RAPID COMMUNICATION JASMONATE IN LEPIDOPTERAN EGGS AND NEONATES
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1 Journal of Chemical Ecology, Vol. 31, No. 11, November 2005 ( #2005) DOI: /s RAPID COMMUNICATION JOHN F. TOOKER* and CONSUELO M. DE MORAES Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA (Received August 4, 2005; Revised September 15, 2005; accepted September 16, 2005) Published Online September 30, 2005 Abstract Jasmonic acid (JA) is a key molecule initiating plant defensive responses to attack by pathogens and herbivores. This phytohormone is produced at sites of insect damage and is ingested by feeding insects, but its subsequent occurrence in insect tissues remains to be studied. We report the presence of JA in eggs and neonates of all nine lepidopteran species that we screened, representing four superfamilies and five families of Lepidoptera. Concentrations of JA in some lepidopteran species far exceeded those found in most plant species. Levels of JA varied significantly among species and between eggs and neonates of the same species. In some cases, eggs contained significantly more JA than neonates, but for at least one species (Lymantria dispar) neonates had more JA than their eggs despite lacking food upon emergence. The presence of JA in eggs and neonates across a wide taxonomic range may indicate that JA has an undescribed function in insects. Key Words Jasmonic acid, octodecanoid pathway, phytohormone. INTRODUCTION The phytohormone jasmonic acid (JA) is an important molecule in plants that has been implicated as a key signal initiating plant defensive responses to attack by herbivores and pathogens (Walling, 2000). Jasmonate is derived from linolenic acid via the octodecanoid pathway and activates defensive genes that initiate Binduced systemic resistance against insect herbivores and the release of volatile compounds that attract natural enemies to herbivore-infested plants (Walling, 2000). * To whom correspondence should be addressed. tooker@psu.edu /05/ /0 # 2005 Springer Science + Business Media, Inc.
2 2754 TOOKER AND DE MORAES While conducting another research project, we detected JA in eggs and neonates of the noctuid Heliothis virescens (Fabricius), prompting us to ask whether JA was present in eggs and neonates of other lepidopteran species. We are unaware of any previous studies that have examined levels of JA in insects; however, JA is produced by plants at sites of herbivory and is ingested by feeding lepidopterans (Walling, 2000; Li et al., 2002). In fact, JA activates detoxification genes in Helicoverpa zea (Boddie), apparently providing Bearlywarning signals that indicate imminent production by plants of toxic defensive compounds (Li et al., 2002). Here, we present evidence that this plant hormone is present in eggs and neonates of all lepidopteran species we screened, possibly indicating that JA plays an unknown functional role in insects. METHODS AND MATERIALS Insect Samples. We obtained eggs of nine moth species representing four superfamilies and five families of Lepidoptera (Table 1). Eight species were reared on artificial s, and one was field-collected. After oviposition, we weighed eggs and either collected them into FastPrep\ tubes (Qbiogene, Carlsbad, CA, USA) containing 1 g of Zirmil beads (1.1 mm; Saint-Gobain ZirPro, Mountainside, NJ, USA), freezing them at j80-c until processing (see below), or kept them in an incubator (25-C; 14:10 L/D; 60% RH) until hatching. Upon emergence, we collected neonates into FastPrep tubes with 1 g of Zirmil beads, weighing and freezing them at j80-c until processing. We observed no evidence of larval cannibalism. Because of the low mass of eggs and neonates (<0.1 mg), we combined multiple eggs or larvae into single samples (10 40 eggs per sample depending on mass; 5 10 neonates), processing five samples of both eggs and neonates for each lepidopteran species (total number of eggs analyzed per species: ; total neonates per species: 25 50). We also collected 10 samples (~0.5 mg each) of the setae, which form the matrix of Lymantria dispar egg masses; these setae originate from the abdomen of the ovipositing mother. Finally, we obtained from the rearing facilities (Table 1) samples of the artificial s used to rear these species, collecting and freezing five samples (~100 mg each) of each for processing. Extraction and Quantification of JA and SA. To extract and detect JA, we modified a previously described protocol (Schmelz et al., 2003, 2004) that derivatized carboxylic acids to methyl esters, which were isolated by using vapor phase extraction and analyzed by gas chromatography-mass spectrometry (GC-MS) with isobutane chemical ionization with selected-ion monitoring. Our method deviated from that of the previous authors in that we quantified amounts of methyl jasmonate (meja) by using standard curves made with the pure compound (Sigma-Aldrich, St. Louis, MO, USA), relying on internal standards
