Dataset Information

The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding.

ABSTRACT:

Background

The 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.

Results

Here 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.

Conclusions

Together 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.

SUBMITTER: Helms AM

PROVIDER: S-EPMC4071026 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Publications

The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding.

Helms Anjel M AM De Moraes Consuelo M CM Mescher Mark C MC Tooker John F JF

BMC plant biology 20140619

<h4>Background</h4>The 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 ...[more]

PMID: 24947749

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Project description:Yeasts form mutualistic interactions with insects. Hallmarks of this interaction include provision of essential nutrients, while insects facilitate yeast dispersal and growth on plant substrates. A phylogenetically ancient chemical dialogue coordinates this interaction, where the vocabulary, the volatile chemicals that mediate the insect response, remains largely unknown. Here, we used gas chromatography-mass spectrometry, followed by hierarchical cluster and orthogonal partial least-squares discriminant analyses, to profile the volatomes of six Metschnikowia spp., Cryptococcus nemorosus, and brewer's yeast (Saccharomyces cerevisiae). The yeasts, which are all found in association with insects feeding on foliage or fruit, emit characteristic, species-specific volatile blends that reflect the phylogenetic context. Species specificity of these volatome profiles aligned with differential feeding of cotton leafworm (Spodoptera littoralis) larvae on these yeasts. Bioactivity correlates with yeast ecology; phylloplane species elicited a stronger response than fruit yeasts, and larval discrimination may provide a mechanism for establishment of insect-yeast associations. The yeast volatomes contained a suite of insect attractants known from plant and especially floral headspace, including (Z)-hexenyl acetate, ethyl (2E,4Z)-deca-2,4-dienoate (pear ester), (3E)-4,8-dimethylnona-1,3,7-triene (DMNT), linalool, α-terpineol, β-myrcene, or (E,E)-α-farnesene. A wide overlap of yeast and plant volatiles, notably floral scents, further emphasizes the prominent role of yeasts in plant-microbe-insect relationships, including pollination. The knowledge of insect-yeast interactions can be readily brought to practical application, as live yeasts or yeast metabolites mediating insect attraction provide an ample toolbox for the development of sustainable insect management.IMPORTANCE Yeasts interface insect herbivores with their food plants. Communication depends on volatile metabolites, and decoding this chemical dialogue is key to understanding the ecology of insect-yeast interactions. This study explores the volatomes of eight yeast species which have been isolated from foliage, from flowers or fruit, and from plant-feeding insects. These yeasts each release a rich bouquet of volatile metabolites, including a suite of known insect attractants from plant and floral scent. This overlap underlines the phylogenetic dimension of insect-yeast associations, which according to the fossil record long predate the appearance of flowering plants. Volatome composition is characteristic for each species, aligns with yeast taxonomy, and is further reflected by a differential behavioral response of cotton leafworm larvae, which naturally feed on foliage of a wide spectrum of broad-leaved plants. Larval discrimination may establish and maintain associations with yeasts and is also a substrate for designing sustainable insect management techniques.

Dataset Information

The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding.

Background

Results

Conclusions

Publications

The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding.

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