Skip to main content
Springer Nature Link
Log in

Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Plants respond differently to damage by different herbivorous insects. We speculated that sibling herbivorous species with different host ranges might also influence plant responses differently. Such differences may be associated with the diet breadth (specialization) of herbivores within a feeding guild, and the specialist may cause less intensive plant responses than the generalist. The tobacco Nicotinana tabacum L. is the common host plant of a generalist Helicoverpa armigera (Hübner) and a specialist H. assulta Guenée (Lepidoptera, Noctuidae). The induced responses of tobacco to feeding of these two noctuid herbivores and mechanical wounding were compared. The results showed that the feeding of the specialist H. assulta and the generalist H. armigera resulted in the same inducible defensive system, but response intensity of plants was different to these two species. Inductions of jasmonic acid (JA), lipoxygenase (LOX), and proteinase inhibitors (PIs) were not significantly different concerning these two species, but H. assulta caused the less intensive foliar polyphenol oxidase (PPO) increase, more intensive nicotine and peroxidase (POD) increases in tobacco than H. armigera. The defensive response of plant to herbivores with different diet breadth seems to be more complicated than we expected, and the specialist does not necessarily cause less intensive plant responses than the generalist.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

JA:

Jasmonic acid

LOX:

Lipoxygenase

PI:

Proteinase inhibitor

POD:

Peroxidase

PPO:

Polyphenol oxidase

References

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500

    Article  Google Scholar 

  • Anderson MA, Van Heeswijck R, West J, Bateman K, Lee M, Christeller JT, McDonald G, Heath RL (1997) Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. J Insect Physiol 43:833–842

    Article  PubMed  Google Scholar 

  • Baldwin IT (1988) The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77:378–381

    Article  Google Scholar 

  • Baldwin IT, Ohnmeiss TE (1994a) Coordination of photosynthetic and alkaloidal responses to leaf damage in uninducible and inducible Nicotiana sylvestris. Ecology 75:1003–1014

    Article  Google Scholar 

  • Baldwin IT, Ohnmeiss TE (1994b) Swords into plowshares? Nicotiana sylvestris does not use nicotine as a nitrogen source under nitrogen-limited growth. Oecologia 8:385–392

    Article  Google Scholar 

  • Baldwin IT, Zhang Z, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397–404

    Article  CAS  Google Scholar 

  • Baldwin IT (1999) Inducible nicotine production in native Nicotiana as an example of adaptive phenotypic plasticity. J Chem Ecol 25:3–30

    Article  CAS  Google Scholar 

  • Bowers MD, Stamp NE (1993) Effects of plant age, genotype, and herbivory on plantago performance and chemistry. Ecology 74:1778–1791

    Article  Google Scholar 

  • Brown WE, Ryan CA (1984) Isolation and characterization of a wound induced trypsin inhibitor from alfalfa leaves. Biochemistry 23:3418–3422

    Article  PubMed  CAS  Google Scholar 

  • Butt VS (1980) Direct oxidases and related enzymes. In: Conn EE, Stumpf PK (eds) The biochemistry of plants, vol 2. Academic, New York, USA, pp 81–123

  • Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, Montagu MV, Inzé D, Camp WV (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci USA 95:5818–5823

    Article  PubMed  CAS  Google Scholar 

  • Chittoor JM, Leach JE, White FF (1999) Induction of peroxidase during defense against pathogens. In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC, Boca Raton, FL, USA, pp 171–193

    Google Scholar 

  • Constabel CP, Dergey DR, Ryan CA (1996) Phytochemical diversity and redundancy in ecological interactions. In: Romeo JT (eds) Recent advances in phytochemistry. Plenum, New York, USA, pp 231–235

    Google Scholar 

  • Constabel CP, Ryan CA (1998) A survey of wounded methyl jasmonate induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511

    Article  CAS  Google Scholar 

  • Farmer EE, Johnson RJ, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol 98:995–1002

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE (1994) Fatty acid signaling in plants and their associated microorganisms. Plant Mol Biol 26:1423–1437

    Article  PubMed  CAS  Google Scholar 

  • Felton GW, Donato K, Delvecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivore. J Chem Ecol 15:2667–2694

    Article  CAS  Google Scholar 

  • Gökmen V, Bahçeci S, Acar J (2002) Characterization of crude lipoxygenase extract from green pea using a modified spectrophotometric method. Eur Food Res Tech 215:42–45

    Article  CAS  Google Scholar 

  • Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuate III: fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717

    Article  PubMed  CAS  Google Scholar 

  • Hartley SE, Lawton JH (1987) Effects of different types of damage on the chemistry of birch foliage and the responses of birch-feeding insects. Oecologia 74:432–437

