Abstract
Various plant antagonists appear to alter phytohormone levels for their own benefit. Among insects, gall-inducing species appear to influence phytohormones and it is widely believed that they alter levels of indole-3-acetic acid (IAA) to help produce their galls, but evidence exists for only a limited number of species. To further explore the role of phytohormones in gall formation, we measured levels of IAA and abscisic acid (ABA), a hormone involved in plant defenses and that can influence IAA, in tissues of control stems of Solidago altissima (Asteraceae) and those galled by Gnorimoschema gallaesolidaginis (Gelechiidae). This gall-inducing caterpillar species significantly altered the distribution of IAA in galls and the larvae themselves contained high concentrations of IAA. In contrast, the generalist caterpillar Heliothis virescens (Noctuidae) neither altered IAA nor accumulated significant concentrations of IAA, suggesting that G. gallaesolidaginis may have a distinctive influence over IAA. The gall-inducing caterpillars, particularly younger larvae, also contained high levels of ABA but did not increase levels of ABA, which is induced by herbivory of H. virescens. Because G. gallaesolidaginis also does not increase levels of other defense-related hormones, avoiding generalized plant defenses may facilitate gall induction and formation.
Similar content being viewed by others
References
Abrahamson WG, Weis AE (1987) Nutritional ecology of arthropod gall makers. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 238–258
Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers and natural enemies. Princeton University Press, Princeton
Abrahamson WG, McCrea KD, Whitwell AJ, Vernieri LA (1991) The role of phenolics in goldenrod ball gall resistance and formation. Biochem Syst Ecol 19:615–622
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166
Bandurski RS, Cohen JD, Slovin J, Reinecke DM (1995) Auxin biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer Academic Publishers, Dordrecht, pp 39–65
Beck EG (1953) The nature of the stimulus in the Solidago gall induced by the larva of Gnorimoschema gallaesolidaginis. Brookhaven Symp Biol 6:235–251
Bi JL, Murphy JB, Felton GW (1997) Does salicylic acid act as a signal in cotton for induced resistance to Helicoverpa zea? J Chem Ecol 23:1805–1818
Bostock RM (1999) Signal conflicts and synergies in induced resistance to multiple attackers. Physiol Mol Plant Pathol 55:99–109
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18
Davies PJ (2004) The plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer Academic Publishers, Dordrecht, pp 1–15
De Bruyn LJ, Vandevyvere J, Jaminé D, Prisen E (1998) The effects of gall formation by Lipara lucens (Diptera: Chloropidae) on its host Phragmites australis (Poaceae). In: Csóka G, Mattson WJ, Stone GN, Price PW (eds) The biology of gall-inducing arthropods. General Technical Report NC-199. USDA Forest Service, St. Paul, Minnesota, pp 173–187
Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D’Alessandro M, Turlings TCJ, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302
Felt EP (1940) Plant galls and gall makers. Comstock Publishing, Ithaca
Gagné RJ (1989) The plant-feeding gall midges of North America. Comstock Publishing, Ithaca
Giron D, Kaiser W, Imbault N, Casas J (2007) Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biol Letters 3:340–343
Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall former? Oecologia 113:492–501
Hori K (1992) Insect secretions and their effect on plant growth, with special reference to Hemipterans. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced plant galls. Oxford University Press, New York, pp 157–170
Jameson P (2000) Cytokinins and auxins in plant-pathogen interactions—an overview. Plant Grow Regul 32:369–380
Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. P Roy Soc B-Biol Sci B 277:2311–2319
Kernan A, Thornburg RW (1989) Auxin levels regulate the expression of a wound-inducible proteinase inhibitor II-chloramphenicol acetyl transferase gene fusion in vitro and in vivo. Plant Physiol 91:73–78
Li X, Schuler MA, Berenbaum MR (2002) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature 419:712–715
Mapes CC, Davies PJ (2001a) Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol 151:195–202
Mapes CC, Davies PJ (2001b) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytol 151:203–212
Miller ME (2000) A comparative taxonomic-natural history study of eight Neartic species of Gnorimoschema that induce stem galls on Asteraceae, including descriptions of three new species (Lepidoptera:Gelechiidae). Thomas Say Publicaton in Entomology: Monographs. Entomological Society of America, Lanham
