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Terpene synthases and their contribution to herbivore-induced volatile emission in western balsam poplar (Populus trichocarpa).

Irmisch S, Jiang Y, Chen F, Gershenzon J, Köllner TG - BMC Plant Biol. (2014)

Bottom Line: Gypsy moth-feeding on individual leaves of P. trichocarpa trees resulted in induced volatile emission from damaged leaves, but not from undamaged adjacent leaves.Our data indicate that the formation of herbivore-induced volatile terpenes in P. trichocarpa is mainly regulated by transcript accumulation of multiple TPS genes and is likely mediated by jasmonates.The specific local emission of volatiles from herbivore-damaged leaves might help herbivore enemies to find their hosts or prey in the tree canopy.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, Jena, Germany. koellner@ice.mpg.de.

ABSTRACT

Background: As a response to caterpillar feeding, poplar releases a complex mixture of volatiles which comprises several classes of compounds. Poplar volatiles have been reported to function as signals in plant-insect interactions and intra- and inter-plant communication. Although the volatile blend is dominated by mono- and sesquiterpenes, there is much to be learned about their formation in poplar.

Results: Here we report the terpene synthase (TPS) gene family of western balsam poplar (Populus trichocarpa) consisting of 38 members. Eleven TPS genes (PtTPS5-15) could be isolated from gypsy moth (Lymantria dispar)-damaged P. trichocarpa leaves and heterologous expression in Escherichia coli revealed TPS activity for ten of the encoded enzymes. Analysis of TPS transcript abundance in herbivore-damaged leaves and undamaged control leaves showed that seven of the genes, PtTPS6, PtTPS7, PtTPS9, PtTPS10, PtTPS12, PtTPS13 and PtTPS15, were significantly upregulated after herbivory. Gypsy moth-feeding on individual leaves of P. trichocarpa trees resulted in induced volatile emission from damaged leaves, but not from undamaged adjacent leaves. Moreover, the concentration of jasmonic acid and its isoleucine conjugates as well as PtTPS6 gene expression were exclusively increased in the damaged leaves, suggesting that no systemic induction occurred within the tree.

Conclusions: Our data indicate that the formation of herbivore-induced volatile terpenes in P. trichocarpa is mainly regulated by transcript accumulation of multiple TPS genes and is likely mediated by jasmonates. The specific local emission of volatiles from herbivore-damaged leaves might help herbivore enemies to find their hosts or prey in the tree canopy.

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Phytohormone concentrations in individualP. trichocarpaleaves after herbivory restricted to an apical or basal leaf or no herbivory. Single leaves were measured from either control trees (ctr), trees which received herbivory apically on leaf LPI3 (ha, herbivory apical) or basally on leaf LPI10 (hb, herbivory basal). Means and standard errors are shown (n = 5). To test for statistical significance between the treatments in one leaf position, a one way analysis of variance (ANOVA) was performed. Different letters show significant differences. t indicates a trend (0.05 < p < 0.1).
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Fig6: Phytohormone concentrations in individualP. trichocarpaleaves after herbivory restricted to an apical or basal leaf or no herbivory. Single leaves were measured from either control trees (ctr), trees which received herbivory apically on leaf LPI3 (ha, herbivory apical) or basally on leaf LPI10 (hb, herbivory basal). Means and standard errors are shown (n = 5). To test for statistical significance between the treatments in one leaf position, a one way analysis of variance (ANOVA) was performed. Different letters show significant differences. t indicates a trend (0.05 < p < 0.1).

Mentions: As herbivore-induced volatile emission is commonly mediated by jasmonates and other phytohormones [29-31], we measured the concentrations of these compounds in individual leaves (LPI 3–10) of trees which suffered herbivory either on an apical leaf (LPI 3) or a basal leaf (LPI10). As illustrated in Figure 6, undamaged control trees showed a gradient for abscisic acid (ABA; R2 = 0.23, p = 0.001) and salicylic acid (SA; R2 = 0.4, p = 0.009) within the tree with higher concentrations in younger leaves. Conversely, 12-oxo-phytodienoic acid (OPDA) concentrations increased in older basal leaves (R2 = 0.55, p = <0.0001) while jasmonic acid (JA) and its isoleucine conjugates (JA-Ile), (−)-jasmonoyl-L-isoleucine and (+)-7-iso-jasmonoyl-L-isoleucine, were equally distributed throughout the tree (p = 0.44; p = 0.76; p = 0.94, respectively). Upon herbivore damage, the concentrations of JA and JA-Ile conjugates increased significantly and specifically in the damaged leaves independent of leaf position compared to undamaged leaves of control trees and leaves within the same tree (Figure 6, Additional file 2: Table S6). A significant induction of SA, ABA and OPDA occurred only after apical damage in damaged leaves or below (Figure 6, Additional file 2: Table S6).Figure 6


Terpene synthases and their contribution to herbivore-induced volatile emission in western balsam poplar (Populus trichocarpa).

