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

Erb M, Veyrat N, Robert CA, Xu H, Frey M, Ton J, Turlings TC - Nat Commun (2015)

Bottom Line: We therefore hypothesized that indole may be involved in airborne priming.Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming.These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Sciences, Department of Biology, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland.

ABSTRACT
Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

No MeSH data available.


Related in: MedlinePlus

Indole is required for within-plant priming.(a) Setup used for experiment. Before the elicitation treatment, the first leaf of each plant was either left intact, induced by scratching and applying Spodoptera littoralis regurgitant, or similarly induced and placed in a Teflon bag for 12 h. The second leaf of all plants was then wounded 12h later and volatiles were collected for 600 min. (b) Sums of volatiles of the four major families of HIPVs released from WT and igl mutant plants are shown: green leaf volatiles, monoterpenes, homoterpenes and sesquiterpenes. Different letters indicate significant differences between treatments (Holm-Sidak post hoc tests, P<0.05; n=4). Error bars correspond to standard errors (±s.e.). For individual compounds, see Supplementary Figs 5 and 6.
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f4: Indole is required for within-plant priming.(a) Setup used for experiment. Before the elicitation treatment, the first leaf of each plant was either left intact, induced by scratching and applying Spodoptera littoralis regurgitant, or similarly induced and placed in a Teflon bag for 12 h. The second leaf of all plants was then wounded 12h later and volatiles were collected for 600 min. (b) Sums of volatiles of the four major families of HIPVs released from WT and igl mutant plants are shown: green leaf volatiles, monoterpenes, homoterpenes and sesquiterpenes. Different letters indicate significant differences between treatments (Holm-Sidak post hoc tests, P<0.05; n=4). Error bars correspond to standard errors (±s.e.). For individual compounds, see Supplementary Figs 5 and 6.

Mentions: To further investigate the role of indole in plant priming, we used igl mutant plants in a bx1 mutant background46. The double mutant plants are impaired in the emission of indole, whereas the bx1 single mutant plants release indole at wild-type levels (Fig. 3). The activity of the Bx1 gene varies considerably across maize lines47, and includes naturally inactive alleles42. Consequently, the use of a bx1 mutant background enabled us to assess the role of IGL-produced indole without potential interference from other sources of free indole. First, we confirmed that igl mutants still release all other classes of volatiles in comparable amounts as plants carrying a wild-type Igl allele (WT). No systematic quantitative and qualitative differences were found between herbivore-induced volatile blends of WT and igl mutants (Fig. 3 and Supplementary Figs 3 and 4). To investigate whether indole is required for systemic priming in unharmed tissues of attacked plants, the first true leaf of igl mutant and WT seedlings was either left intact or subjected to elicitation treatment by mechanical wounding and application of oral caterpillar secretions. A subset of the elicited emitter leaves was then wrapped in a small Teflon bag that was sealed around the base of the leaf to minimize HIPV contact of undamaged systemic tissues. All plants were then placed in glass bottles and exposed to a continuous clean airflow of 0.3 l min−1 to prevent non-physiological build-up of HIPVs and to isolate the headspace of the different plants. Twelve hours later, all plants were challenged with a second elicitation treatment of leaf 2, after which HIPV emissions were measured at different time points (Fig. 4). During these volatile collections, all the first true leaves were enclosed in a clean Teflon bag to ensure that only volatiles from the second elicitation treatment were captured. No HIPVs except GLVs were detected at the beginning of the second elicitation treatment, indicating that 12 h after elicitation, there was no systemic release of HIPVs induced by the first elicitation treatment anymore48. Throughout the sampling period, indole-competent plants that were previously exposed to their own induced headspace released significantly higher total amounts of mono- and homoterpenes than genetically similar plants that were exposed to constitutive volatiles (Fig. 4, Holm-Sidak post hoc tests: P<0.05). These differences were mainly driven by linalool and DMNT (Supplementary Figs 5 and 6). When volatile exposure was interrupted with a Teflon bag, the systemic priming effect of mono- and homoterpenes disappeared, indicating that within-plant systemic priming of HIPVs in maize partially depends on previous HIPVs exposure. Moreover, indole-deficient mutant plants released the same total amounts of mono- and homoterpenes, irrespective of previous exposure to their own (indole-free) HIPV blend (Fig. 4), showing that indole is required for within-plant priming of the above volatiles.


