metabolomic data after phytohormone application, we made speculations as follows: For all three herbivore species, plants with high levels of threonine and citric acid showed less herbivory while plants with high levels of glucose showed more herbivory. Herbivory by thrips was lower on plants with high levels of alanine while it was higher on plants with high levels of 3,5-dicaffeoylquinic acid. The plant compounds that related to feeding of piercing-sucking herbivore were further verified with previous independent experiments.

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)

  • M. Eisenring et al.

    Differential impact of herbivores from three feeding guilds on systemic secondary metabolite induction, phytohormone levels and plant-mediated herbivore interactions

    J. Chem. Ecol.

    (2018)
  • J. Glazebrook

    Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens

    Annu. Rev. Phytopathol.

    (2005)
  • L.L. Walling

    The myriad plant responses to herbivores

    J. Plant Growth Regul.

    (2000)
  • K. Kawazu et al.

    Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes

    Arthropod-Plant Inte.

    (2012)
  • G. Beckers et al.

    Fine‐tuning plant defence signalling: salicylate versus jasmonate

    Plant Biol.

    (2006)
  • C.M. Pieterse et al.

    Cross-talk between plant defence signalling pathways: boost or burden?

    Ag Biotech. Net

    (2001)
  • M. De Vos et al.

    Herbivore-induced resistance against microbial pathogens in Arabidopsis

    Plant Physiol.

    (2006)
  • P.M. Schenk et al.

    Coordinated plant defense responses in Arabidopsis revealed by microarray analysis

    P. Natl. Acad. Sci.

    (2000)
  • S.K. Devadas et al.

    The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens

    Plant J.

    (2002)
  • P.J. Zhang et al.

    Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting salicylic acid signaling

    J. Chem. Ecol.

    (2013)
  • C. Diezel et al.

    Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling

    Plant Physiol.

    (2009)
  • G.A. Howe et al.

    Plant immunity to insect herbivores

    Annu. Rev. Plant Biol.

    (2008)
  • N.M. Van Dam et al.

    Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species

    New Phytol.

    (2004)
  • I.T. Baldwin

    Methyl jasmonate‐induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding

    Entomol. Exp. Appl.

    (1996)
  • T.F.S. de Freitas et al.

    Effects of exogenous methyl jasmonate and salicylic acid on rice resistance to Oebalus pugnax

    Pest Manag. Sci.

    (2019)
  • R. Schweiger et al.

    Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types

    Plant Cell Environ.

    (2014)
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