3 2755 TABLE 1. LEPIDOPTERAN SPECIES WHOSE EGGS AND NEONATES WERE ANALYZED FOR JASMONIC ACID (JA) Lepidopteran superfamily, family, and species Common name Source Diet ng JA/g (mean T SE) Gelechioidea Gelechiidae Gnorimoschema gallaesolidaginis (Riley) Pyraloidea Crambidae Diatraea saccharalis (Fabricius) Ostrinia nubilalis Hübner Sphingoidea Sphingidae Manduca sexta L. Noctuoidea Noctuidae Heliothis virescens (Fabricius) Helicoverpa zea (Boddie) Spodoptera exigua (Hübner) Spodoptera frugiperda (J.E. Smith) Centre Co., PA, USA Sugarcane borer European corn borer Tobacco hornworm Univ. of Illinois USDA c NC State Univ. Solidago altissima stems Tobacco budworm USDA d Pinto bean Corn earworm USDA d Pinto bean Beet USDA d Pinto bean armyworm Fall USDA d Pinto bean armyworm T a Wheat germ 42.4 T 23.9 b Corn-based 62.9 T 30.1 Wheat germ b 36.9 T 10.1 Lymantridae Lymantria dispar L. Gypsy moth USDA e Wheat germ b a Field-collected stems newly infested by G. gallaesolidaginis; unpublished data. b Each wheat germ is a species-specific formulation. c Ames, IA, USA. d Tifton, GA, USA. e Otis, MA, USA. to confirm derivatization and recovery. We also processed samples without the derivatization agent to verify that the meja we recovered was not itself present in eggs and neonates, but was derived from JA. To confirm the identity of meja in our samples, we analyzed extracts by GC-MS with electron ionization, comparing retention times and spectra with that of the pure compound. To normalize the data and stabilize variance, we square-root transformed our data and compared mean amounts of JA among samples by ANOVA
4 2756 TOOKER AND DE MORAES
5 2757 (Statistix, 2003), testing differences between eggs and neonates of each species as planned comparisons with the LSD means separation test (Sokal and Rohlf, 1995). RESULTS AND DISCUSSION We recovered JA from all the eggs, neonates, and s we analyzed (Figure 1). Mass spectra of meja recovered from lepidopterans and their s were nearly identical to that of the pure standard, confirming the identity of JA in our samples (Figure 1A). Moreover, we did not recover meja in absence of the derivatization agent, verifying that the meja we measured was derivatized from JA and was not itself present in samples. Remarkably, concentrations of JA in eggs and neonates were in some cases hundreds of times greater than the concentrations in their s (Table 1) and those typically found per gram of plant tissue (e.g., Schmelz et al., 2003). We suspect that the probable source of JA in eggs and neonates was the larval of ovipositing mothers and that the high concentrations resulted from bioaccumulation. If so, the presence of JA could conceivably be a nonadaptive by-product of larval feeding. Still, the presence of JA at such high concentrations in eggs and neonates raises the possibility that it may play some yet to be described functional role in these stages. Amounts of JA in eggs and neonates varied within and among species (Figure 1B; ANOVA: F 18,97 = 26.2, P < 0.001). Levels of JA were highest in eggs of the four noctuid species, and amounts of JA in eggs of these species were greater than amounts found in neonates (LSD, P < 0.05). Jasmonate levels in neonates were similar across noctuid species (LSD, P > 0.05), suggesting these species process JA similarly. Ostrinia nubilalis, D. saccharalis, and M. sexta had low levels of JA that were similar in eggs and neonates (LSD, P > 0.05), but L. dispar neonates had greater amounts of JA than their eggs (LSD, P < 0.05). Gnorimoschema gallaesolidaginis neonates also had greater amounts of JA than their eggs, but only at the 0.1 significance level. Neonates did not have available food upon emergence, but consumed a small portion of their egg chorion in the course of emergence. Chorions appear to contain small amounts of JA (unpublished data), FIG. 1. Jasmonic acid (JA) in lepidopteran species. (A) EI mass spectra of meja: the pure standard (top); derivatized from JA and recovered from Spodoptera frugiperda eggs (bottom). (B) JA recovered from eggs and neonates of nine lepidopteran species. Data shown are untransformed. Species marked with asterisks had significant differences in JA concentrations between eggs and neonates (*P < 0.1; **P < 0.05; ***P < 0.001). See text for details on statistics.
