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Journal of Chemical Ecology

, Volume 40, Issue 6, pp 632–642 | Cite as

The Mono - and Sesquiterpene Content of Aphid-Induced Galls on Pistacia palaestina is Not a Simple Reflection of Their Composition in Intact Leaves

  • Karin Rand
  • Einat Bar
  • Matan Ben-Ari
  • Efraim Lewinsohn
  • Moshe Inbar
Article

Abstract

Pistacia palaestina Boiss. (Anacardiaceae), a sibling species of P. terebinthus also known as turpentine tree or terebinth tree, is common in the Levant region. The aphid Baizongia pistaciae L. manipulates the leaves of the plant to form large galls, which provide both food and protection for its developing offspring. We analyzed the levels and composition of mono-and sesquiterpenes in both leaves and galls of ten naturally growing trees. Our results show that monoterpene hydrocarbons are the main constituents of P. palaestina leaves and galls, but terpene levels and composition vary among trees. Despite this inter-tree variation, terpene levels and compositions in galls from different trees resemble each other more than the patterns displayed by leaves from the same trees. Generally, galls contain 10 to 60 fold higher total terpene amounts than leaves, especially of the monoterpenes α-pinene and limonene. Conversely, the leaves generally accumulate more sesquiterpenes, in particular E-caryophyllene, germacrene D and δ-cadinene, in comparison to galls. Our results clearly show that the terpene pattern in the galls is not a simple reflection of that of the leaves and suggest that aphids have a strong impact on the metabolism of their host plant, possibly for their own defense.

Keywords

Baizongia Chemical defense Insect-plant relationship Terpenes Secondary compounds 

Notes

Acknowledgments

Constructive comments and suggestions of two anonymous reviewers are greatly appreciated. We thank Avi Koplovich for his help during sampling in the field. This research was supported by The Israel Science Foundation (grant No. 940/08 to M.I.), the US-Israel Binational Science foundation (grant No. 2012241), and Rene Karschon scholarship to K.R.