Nason JD, Heard SB, Williams FR (2002) Host-associated genetic differentiation in the goldenrod elliptical-gall moth, Gnorimoschema gallaesolidaginis (Lepidoptera: Gelechiidae). Evolution 56:1475–1488
Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Nat Acad Sci USA 97:13184–13187
Ollerstam O, Larsson S (2003) Salicylic acid mediates resistance in the willow Salix viminalis against the gall midge Dasineura marginemtorquens. J Chem Ecol 29:163–174
Pena-Cortes H, Sánchez-Serrano JJ, Mertens R, Willmitzer L, Prat S (1989) Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. Proc Nat Acad Sci USA 86:9851–9855
Peña-Cortés H, Fisahn J, Willmitzer L (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Nat Acad Sci USA 92:4106–4113
Raman A, Schaefer CW, Withers TM (2005) Galls and gall-inducing arthropods: an overview of their biology, ecology and evolution. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Enfield, pp 1–33
Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379
Saniewski M, Ueda J, Miyamoto K (2002) Relationships between jasmonates and auxin in regulation of some physiological processes in higher plants. Acta Physiol Plant 24:211–220
SAS Institute (2003) SAS/STAT user’s guide for personal computers, release 9. SAS Institute, Cary
Schmelz E, Grebenok RJ, Galbraith DW, Bowers WS (1999) Insect-induced synthesis of phytoecdysteroids in spinach, Spinacia oleracea. J Chem Ecol 25:1739–1757
Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Nat Acad Sci USA 100:10552–10557
Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT (2004) The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J 39:790–808
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman, New York
Sopow SL, Shorthouse JD, Strong W, Quiring DT (2003) Evidence for long-distance, chemical gall induction by an insect. Ecol Lett 6:102–105
Stireman JO, Nason JD, Heard SB, Seehawer JM (2006) Cascading host associated genetic differentiation in parasitoids of phytophagous insects. Proc R Soc Lond B Biol Sci 273:523–530
Swiatek A, Lenjou M, Van Bockstaele M, Inze D, Van Onckelen H (2002) Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol 128:201–211
Tooker JF, De Moraes CM (2005) Jasmonate in lepidopteran eggs and neonates. J Chem Ecol 31:2753–2759
Tooker JF, De Moraes CM (2006) Jasmonate in lepidopteran larvae. J Chem Ecol 32:2321–2326
Tooker JF, De Moraes CM (2007a) Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol Entomol 32:153–161
Tooker JF, De Moraes CM (2007b) Jasmonate, salicylate, and benzoate in insect eggs. J Chem Ecol 33:331–343
Tooker JF, De Moraes CM (2008) Gall insects and indirect plant defenses: a case of active manipulation? Plant Sig Behav 3:503–504
Tooker JF, De Moraes CM (2009) A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Mol Plant-Microbe Inter 22:551–559
Tooker JF, De Moraes CM (2010) Feeding by Hessian fly (Mayetiola destructor [Say]) larvae increases levels of fatty acids and indole-3-acetic acid, but not hormones involved in plant-defense signaling. J Plant Grow Regul. doi:10.1007/s00344-010-9177-5
Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671
von Dahl CC, Baldwin IT (2004) Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuata. Physiol Plant 120:474–481
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216
Wood BW, Payne JA (1988) Growth regulators in chestnut shoot galls infected with oriental chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 17:915–920
Acknowledgments
We thank J. Saunders, E. Bogus, C. Wagner, and E. Smeyers for research assistance, W. Abrahamson and C. Frost for helpful comments on the manuscript, and the Chamber of Business and Industry of Centre County (PA) for access to their property. The project was supported by the David and Lucile Packard Foundation, the Beckman Foundation, the DuPont Young Investigator grant, the National Science Foundation (NSF CAREER no. 0643966), and the National Research Initiative of the United State Department of Agriculture Cooperative State Research, Education and Extension Service (#2002-35302-12375 [CMDM]; #2006-01823 [JFT]).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Anna-Karin Borg-Karlson.
Rights and permissions
About this article
Cite this article
Tooker, J.F., De Moraes, C.M. Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod-Plant Interactions 5, 115–124 (2011). https://doi.org/10.1007/s11829-010-9120-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-010-9120-5