6 2758 TOOKER AND DE MORAES but not enough to account for the elevated levels of JA in neonates of these two species. After emerging, L. dispar larvae may also have consumed some of the setae that form the matrix of their egg mass. Setae also contain JA (Figure 1B), and further research will be needed to determine if setae are a source of JA for neonates. If chorions and setae are not significant sources of additional JA in L. dispar and G. gallaesolidaginis neonates, the possibility remains that larvae of these species synthesize JA. Other insect species are suspected to produce phytohormones to manipulate their host plants (e.g., Mapes and Davies, 2001), and further research should explore this possibility. All but one of the species we screened originated from laboratory colonies maintained on artificial s containing JA (Table 1); therefore, the presence of JA in eggs and neonates, or its presence at the high concentrations we measured, could conceivably be artifacts of these man-made s. The four species of noctuid exhibiting very high amounts of JA in their eggs were all reared on the same, which had relatively high concentrations of JA (Table 1). However, JA recovered from field-collected G. gallaesolidaginis indicates that artificial s are not solely responsible for JA in eggs and neonates. Moreover, concentrations of JA in the artificial s used (Table 1) appear to be comparable to those found in live plants and those used by other researchers (e.g., Li et al., 2002). Oviposition by some insect species can elicit plant volatile responses that attract natural enemies (Meiners and Hilker, 2000). Similar volatile emissions can be induced by applying exogenous JA, suggesting that JA plays a role in the initiation of plant defensive responses (Meiners and Hilker, 2000). Despite the recent implication of a protein in oviduct secretions as an elicitor of volatiles in response to oviposition (Hilker et al., 2005), our discovery of JA in lepidopteran eggs provides a plausible mechanism that could contribute to volatile production following oviposition. The consistent presence of JA in lepidopteran eggs and neonates raises the possibility that it may serve some adaptive function for the insects themselves. Significant similarities exist between hormone signals used in plant and animal systems (Schultz and Appel, 2004), so JA might have a signaling function in lepidopterans. Jasmonates convey messages between plants and insects, inducing detoxification genes in feeding caterpillars (Li et al., 2002). Moreover, JA has substantial structural similarities to eicosanoids, and to prostaglandins in particular, which serve a range of functions in invertebrates including mediating oviposition, salivary secretions, and immune responses (Stanley-Samuelson and Pedibhotla, 1996). Further research is underway to determine what role, if any, JA plays in lepidopteran eggs and neonates. Acknowledgements We thank J. Saunders, A. Conrad, and K. Cortellini for logistical support, E. Bogus and J. Engelberth for technical assistance, A. Boughton for discussion of our results,
7 2759 J. Lewis and T. Green (USDA, Tifton, GA), J. Dyer (USDA, Ames, IA), M. Grove (Penn State), J. Tanner (USDA, Otis, MA), B. Cash (North Carolina State Univ.), and M. Alleyne (Univ. of Illinois at Urbana Champaign) for eggs and/or. We thank M. C. Mescher, J. H. Tumlinson, J. C. Schultz, and two anonymous reviewers for helpful comments on the manuscript. The project was supported by the USDA National Research Initiative (# ), the David and Lucile Packard Foundation, and the Beckman Foundation. REFERENCES HILKER, M., STEIN, C., SCHRÖDER, R., VARAMA, M., and MUMM, R Insect egg deposition induces defence responses in Pinus sylvestris: characterisation of the elicitor. J. Exp. Biol. 208: LI, X., SCHULER, M. A., and BERENBAUM, M. R Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419: MAPES, C. C. and DAVIES, P. J Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol. 151: MEINERS, T. and HILKER, M Induction of plant synomones by oviposition of a phytophagous insect. J. Chem. Ecol. 26: SCHMELZ, E. A., ENGELBERTH, J., ALBORN, H. T., O DONNELL, P., SAMMONS, M., TOSHIMA, H., and TUMLINSON, J. H Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Nat. Acad. Sci. USA 100: SCHMELZ, E. A., ENGELBERTH, J., TUMLINSON, J. H., BLOCK, A., and ALBORN, H. T The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J. 39: SCHULTZ, J. C. and APPEL, H. M Cross-kingdom cross-talk: hormones shared by plants and their insect herbivores. Ecology 85: SOKAL, R. R. and ROHLF, F. J Biometry, 3rd edn. W.H. Freeman, New York. STANLEY-SAMUELSON, D. W. and PEDIBHOTLA, V. K What can we learn from prostaglandins and related eicosanoids in insects. Insect Biochem. Mol. Biol. 26: STATISTIX User Manual, Release 8.0. Analytical Software, Tallahassee, FL. WALLING, L. L The myriad plant responses to herbivores. J. Plant Growth Regul. 19:
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