Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (−)‐germacrene D synthase, PtdTPS1

Abstract

These authors contributed equally to this work. SummaryFeeding forest tent caterpillars (FTCs) induced local and systemic diurnal emissions of (À)-germacrene D, along with (E )-b-ocimene, linalool, (E )-4,8-dimethyl-1,3,7-nonatriene (DMNT), benzene cyanide, and (E,E )-a-farnesene, from leaves of hybrid poplar. FTC feeding induced substantially higher levels of volatiles in local and systemic leaves than did mechanical wounding. A full-length poplar sesquiterpene synthase cDNA (PtdTPS1) was isolated and functionally identi®ed as (À)-germacrene D synthase. Expression of PtdTPS1, expression of genes of early, intermediate and late steps in terpenoid biosynthesis, and expression of a lipoxygenase gene (PtdLOX1) were analyzed in local FTC-infested and systemic leaves. Transcript levels of PtdTPS1 and PtdLOX1 were strongly increased in response to herbivory. PtdTPS1 was also induced by mechanical wounding or by methyl jasmonate (MeJA) treatment. FTC feeding did not affect transcript levels of 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), 1-deoxy-D-xylulose 5-phosphate reductoisomerase (DXR), and isoprene synthase (IPS). Two other TPS genes, PtdTPS2 and PtTPS3, and farnesyl diphosphate synthase were only very transiently induced. These results illustrate differential expression of terpenoid pathway genes in response to insect feeding and a key function of (À)-germacrene D synthase PtdTPS1 for herbivore-induced local and systemic volatile emissions in hybrid poplar. FTC-induced transcripts of PtdTPS1 followed diurnal rhythm. Spatial patterns of FTC-induced PtdTPS1 transcript accumulation revealed acropetal but not basipetal direction of the systemic response. Implications for tritrophic poplar-FTCpredator/parasitoid interactions are discussed.

Two Herbivore-Induced Cytochrome P450 Enzymes CYP79D6 and CYP79D7 Catalyze the Formation of Volatile Aldoximes Involved in Poplar Defense

“…For example, feeding of forest tent caterpillars (Malacosoma disstria) on P. trichocarpa 3 deltoides resulted in local and systemic emission of a complex volatile blend comprising mainly monoand sesquiterpenes, but also benzyl cyanide (Arimura et al, 2004). Here, we demonstrated that aldoximes and related nitrogen-containing volatiles in P. trichocarpa were only produced and released from herbivore-damaged leaves and not from undamaged neighboring leaves (Figures 6B and 6C; see Supplemental Table 5 online).…”

Functional Characterization of Nine Norway Spruce TPS Genes and Evolution of Gymnosperm Terpene Synthases of the TPS-d Subfamily

“…However, the known grand fir and few loblolly pine TPS genes cannot account for all oleoresin terpenoids in conifers. Nothing is known about TPS genes of induced volatile emissions in conifers , and only a few TPS genes of herbivore-induced terpene emission are known in other angiosperm plants (Shen et al, 2000;Schnee et al, 2002;Fäldt et al, 2003a;Arimura et al, 2004). Species of spruce (Picea spp.…”

A genomic approach to characterization of the Citrus terpene synthase gene family

“…Accordingly, tent caterpillars feeding on leaves of hybrid poplar induced local and systemic emissions of (-)-germacrene D, (E)-β-ocimene, linalool, (E)-4,8-dimethyl-1,3,7-nonatriene, benzene cyanide, and (E,E)-α-farnesene (Arimura et al, 2004b). This emission of volatile terpene compounds was correlated with an increase in transcription levels of a sesquiterpene synthase greatly induced in response to herbivory (Arimura et al, 2004a). We found putative Citrus homologs to terpene synthases expressed preferentially in leaves (Figure 4).…”