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

Erb M, Veyrat N, Robert CA, Xu H, Frey M, Ton J, Turlings TC - Nat Commun (2015)

Indole is required for within-plant priming.(a) Setup used for experiment. Before the elicitation treatment, the first leaf of each plant was either left intact, induced by scratching and applying Spodoptera littoralis regurgitant, or similarly induced and placed in a Teflon bag for 12 h. The second leaf of all plants was then wounded 12h later and volatiles were collected for 600 min. (b) Sums of volatiles of the four major families of HIPVs released from WT and igl mutant plants are shown: green leaf volatiles, monoterpenes, homoterpenes and sesquiterpenes. Different letters indicate significant differences between treatments (Holm-Sidak post hoc tests, P<0.05; n=4). Error bars correspond to standard errors (±s.e.). For individual compounds, see Supplementary Figs 5 and 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4339915&req=5

f4: Indole is required for within-plant priming.(a) Setup used for experiment. Before the elicitation treatment, the first leaf of each plant was either left intact, induced by scratching and applying Spodoptera littoralis regurgitant, or similarly induced and placed in a Teflon bag for 12 h. The second leaf of all plants was then wounded 12h later and volatiles were collected for 600 min. (b) Sums of volatiles of the four major families of HIPVs released from WT and igl mutant plants are shown: green leaf volatiles, monoterpenes, homoterpenes and sesquiterpenes. Different letters indicate significant differences between treatments (Holm-Sidak post hoc tests, P<0.05; n=4). Error bars correspond to standard errors (±s.e.). For individual compounds, see Supplementary Figs 5 and 6.
Mentions: To further investigate the role of indole in plant priming, we used igl mutant plants in a bx1 mutant background46. The double mutant plants are impaired in the emission of indole, whereas the bx1 single mutant plants release indole at wild-type levels (Fig. 3). The activity of the Bx1 gene varies considerably across maize lines47, and includes naturally inactive alleles42. Consequently, the use of a bx1 mutant background enabled us to assess the role of IGL-produced indole without potential interference from other sources of free indole. First, we confirmed that igl mutants still release all other classes of volatiles in comparable amounts as plants carrying a wild-type Igl allele (WT). No systematic quantitative and qualitative differences were found between herbivore-induced volatile blends of WT and igl mutants (Fig. 3 and Supplementary Figs 3 and 4). To investigate whether indole is required for systemic priming in unharmed tissues of attacked plants, the first true leaf of igl mutant and WT seedlings was either left intact or subjected to elicitation treatment by mechanical wounding and application of oral caterpillar secretions. A subset of the elicited emitter leaves was then wrapped in a small Teflon bag that was sealed around the base of the leaf to minimize HIPV contact of undamaged systemic tissues. All plants were then placed in glass bottles and exposed to a continuous clean airflow of 0.3 l min−1 to prevent non-physiological build-up of HIPVs and to isolate the headspace of the different plants. Twelve hours later, all plants were challenged with a second elicitation treatment of leaf 2, after which HIPV emissions were measured at different time points (Fig. 4). During these volatile collections, all the first true leaves were enclosed in a clean Teflon bag to ensure that only volatiles from the second elicitation treatment were captured. No HIPVs except GLVs were detected at the beginning of the second elicitation treatment, indicating that 12 h after elicitation, there was no systemic release of HIPVs induced by the first elicitation treatment anymore48. Throughout the sampling period, indole-competent plants that were previously exposed to their own induced headspace released significantly higher total amounts of mono- and homoterpenes than genetically similar plants that were exposed to constitutive volatiles (Fig. 4, Holm-Sidak post hoc tests: P<0.05). These differences were mainly driven by linalool and DMNT (Supplementary Figs 5 and 6). When volatile exposure was interrupted with a Teflon bag, the systemic priming effect of mono- and homoterpenes disappeared, indicating that within-plant systemic priming of HIPVs in maize partially depends on previous HIPVs exposure. Moreover, indole-deficient mutant plants released the same total amounts of mono- and homoterpenes, irrespective of previous exposure to their own (indole-free) HIPV blend (Fig. 4), showing that indole is required for within-plant priming of the above volatiles.

Bottom Line: We therefore hypothesized that indole may be involved in airborne priming.Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming.These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Sciences, Department of Biology, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland.

ABSTRACT
Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

No MeSH data available.


Related in: MedlinePlus