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Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima).

ABSTRACT: BACKGROUND:By sensing environmental cues indicative of pathogens or herbivores, plants can "prime" appropriate defenses and deploy faster, stronger responses to subsequent attack. Such priming presumably entails costs-else the primed state should be constitutively expressed-yet those costs remain poorly documented, in part due to a lack of studies conducted under realistic ecological conditions. We explored how defence priming in goldenrod (Solidago altissima) influenced growth and reproduction under semi-natural field conditions by manipulating exposure to priming cues (volatile emissions of a specialist herbivore, Eurosta solidaginis), competition between neighbouring plants, and herbivory (via insecticide application). RESULTS:We found that primed plants grew faster than unprimed plants, but produced fewer rhizomes, suggesting reduced capacity for clonal reproduction. Unexpectedly, this effect was apparent only in the absence of insecticide, prompting a follow-up experiment that revealed direct effects of the pesticide esfenvalerate on plant growth (contrary to previous reports from goldenrod). Meanwhile, even in the absence of pesticide, priming had little effect on herbivore damage levels, likely because herbivores susceptible to the primed defences were rare or absent due to seasonality. CONCLUSIONS:Reduced clonal reproduction in primed plants suggest that priming can entail significant costs for plants. These costs, however, may only become apparent when priming cues fail to provide accurate information about prevailing threats, as was the case in this study. Additionally, our insecticide data indicate that pesticides or their carrier compounds can subtly, but significantly, affect plant physiology and may interact with plant defences.

SUBMITTER: Yip EC

PROVIDER: S-EPMC6528222 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima).

Yip Eric C EC Tooker John F JF Mescher Mark C MC De Moraes Consuelo M CM

BMC plant biology 20190521 1

<h4>Background</h4>By sensing environmental cues indicative of pathogens or herbivores, plants can "prime" appropriate defenses and deploy faster, stronger responses to subsequent attack. Such priming presumably entails costs-else the primed state should be constitutively expressed-yet those costs remain poorly documented, in part due to a lack of studies conducted under realistic ecological conditions. We explored how defence priming in goldenrod (Solidago altissima) influenced growth and repro ...[more]

PMID: 31113387

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Project description:BackgroundThe induction of plant defenses in response to herbivory is well documented. In addition, many plants prime their anti-herbivore defenses following exposure to environmental cues associated with increased risk of subsequent attack, including induced volatile emissions from herbivore-damaged plant tissues. Recently, we showed in both field and laboratory settings that tall goldenrod plants (Solidago altissima) exposed to the putative sex attractant of a specialist gall-inducing fly (Eurosta solidaginis) experienced less herbivory than unexposed plants. Furthermore, we observed stronger induction of the defense phytohormone jasmonic acid in exposed plants compared to controls. These findings document a novel class of plant-insect interactions mediated by the direct perception, by plants, of insect-derived olfactory cues. However, our previous study did not exclude the possibility that the fly emission (or its residue) might also deter insect feeding via direct effects on the herbivores.ResultsHere we show that the E. solidaginis emission does not (directly) deter herbivore feeding on Cucurbita pepo or Symphyotrichum lateriflorum plants--which have no co-evolutionary relationship with E. solidaginis and thus are not expected to exhibit priming responses to the fly emission. We also document stronger induction of herbivore-induced plant volatiles (HIPV) in S. altissima plants given previous exposure to the fly emission relative to unexposed controls. No similar effect was observed in maize plants (Zea mays), which have no co-evolutionary relationship with E. solidaginis.ConclusionsTogether with our previous findings, these results provide compelling evidence that reduced herbivory on S. altissima plants exposed to the emission of male E. solidaginis reflects an evolved plant response to olfactory cues associated with its specialist herbivore and does not involve direct effects of the fly emission on herbivore feeding behavior. We further discuss mechanisms by which the priming of HIPV responses documented here might contribute to enhanced S. altissima defense against galling.

Project description:New substances with antimicrobial properties are needed to successfully treat emerging human, animal, or plant pathogens. Seven clerodane diterpenes, previously isolated from giant goldenrod (Solidago gigantea) root, were tested against Gram-positive Bacillus subtilis, Bacillus spizizenii and Rhodococcus fascians by measuring minimal bactericidal concentration (MBC), minimal inhibitory concentration (MIC) and half-maximal inhibitory concentration (IC50). Two of them, Sg3a (a dialdehyde) and Sg6 (solidagoic acid B), were proved to be the most effective and were selected for further study. Bacillus spizizenii was incubated with the two diterpenes for shorter (1 h) or longer (5 h) periods and then subjected to genome-wide transcriptional analyses. Only a limited number of common genes (28 genes) were differentially regulated after each treatment, and these were mainly related to the restoration of cell membrane integrity and to membrane-related transports. Changes in gene activity indicated that, among other things, K+ and Na+ homeostasis, pH and membrane electron transport processes may have been affected. Activated export systems can be involved in the removal of harmful molecules from the bacterial cells. Inhibition of bacterial chemotaxis and flagellar assembly, as well as activation of genes for the biosynthesis of secondary metabolites, were observed as a general response. Depending on the diterpenes and the duration of the treatments, down-regulation of the protein synthesis-related, oxidative phosphorylation, signal transduction and transcription factor genes was found. In other cases, up-regulation of the genes of oxidation-reduction processes, sporulation and cell wall modification could be detected. Comparison of the effect of diterpenes with the changes induced by different environmental and nutritional conditions revealed several overlapping processes with stress responses. For example, the Sg6 treatment seems to have caused a starvation-like condition. In summary, there were both common and diterpene-specific changes in the transcriptome, and these changes were also dependent on the length of treatments. The results also indicated that Sg6 exerted its effect more slowly than Sg3a, but ultimately its effect was greater.

Dataset Information

Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima).

Publications

Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima).

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