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121:153–162

    Article  PubMed  CAS  Google Scholar 

  • Kruzmane D, Jankevica L, Ievinsh G (2002) Effect of regurgitant from Leptinotarsa decemlineata on wound responses in Solanum tuberosum and Phaseolus vulgaris. Physiol Plant 115:577–584

    Article  PubMed  CAS  Google Scholar 

  • Liechti R, Farmer EE (2002) The jasmonate pathway. Science 296:1649–1650

    Article  PubMed  CAS  Google Scholar 

  • Marquis RJ (1992) The selective impact of herbivore. In: Fritz RS, Sims EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, IL, pp 301–325

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mueller MJ, Brodschelm W (1994) Quantification of jasmonic acid by capillary gas chromatography-negative chemical ionization-mass spectrometry. Anal Biochem 218:425–435

    Article  PubMed  CAS  Google Scholar 

  • Musser RO, Hum-Musser SM, Ekichensser H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defences. Nature 416:599–600

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in arabidopsis. Plant Cell 12:707–719

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE (2004) A Conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147

    Article  PubMed  CAS  Google Scholar 

  • Richardson M (1979) The complete amino acid sequence and the trypsin reactive (inhibitory) site of the major proteinase inhibitor from the fruits of aubergine (Solanum melongena L.). FEBS Lett 104:322–326

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. BBA-Proteins Proteom 1477:112–121

    CAS  Google Scholar 

  • Saunders JA, Blume DE (1981) Quantitation of major tobacco alkaloids by high performance liquid chromatography. J Chromatogr 205:147–154

    Article  CAS  Google Scholar 

  • Shi Q, Li C, Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L induced by mechanical wounding is regulated by auxin. J Exp Bot 57:2899–2907

    Article  PubMed  CAS  Google Scholar 

  • SPSS (2001) SPSS 11.01 for Windows. SPSS, Chicago, IL

  • Stout MJ, Workman KV, Duffey SS (1996) Identity, spatial distribution and variability of induced chemical responses in tomato plants. Entomol Exp Appl 79:255–271

    Article  Google Scholar 

  • Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Specificity of induced resistance in the tomato Lycopersicon esculentum. Oecologia 113:74–81

    Article  Google Scholar 

  • Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781

    Article  CAS  Google Scholar 

  • Voelckel C, Baldwin IT (2004) Generalist and specialist lepidopteran larvae elicit different transcriptional responses in Nicotiana attenuata, which correlate with larval FAC profiles. Ecol Lett 7:770–775

    Article  Google Scholar 

  • Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata IV. Insect-induced ethylene reduces jasmonate induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125:2189–2202

    Article  PubMed  CAS  Google Scholar 

  • Wu K (1985) A Lucerne-wheat germ diet for rearing the cotton bollworm, Heliothis armigera (Hübner). Acta Entomol Sinica 23:22–29

    Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Hui D, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuate demonstrates their function as anti herbivore defenses. Plant Physiol 134:1181–1190

    Article  PubMed  CAS  Google Scholar 

  • Zong N, Wang C (2004) Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chin Sci Bull 49:1596–1601

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Yan Yunhua and Feng Li for their technical assistance and for providing H. armigera and H. assulta eggs, Wang Honglei for help in GC-MS operation, Wang Rui for help in HPLC operation, and Shi Wuliang (China Agricultural University, Beijing) for offering JA standard. Especially, we thank Prof. Wilhelm Boland and Mrs. Birgit Schulze (Max Planck Institute of Chemical Ecology, Jena, Germany) for offering us the JA inter-standard [9, 10-2H2]dihydro-JA.We also thank Professor Ian T. Baldwin, Mr. Bernd Krock (Max Planck Institute of Chemical Ecology) and Prof. Zhao Cheng-hua (Zoology Institute, Chinese Academy of Science) for their help in the JA extract and assay method. Finally, we thank Dr. Kun Yan Zhu (Department of Entomology, Kansas State University, Manhattan, KS, USA) for his critical review of the manuscript. This work was supported by National Basic Research Program of China (2006CB102006), the Chinese Academy of Sciences (KSCX2-YW-N-006, CXTDS2005-4), and the National Natural Science Foundation of China (30571227, 30621003).

Author information

Authors and Affiliations

  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, The Chinese Academy of Sciences, 25 Beisihuanxi Road, Haidian, Beijing, 100080, China

    Na Zong & Chen-Zhu Wang

Authors
  1. Na Zong
    View author publications

    Search author on:PubMed Google Scholar

  2. Chen-Zhu Wang
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Chen-Zhu Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zong, N., Wang, CZ. Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226, 215–224 (2007). https://doi.org/10.1007/s00425-006-0459-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0459-x

Keywords