References

  1. Abrahamson WG, Weis AE (1997) Evolutionary ecology across three tropic levels: goldenrods, gallmakers, and natural enemies. Princeton University PressGoogle Scholar
  2. Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166. doi: 10.1007/s10886-005-0981-5 PubMedCrossRefGoogle Scholar
  3. Aloni R, Katz DA, Wool D (1989) Effect of the gall-forming aphid Slavum wertheimae on the differentiation of xylem in branches of Pistacia atlantica. Ann Bot 63:373–375Google Scholar
  4. Barra A, Coroneo VC, Dessi S, Cabras P, Angioni A (2007) Characterization of the volatile constituents in the essential oil of Pistacia lentiscus L. from different origins and its antifungal and antioxidant activity. J Agric Food Chem 55:7093–7098. doi: 10.1021/jf071129w PubMedCrossRefGoogle Scholar
  5. Ben-Shlomo R, Inbar M (2012) Patch size of gall-forming aphids: deme formation revisited. Popul Ecol 54:135–44CrossRefGoogle Scholar
  6. Bohlmann J, Crock J, Jetter R, Croteau R (1998) Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). Proc Natl Acad Sci U S A 95:6756–6761PubMedCentralPubMedCrossRefGoogle Scholar
  7. Burstein M, Wool D, Eshel A (1994) Sink strength and clone size of sympatric, gall-forming aphids. Eur J Entomol 91:57–61Google Scholar
  8. Caputo R, Mangoni L, Monaco P, Palumbo G (1979) Triterpenes from the galls of Pistacia palaestina. Phytochemistry 18:896–898. doi: 10.1016/0031-9422(79)80046-1 CrossRefGoogle Scholar
  9. Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? Am Midl Nat 110:225–234CrossRefGoogle Scholar
  10. Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902. doi: 10.1104/pp. 104.049981 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Fäldt J, Martin D, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol Biol 51:119–133. doi: 10.1023/A:1020714403780 PubMedCrossRefGoogle Scholar
  12. Flamini G, Bader A, Cioni PL, Katbeh-Bader A, Morelli I (2004) Composition of the essential oil of leaves, galls, and ripe and unripe fruits of Jordanian Pistacia palaestina Boiss. J Agric Food Chem 52:572–576. doi: 10.1021/jf034773t PubMedCrossRefGoogle Scholar
  13. Gerchman Y, Inbar M (2011) Distinct antimicrobial activities in aphid galls on Pistacia atlantica. Plant Signal Behav 6:2008–2012. doi: 10.4161/psb.6.12.18031 PubMedCrossRefGoogle Scholar
  14. Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328PubMedCrossRefGoogle Scholar
  15. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–14. doi: 10.1038/nchembio.2007.5 PubMedCrossRefGoogle Scholar
  16. Gomez SK, Cox MM, Bede JC, Inoue K, Alborn HT, Tumlinson JH, Korth L (2005) Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula. Arch Insect Biochem Physiol 58:114–27. doi: 10.1002/arch.20037 PubMedCrossRefGoogle Scholar
  17. Gourine N, Yousfi M, Bombarda I, Nadjemi B, Gaydou E (2010) Seasonal variation of chemical composition and antioxidant activity of essential oil from Pistacia atlantica Desf. leaves. J Am Oil Chem Soc 87:157–166. doi: 10.1007/s11746-009-1481-5 CrossRefGoogle Scholar
  18. Hall DE, Robert A, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk HB, Borchers CH, Bohlmann J (2011) An integrated genomic, proteomic and biochemical analysis of (+)–3–carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J 65:936–948. doi: 10.1111/j.1365-313X.2010.04478.x PubMedCrossRefGoogle Scholar
  19. 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. doi: 10.1007/s004420050401 CrossRefGoogle Scholar
  20. Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76:1506–1515. doi: 10.2307/1938152 CrossRefGoogle Scholar
  21. Inbar M, Izhaki I, Koplovich A, Lupo I, Silanikove N, Glasser T, Gerchman Y, Perevolotsky A, Lev-Yadun S (2010) Why do many galls have conspicuous colors? A new hypothesis. Arthropod Plant Interact 4:1–6. doi: 10.1007/s11829-009-9082-7 CrossRefGoogle Scholar
  22. Inbar M, Mayer RT, Doostdar H (2003) Induced activity of pathogenesis related (PR) proteins in aphid galls. Symbiosis 34:293–300Google Scholar
  23. Inbar M, Wink M, Wool D (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Mol Phylogenet Evol 32:504–511. doi: 10.1016/j.ympev.2004.01.006 PubMedCrossRefGoogle Scholar
  24. Joel D, Fahn A (1980) Ultrastructure of the resin ducts of Mangifera indica L. (Anacardiaceae). 2. Resin secretion in the primary stem ducts. Ann Bot 46:779–783Google Scholar
  25. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675. doi: 10.1111/j.1469-8137.2006.01716.x PubMedCrossRefGoogle Scholar
  26. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. doi: 10.1126/science.291.5511.2141 PubMedCrossRefGoogle Scholar
  27. Kurosu U, Aoki S, Fukatsu T (2003) Self-sacrificing gall repair by aphid nymphs. Proc R Soc Lond B 270:S12–S14. doi: 10.1098/rsbl.2003.0026 CrossRefGoogle Scholar
  28. Kurzfeld-Zexer L, Wool D, Inbar M (2010) Modification of tree architecture by a gall-forming aphid. Trees Struct Funct 24:13–18CrossRefGoogle Scholar
  29. Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological role. J Chem Ecol 20:1223–1280. doi: 10.1007/BF02059809 PubMedCrossRefGoogle Scholar