Irmisch S, Jiang Y, Chen F, Gershenzon J, Köllner TG - BMC Plant Biol. (2014)

Phytohormone concentrations in individualP. trichocarpaleaves after herbivory restricted to an apical or basal leaf or no herbivory. Single leaves were measured from either control trees (ctr), trees which received herbivory apically on leaf LPI3 (ha, herbivory apical) or basally on leaf LPI10 (hb, herbivory basal). Means and standard errors are shown (n = 5). To test for statistical significance between the treatments in one leaf position, a one way analysis of variance (ANOVA) was performed. Different letters show significant differences. t indicates a trend (0.05 < p < 0.1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4197230&req=5

Fig6: Phytohormone concentrations in individualP. trichocarpaleaves after herbivory restricted to an apical or basal leaf or no herbivory. Single leaves were measured from either control trees (ctr), trees which received herbivory apically on leaf LPI3 (ha, herbivory apical) or basally on leaf LPI10 (hb, herbivory basal). Means and standard errors are shown (n = 5). To test for statistical significance between the treatments in one leaf position, a one way analysis of variance (ANOVA) was performed. Different letters show significant differences. t indicates a trend (0.05 < p < 0.1).
Mentions: As herbivore-induced volatile emission is commonly mediated by jasmonates and other phytohormones [29-31], we measured the concentrations of these compounds in individual leaves (LPI 3–10) of trees which suffered herbivory either on an apical leaf (LPI 3) or a basal leaf (LPI10). As illustrated in Figure 6, undamaged control trees showed a gradient for abscisic acid (ABA; R2 = 0.23, p = 0.001) and salicylic acid (SA; R2 = 0.4, p = 0.009) within the tree with higher concentrations in younger leaves. Conversely, 12-oxo-phytodienoic acid (OPDA) concentrations increased in older basal leaves (R2 = 0.55, p = <0.0001) while jasmonic acid (JA) and its isoleucine conjugates (JA-Ile), (−)-jasmonoyl-L-isoleucine and (+)-7-iso-jasmonoyl-L-isoleucine, were equally distributed throughout the tree (p = 0.44; p = 0.76; p = 0.94, respectively). Upon herbivore damage, the concentrations of JA and JA-Ile conjugates increased significantly and specifically in the damaged leaves independent of leaf position compared to undamaged leaves of control trees and leaves within the same tree (Figure 6, Additional file 2: Table S6). A significant induction of SA, ABA and OPDA occurred only after apical damage in damaged leaves or below (Figure 6, Additional file 2: Table S6).Figure 6

Bottom Line: Gypsy moth-feeding on individual leaves of P. trichocarpa trees resulted in induced volatile emission from damaged leaves, but not from undamaged adjacent leaves.Our data indicate that the formation of herbivore-induced volatile terpenes in P. trichocarpa is mainly regulated by transcript accumulation of multiple TPS genes and is likely mediated by jasmonates.The specific local emission of volatiles from herbivore-damaged leaves might help herbivore enemies to find their hosts or prey in the tree canopy.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, Jena, Germany. koellner@ice.mpg.de.

ABSTRACT

Background: As a response to caterpillar feeding, poplar releases a complex mixture of volatiles which comprises several classes of compounds. Poplar volatiles have been reported to function as signals in plant-insect interactions and intra- and inter-plant communication. Although the volatile blend is dominated by mono- and sesquiterpenes, there is much to be learned about their formation in poplar.

Results: Here we report the terpene synthase (TPS) gene family of western balsam poplar (Populus trichocarpa) consisting of 38 members. Eleven TPS genes (PtTPS5-15) could be isolated from gypsy moth (Lymantria dispar)-damaged P. trichocarpa leaves and heterologous expression in Escherichia coli revealed TPS activity for ten of the encoded enzymes. Analysis of TPS transcript abundance in herbivore-damaged leaves and undamaged control leaves showed that seven of the genes, PtTPS6, PtTPS7, PtTPS9, PtTPS10, PtTPS12, PtTPS13 and PtTPS15, were significantly upregulated after herbivory. Gypsy moth-feeding on individual leaves of P. trichocarpa trees resulted in induced volatile emission from damaged leaves, but not from undamaged adjacent leaves. Moreover, the concentration of jasmonic acid and its isoleucine conjugates as well as PtTPS6 gene expression were exclusively increased in the damaged leaves, suggesting that no systemic induction occurred within the tree.

Conclusions: Our data indicate that the formation of herbivore-induced volatile terpenes in P. trichocarpa is mainly regulated by transcript accumulation of multiple TPS genes and is likely mediated by jasmonates. The specific local emission of volatiles from herbivore-damaged leaves might help herbivore enemies to find their hosts or prey in the tree canopy.

Show MeSH
Related in: MedlinePlus