Indole is an essential herbivore-induced volatile priming signal in maize

Erb, Matthias; Veyrat, Nathalie; Robert, Christelle; Xu, Hao; Frey, Monika; Ton, Jurriaan; Turlings, Ted C. J.

doi:10.1038/ncomms7273

Cited by 363 publications

(410 citation statements)

References 62 publications

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“…Bx2 encodes a cytochrome P450 that uses indole as a substrate to produce indolin-3-one (Frey et al, 1997) and is thus the committing enzyme for benzoxazinoid biosynthesis. Since a bx2 mutation is less likely to affect the production of other indole-derived plant defensive metabolites (Erb et al, 2015), the improved aphid growth on this mutant line is more plausibly caused by reduced benzoxazinoid content.…”

Section: Discussionmentioning

confidence: 99%

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

et al. 2015

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(A.H.); 0000-0002-9675-934X (G.J.).As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.

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Section: Discussionmentioning

confidence: 99%

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

et al. 2015

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“…Niinemets et al (2013) found evidence that quantitative relationships exist between the severity of biotic stress and induced volatile emissions, in addition to the previously demonstrated dose-response relationships for abiotic stresses. Erb et al (2015) showed that herbivore induced indole emissions in maize plants precede the release of mono-, homo-, and sesquiterpenes, supporting the conclusion that indole is involved in the airborne priming of terpenoids. Different plant stress mechanisms typically elicit release of the same ubiquitous stress volatiles, such as indole, and more stress-specific mono-and sesquiterpene blends (Erb et al, 2015;Gentner et al, 2014;Niinemets et al, 2013;Schmelz et al, 2003).…”

Section: Introductionmentioning

confidence: 48%

“…Such compounds can also be emitted by vegetation; for example, indole is produced by wide variety of plants (Cardoza et al, 2003;De Boer et al, 2004;Gols et al, 1999;McCall et al, 1993;Turlings et al, 1990;. Indole is emitted in response to physical or herbivore-induced stress (Erb et al, 2015;Frey et al, 2004;Misztal et al, 2015;Niinemets et al, 2013;Schmelz et al, 2003;Turlings et al, 2004) and during flowering events (Gentner et al, 2014). Once emitted, indole performs critical roles in plant ecology, for example in attracting pollinators (Zito et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Studies of maize plants under stress revealed that indole acts as an aerial priming agent, released before terpenoids (Erb et al, 2015;Schmelz et al, 2003). For example, Schmelz et al (2003) examined insect induced volatile emissions in Zea Mays seedlings and demonstrated direct positive relationships between jasmonic acid levels and both sesquiterpene and indole volatile emissions.…”

Section: Introductionmentioning

confidence: 99%

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Secondary organic aerosol from atmospheric photooxidation of indole

et al. 2017

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Abstract. Indole is a heterocyclic compound emitted by various plant species under stressed conditions or during flowering events. The formation, optical properties, and chemical composition of secondary organic aerosol (SOA) formed by low-NO x photooxidation of indole were investigated. The SOA yield (1.3 ± 0.3) was estimated from measuring the particle mass concentration with a scanning mobility particle sizer (SMPS) and correcting it for wall loss effects. The high value of the SOA mass yield suggests that most oxidized indole products eventually end up in the particle phase. The SOA particles were collected on filters and analysed offline with UV-vis spectrophotometry to measure the mass absorption coefficient (MAC) of the bulk sample. The samples were visibly brown and had MAC values of ∼ 2 m 2 g −1 at λ = 300 nm and ∼ 0.5 m 2 g −1 at λ = 400 nm, comparable to strongly absorbing brown carbon emitted from biomass burning. The chemical composition of SOA was examined with several mass spectrometry methods. Direct analysis in real-time mass spectrometry (DART-MS) and nanospray desorption electrospray high-resolution mass spectrometry (nano-DESI-HRMS) were both used to provide information about the overall distribution of SOA compounds. High-performance liquid chromatography, coupled to photodiode array spectrophotometry and high-resolution mass spectrometry (HPLC-PDA-HRMS), was used to identify chromophoric compounds that are responsible for the brown colour of SOA. Indole derivatives, such as tryptanthrin, indirubin, indigo dye, and indoxyl red, were found to contribute significantly to the visible absorption spectrum of indole SOA. The potential effect of indole SOA on air quality was explored with an airshed model, which found elevated concentrations of indole SOA during the afternoon hours contributing considerably to the total organic aerosol under selected scenarios. Because of its high MAC values, indole SOA can contribute to decreased visibility and poor air quality.

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“…In cucumbers, we found one difference between Si+ and Si-plants in production of volatiles, an increase in Indole. Although, our volatile extraction was conducted on harvested plants that had not experienced herbivory, while the Kvedaras et al (2010) study used plants that were currently undergoing herbivore damage, the constitutive increase in Indole indicates that Si+ plants are more primed for herbivore defense, and able to communicate attack to surrounding plants (Erb et al 2015). This, along with the potential greater sensitivity of the JA pathway through silicon, could indicate that along with increased physical defenses the volatiles also helped deter the mobile piercing sucking herbivores (Pare & Tumlinson 1999, Reynolds et al 2016).…”

Section: Discussionmentioning

confidence: 99%

The Effects of Silica Fertilizer as an Anti-Herbivore Defense in Cucumber

Callis‐Duehl

McAuslane

Duehl

et al. 2017

Journal of Horticultural Research

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This study aims to improve our understanding of silicon's role in deterring herbivores from Cucumis sativa. We hypothesized that silicon's role in plant defense is due to the presence of silica augmenting other physical and/or chemical defenses used by the plant. Using C. sativa plants treated with either a silica fertilizer treatment (Si+) or a control solution (Si-), we monitored feeding preferences of two types of herbivores, a chewing herbivore (Diabrotica balteata) and a piercing/sucking herbivore (Bemisia tabaci). Leaves from treatment plants were visited less and eaten less than leaves from control plants. We then assessed the differences in physical defenses by comparing the leaf structural components, nutrient and water content, and trichome density between treatment and control plants. For chemical plant defenses, we measured leaf carbon and nitrogen levels in, and volatile organic compounds (VOCs) from treatment and control plants. We found no significant difference between treatment and control plants in: lignin content, most elemental plant nutrients, water content, trichome density, and quantity of carbon and nitrogen. We did see an increase in the VOC Indole, known for plant defense priming, an increase in phosphorous levels and a decrease in cellulose levels in silica treated plants.

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Indole is an essential herbivore-induced volatile priming signal in maize

Cited by 363 publications

References 62 publications

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

Secondary organic aerosol from atmospheric photooxidation of indole

The Effects of Silica Fertilizer as an Anti-Herbivore Defense in Cucumber

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