Skip to main content
Log in

Effect of Sequential Induction by Mamestra brassicae L. and Tetranychus urticae Koch on Lima Bean Plant Indirect Defense

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Attack by multiple herbivores often leads to modification of induced plant defenses compared to single herbivory, yet little is known about the effects on induced indirect plant defense. Here, we investigated the effect of sequential induction of plant defense by Mamestra brassicae caterpillar oral secretion and an infestation by Tetranychus urticae spider mites on the expression of indirect plant defense in Lima bean plants. The effect on indirect defense was assessed using behavior assays with the specialist predatory mite Phytoseiulus persimilis in an olfactometer, headspace analysis of 11 major herbivore-induced plant volatiles (HIPVs) including (E)-β-ocimene, and transcript levels of the corresponding gene Phaseolus lunatus (E)-β-ocimene synthase (PlOS). Predatory mites were found to distinguish between plants induced by spider mites and caterpillar oral secretion but not between plants with single spider mite infestation and plants induced by caterpillar oral secretion prior to spider mite infestation. Indeed, the volatile blends emitted by plants induced by spider mites only and the sequential induction treatment of caterpillar oral secretion followed by spider mite infestation, were similar. Our results suggest that plant indirect defense is not affected by previous treatment with oral secretion of M. brassicae caterpillars.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arimura GI, Ozawa R, Shimoda T, Nishloka T, Boland W, Takabayashi J (2000) Herbivory-induced volatiles elicit defence genes in Lima bean leaves. Nature 406:512–515

    Article  CAS  PubMed  Google Scholar 

  • Arimura GI, Köpke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on Lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146:965–973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brunissen L, Cherqui A, Pelletier Y, Vincent C, Giordanengo P (2009) Host-plant mediated interactions between two aphid species. Entomol Exp Appl 132:30–38

    Article  Google Scholar 

  • Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395

    Article  CAS  Google Scholar 

  • De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271

    Article  PubMed  Google Scholar 

  • De Boer JG, Posthumus MA, Dicke M (2004) Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J Chem Ecol 30:2215–2230

    Article  PubMed  Google Scholar 

  • De Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290

    Article  PubMed Central  PubMed  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Hervibore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, Van Beek TA, Posthumus MA, Ben Dom N, Van Bokhoven H, De Groot A (1990) Isolation and identification of volatile kairomone that affects acarine predator–prey interactions Involvement of host plant in its production. J Chem Ecol 16:381–396

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, Gols R, Ludeking D, Posthumus MA (1999) Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J Chem Ecol 25:1907–1922

    Article  CAS  Google Scholar 

  • Dicke M, Van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nature Chem Biol 5:317–324

    Article  CAS  Google Scholar 

  • Engelberth J, Viswanathan S, Engelberth MJ (2011) Low concentrations of salicylic acid stimulate insect elicitor responses in Zea mays seedlings. J Chem Ecol 37:263–266

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Foresti N, Turlings TCJ. 2010. A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol 10, art. no. 247.

  • Erb M, Robert CA, Hibbard BE, Turlings TC (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15

    Article  Google Scholar 

  • Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecology Lett 10:977–994

    Article  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  CAS  PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2004) Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J 38:639–649

    Article  CAS  PubMed  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kramer KJ, Muthukrishnan S (1997) Insect chitinases: molecular biology and potential use as biopesticides. Insect Biochem Molec Biol 27:887–900

    Article  CAS  Google Scholar 

  • Li C, Williams MM, Loh YT, Gyu IL, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130:494–503

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Margis-Pinheiro M, Metz-Boutigue MH, Awade A, de Tapia M, le Ret M, Burkard G (1991) Isolation of a complementary DNA encoding the bean PR4 chitinase: an acidic enzyme with an amino-terminus cysteine-rich domain. Plant Mol Biol 17:243–253

  • Mathur V, Ganta S, Raaijmakers CE, Reddy AS, Vet LEM, Van Dam NM (2011) Temporal dynamics of herbivore-induced responses in Brassica juncea and their effect on generalist and specialist herbivores. Entomol Exp Appl 139:215–225

    Article  Google Scholar 

  • Mathur V, Tytgat TOG, de Graaf RM, Kalia V, Sankara Reddy A, Vet LEM, van Dam NM (2013) Dealing with double trouble: consequences of single and double herbivory in Brassica juncea. Chemoecology 23:71–82

    Article  Google Scholar 

  • McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci U S A 94:5473–5477

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Menzel TR, Weldegergis BT, David A, Boland W, Gols, R, Van Loon, JJA, Dicke M. 2014. Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: transcription of a monoterpene synthase gene and volatile emission. J Exp Bot 65:4821–4831 doi:10.1093/jxb/eru242.

  • Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Canad J Zool 88:628–667

    Article  CAS  Google Scholar 

  • Ozawa R, Arimura GI, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398

    Article  CAS  PubMed  Google Scholar 

  • Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365

  • Rodriguez-Saona C, Crafts-Brandner SJ, Cañas LA (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057

    Article  CAS  PubMed  Google Scholar 

  • Schlumbaum A, Mauch F, Vögeli U, Boller T (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367

    Article  CAS  Google Scholar 

  • Schwartzberg EG, Böröczky K, Tumlinson JH (2011) Pea aphids, Acyrthosiphon Pisum, suppress induced plant iolatiles in broad bean, Vicia Faba. J Chem Ecol 37:1055–1062

    Article  CAS  PubMed  Google Scholar 

  • Shiojiri K, Takabayashi J, Yano S, Takafuji A (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Pop Ecol 43:23–29

    Article  Google Scholar 

  • Stam JM, Kroes A, Li Y, Gols R, Van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713

    Article  CAS  PubMed  Google Scholar 

  • Takabayashi J, Dicke M (1992) Response of predatory mites with different rearing histories to volatiles of uninfested plants. Entomol Exp Appl 64:187–193

  • Takabayashi J, Takahashi S, Dicke M, Posthumus MA (1995) Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J Chem Ecol 21:273–287

    Article  CAS  PubMed  Google Scholar 

  • Van Poecke RMP, Dicke M (2002) Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J Exp Bot 53:1793–1799

  • Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399

    Article  Google Scholar 

  • Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663

    Article  CAS  PubMed  Google Scholar 

  • Zhang PJ, Zheng SJ, Van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc Natl Acad Sci U S A 106:21202–21207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, Van Loon JJA, Gols R, Dicke M (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197:1291–1299

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcel Dicke.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 214 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Menzel, T.R., Huang, TY., Weldegergis, B.T. et al. Effect of Sequential Induction by Mamestra brassicae L. and Tetranychus urticae Koch on Lima Bean Plant Indirect Defense. J Chem Ecol 40, 977–985 (2014). https://doi.org/10.1007/s10886-014-0499-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0499-9

Keywords

Navigation