  30. Langenheim JH (1990) Plant resins: chemistry, evolution, ecology, and ethnobotany. Timber PressGoogle Scholar
  31. Larson KC, Whitham TG (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109:575–582. doi: 10.1007/s004420050119 CrossRefGoogle Scholar
  32. Lewinsohn E, Gijzen M, Muzika RM, Barton K, Croteau R (1993) Oleoresinosis in grand fir (Abies grandis) saplings and mature trees (modulation of this wound response by light and water stresses). Plant Physiol 101:1021–1028PubMedCentralPubMedGoogle Scholar
  33. Lewinsohn E, Gijzen M, Croteau R (1992) Wound-inducible pinene cyclase from grand fir: purification, characterization, and renaturation after SDS-PAGE. Arch Biochem Biophys 293:167–173PubMedCrossRefGoogle Scholar
  34. Lewinsohn E, Gijzen M, Crouteau R (1991) Defense mechanisms of conifers: differences in constitutive and wound-induced monoterpene biosynthesis among species. Plant Physiol 96:44–49PubMedCentralPubMedCrossRefGoogle Scholar
  35. Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway Spruce. Plant Physiol 132:1586–1599PubMedCentralPubMedCrossRefGoogle Scholar
  36. Martinez JJI (2010) Anti-insect effects of the gall wall of Baizongia pistaciae [L.], a gall-inducing aphid on Pistacia palaestina Boiss. Arthropod Plant Interact 4:29–34CrossRefGoogle Scholar
  37. Mumm R, Hilker M (2006) Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci 11:351–358. doi: 10.1016/j.tplants.2006.05.007 PubMedCrossRefGoogle Scholar
  38. Nabity PD, Haus MJ, Berenbaum MR, DeLucia EH (2013) Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. Proc Natl Acad Sci U S A 110:16663–8. doi: 10.1073/pnas.1220219110 PubMedCentralPubMedCrossRefGoogle Scholar
  39. Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of Willows by gall-inducing Sawflies. Proc Natl Acad Sci U S A 97:13184–13187PubMedCentralPubMedCrossRefGoogle Scholar
  40. Özcan MM, Tzakou O, Couladis M (2009) Essential oil composition of the turpentine tree (Pistacia terebinthus L.) fruits growing wild in Turkey. Food Chem 114:282–285. doi: 10.1016/j.foodchem.2008.08.094 CrossRefGoogle Scholar
  41. Paré P, Tumlinson J (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. doi: 10.1104/pp.114.4.1161 PubMedCentralPubMedGoogle Scholar
  42. Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insects galls. Environ Entomol 16:15–24Google Scholar
  43. Raffa KF (2014) Terpenes tell different tales at different scales: glimpses into the chemical ecology of conifer-bark beetle-microbial interactions. J Chem Ecol 40:1–20PubMedCrossRefGoogle Scholar
  44. Rehill BJ, Schultz JC (2003) Enhanced invertase activities in the galls of Hormaphis hamamelidis. J Chem Ecol 29:2703–2720PubMedCrossRefGoogle Scholar
  45. Rostás M, Maag D, Ikegami M, Inbar M (2013) Gall volatiles defend aphids against a browsing mammal. BMC Evol Biol 13:193. doi: 10.1186/1471-2148-13-193 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Steele CL, Lewinsohn E, Croteau R (1995) Induced oleoresin biosynthesis in grand fir as a defense against bark beetles. Proc Natl Acad Sci U S A 92:4164–4168PubMedCentralPubMedCrossRefGoogle Scholar
  47. Stireman JO, Devlin H, Abbot P (2012) Rampant host–and defensive phenotype–associated diversification in a goldenrod gall midge. J Evol Biol 25:1991–2004. doi: 10.1111/j.1420-9101.2012.02576.x PubMedCrossRefGoogle Scholar
  48. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522. doi: 10.1016/S0169-5347(03)00247-7 CrossRefGoogle Scholar
  49. Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr Opin Plant Biol 9:297–304. doi: 10.1016/j.pbi.2006.03.014 PubMedCrossRefGoogle Scholar
  50. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671. doi: 10.1111/j.1469-8137.2008.02392.x PubMedCrossRefGoogle Scholar
  51. Tzakou O, Bazos I, Yannitsaros A (2007) Volatile metabolites of Pistacia atlantica Desf. from Greece. Flavour Fragr 22:358–362. doi: 10.1002/ffj.1805 CrossRefGoogle Scholar
  52. Uematsu K, Kutsukake M, Fukatsu T, Shimada M, Shibao H (2010) Altruistic colony defense by menopausal female insects. Curr Biol 20:1182–1186. doi: 10.1016/j.cub.2010.04.057 PubMedCrossRefGoogle Scholar
  53. Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307. doi: 10.1016/S1369-5266(02)00264-9 PubMedCrossRefGoogle Scholar
  54. Wool D (2012) Autecology of Baizongia pistaciae (L.): a monographical study of a galling aphid. Isr J Entomol 41:67–93Google Scholar
  55. Wool D (2004) Galling aphids: specialization, biological complexity, and variation. Annu Rev Entomol 49:175–792. doi: 10.1146/annurev.ento.49.061802.123236 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Karin Rand
    • 1
    • 2
  • Einat Bar
    • 2
  • Matan Ben-Ari
    • 1
  • Efraim Lewinsohn
    • 2
  • Moshe Inbar
    • 1
  1. 1.Department of Evolutionary & Environmental BiologyUniversity of HaifaHaifaIsrael
  2. 2.Institute of Plant Sciences, Newe Ya’ar Research Center, Agricultural Research OrganizationRamat YishayIsrael

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