Planta

, Volume 222, Issue 2, pp 327–335

Systemic induction of volatile release in cotton: How specific is the signal to herbivory?

Original Article

Abstract

Plants attacked by herbivorous insects release chemical signals that attract natural enemies of the herbivores to the damaged plants. Feeding of Spodoptera exigua larvae on the lower leaves of cotton (Gossypium hirsutum L.) for multiple feeding periods of 9–12 h with a 12 h, interval in between when the caterpillars are removed overnight, will induce a systemic release of volatile compounds that is comparable to the volatiles released in response to continuous feeding damage on the lower leaves for several days. The systemic volatile release in response to herbivory can be mimicked by mechanically damaging the lower leaves and applying caterpillar oral secretion to the injured leaves over 4 days. Cotton plants that are only mechanically damaged systemically release significantly less β-pinene, myrcene, (Z)-3-hexenyl acetate, (E)-β-farnesene and (E,E)-α-farnesene after 4 days compared to plants damaged mechanically with application of caterpillar regurgitant. However, multiple 9–12 h mechanical damage alone induces a significantly higher systemic release of (Z)-3-hexenyl acetate, myrcene, (E)-β-ocimene, and (E)-β-farnesene after 4 days compared to undamaged control plants. This indicates that multiple mechanical damage alone cannot mimic completely the response induced by mechanically injuring the leaves and applying caterpillar regurgitant. A specific elicitor in the regurgitant of the caterpillar enhances the amount of several systemically released volatiles. Thus, the systemic release of volatile compounds by herbivore-damaged cotton plants appears to be regulated by at least two different mechanisms.

Keywords

Caterpillar regurgitant Gossypium Mechanical damage Spodoptera Systemic response Volatiles 

Abbreviations

SPOD

Spodoptera exigua larvae

SYST-SPOD

Volatiles collected from undamaged upper leaves of the caterpillar damaged plant

SYST-ART

Volatiles collected from undamaged upper leaves of the artificially damaged plant

SYST-ART & REG

Volatiles collected from undamaged upper leaves of the artificially damaged plant with application of regurgitant

SYST-CTRL

Volatiles collected from undamaged upper leaves of an undamaged control plant

References

  1. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles identified from beet armyworm oral secretion. Science 276:945–949Google Scholar
  2. Alborn HT, Jones TH, Stenhagen GS, Tumlinson JH (2000) Identification and synthesis of volicitin and related components from beet armyworm oral secretions. J Chem Ecol 26:203–220Google Scholar
  3. Benjamini Y (1988) Opening the box of a box plot. Amer Stat 42:257–262Google Scholar
  4. Bernasconi Ockroy ML, Turlings TCJ, Edwards PJ, Fritzsche-Hoballah ME, Ambrosetti L, Bassetti P, Dorn S (2001) Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agric Forest Entomol 3:201–209Google Scholar
  5. Caccioni DRL, Gardini F, Lanciotti R, Guerzoni ME (1997) Antifungal activity of natural volatile compounds in relation to their vapor pressure. Sciences des Aliments 17:21–34Google Scholar
  6. Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants – regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119Google Scholar
  7. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–773Google Scholar
  8. Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165Google Scholar
  9. Dicke M, van Beek TA, Posthumus MA, Ben Dom N, van Bokhoven H, de Groot AE (1990) Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. J Chem Ecol 16:381–396Google Scholar
  10. Elzen GW, Williams HJ, Bell AA, Stipanovic RD, Vinson SB (1985) Quantification of volatile terpenes of glanded and glandless Gossypium hirsutum L. cultivars and lines by gas chromatography. J Agric Food Chem 33:1079–1082Google Scholar
  11. Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134Google Scholar
  12. Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328Google Scholar
  13. Halitschke R, Keßler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417Google Scholar
  14. Halitschke R, Schittko U, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717Google Scholar
  15. Heath RR, Manukian A (1994) An automated system for use in collecting volatile chemicals released from plants. J Chem Ecol 20:593–608Google Scholar
  16. Hopke J, Donath J, Blechert S, Boland W (1994) Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a β-glucosidase and jasmonic acid. FEBS Lett 352:146–150Google Scholar
  17. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emission in Nature. Science 291:2141–2144Google Scholar
  18. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328Google Scholar
  19. King EG, Leppla NC (1984) Advances and challenges in insect rearing. Agriculture Research Service USDA. US Government Printing Office, WashingtonGoogle Scholar
  20. Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc Natl Acad Sci USA 91:11836–11840Google Scholar
  21. Mattiacci L, Dicke M, Posthumus MA (1995) Beta-glucosidase – an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92:2036–2040Google Scholar
  22. McCall PJ, Turlings TCJ, Loughrin J, Proveaux AT, Tumlinson JH (1994) Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings. J Chem Ecol 20:3039–3050Google Scholar
  23. McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435Google Scholar
  24. Paré PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167Google Scholar
  25. Paré PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975Google Scholar
  26. Pohnert G, Jung V, Haukioja E, Lempa K, Boland W (1999) New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars. Tetrahedron 55:11275–11280Google Scholar
  27. Röse USR, Tumlinson JH (2004) Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218:824–832Google Scholar
  28. Röse USR, Manukian A, Heath RR, Tumlinson JH (1996) Volatile semiochemicals released from undamaged cotton leaves: a systemic response of living plants to caterpillar damage. Plant Physiol 111:487–495Google Scholar
  29. Röse USR, Lewis WJ, Tumlinson JH (1998) Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps. J Chem Ecol 24:303–319Google Scholar
  30. Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44:569–589Google Scholar
  31. Takabayashi J, Dicke M, Takahashi S, Posthumus MA, Van Beek TA (1994) Leaf age affects composition of herbivore-induced synomones and attraction of predatory mites. J Chem Ecol 20:373–386Google Scholar
  32. Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading MAGoogle Scholar
  33. Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-induced corn. Proc Natl Acad Sci USA 89:8399–8402Google Scholar
  34. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host seeking parasitic wasps. Science 250:1251–1253Google Scholar
  35. Turlings TCJ, Tumlinson JH, Eller FJ, Lewis WJ (1991) Larval-damaged plants: source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts. Entomol Exp Appl 58:75–82Google Scholar
  36. Turlings TCJ, McCall PJ, Alborn HT, Tumlinson JH (1993) An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. J Chem Ecol 19:411–425Google Scholar
  37. Turlings TCJ, Loughrin JH, McCall PJ, Röse USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Center for Medical, Agricultural, and Veterinary Entomology, U.S. Department of AgricultureAgricultural Research ServiceGainesvilleUSA
  2. 2.Institut Phytosphäre (ICG-III)Forschungszentrum JülichJülichGermany
  3. 3.Department of EntomologyThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations