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.
Similar content being viewed by others
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
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 276:945–949
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 26:203–220
Benjamini Y (1988) Opening the box of a box plot. Amer Stat 42:257–262
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 3:201–209
Caccioni DRL, Gardini F, Lanciotti R, Guerzoni ME (1997) Antifungal activity of natural volatile compounds in relation to their vapor pressure. Sciences des Aliments 17:21–34
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 92:4114–4119
De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–773
Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165
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 16:381–396
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 33:1079–1082
Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134
Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328
Halitschke R, Keßler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417
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 125:711–717
Heath RR, Manukian A (1994) An automated system for use in collecting volatile chemicals released from plants. J Chem Ecol 20:593–608
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 352:146–150
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emission in Nature. Science 291:2141–2144
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328
King EG, Leppla NC (1984) Advances and challenges in insect rearing. Agriculture Research Service USDA. US Government Printing Office, Washington
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 91:11836–11840
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 92:2036–2040
McCall PJ, Turlings TCJ, Loughrin J, Proveaux AT, Tumlinson JH (1994) Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings. J Chem Ecol 20:3039–3050
McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435
Paré PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167
Paré PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975
Pohnert G, Jung V, Haukioja E, Lempa K, Boland W (1999) New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars. Tetrahedron 55:11275–11280
Röse USR, Tumlinson JH (2004) Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218:824–832
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 111:487–495
Röse USR, Lewis WJ, Tumlinson JH (1998) Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps. J Chem Ecol 24:303–319
Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44:569–589
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 20:373–386
Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading MA
Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-induced corn. Proc Natl Acad Sci USA 89:8399–8402
Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host seeking parasitic wasps. Science 250:1251–1253
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 58:75–82
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 19:411–425
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 92:4169–4174
Acknowledgments
We are grateful to Jürgen Engelberth and Consuelo De Moraes (both Penn State University, Department of Entomology, University Park, PA, USA) for their helpful comments concerning the initial manuscript. We thank the Delta and Pine Land Company (Hollandale, Scott, MS, USA) for donation of the seeds.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Röse, U.S.R., Tumlinson, J.H. Systemic induction of volatile release in cotton: How specific is the signal to herbivory?. Planta 222, 327–335 (2005). https://doi.org/10.1007/s00425-005-1528-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-005-1528-2