Skip to main content

Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites

Oecologia volume 173, pages 1379–1386 (2013)Cite this article

Abstract

Induced defenses mediate interactions between parasites sharing the same host plant, but the outcomes of these interactions are challenging to predict because of spatiotemporal variation in plant responses and differences in defense pathways elicited by herbivores or pathogens. Dissecting these mediating factors necessitates an approach that encompasses a diversity of parasitic feeding styles and tracks interactions over space and time. We tested indirect plant-mediated relationships across three tomato (Solanum lycopersicum) consumers: (1) the fungal pathogen—powdery mildew, Oidium neolycopersici; (2) a sap-feeding insect—silverleaf whitefly, Bemisia tabaci; and (3) a chewing insect—the leaf miner, Tuta absoluta. Further, we evaluated insect/pathogen responses on local vs. systemic leaves and over short (1 day) vs. long (4 days) time scales. Overall, we documented: (1) a bi-directional negative effect between O. neolycopersici and B. tabaci; (2) an asymmetrical negative effect of B. tabaci on T. absoluta; and (3) an asymmetrical positive effect of T. absoluta on O. neolycopersici. Spatiotemporal patterns varied depending on the species pair (e.g., whitefly effects on leaf miner performance were highly localized to the induced leaf, whereas effects on pathogen growth were both local and systemic). These results highlight the context-dependent effects of induced defenses on a diverse community of tomato parasites. Notably, the outcomes correspond to those predicted by phytohormonal theory based on feeding guild differences with key implications for the recent European invasion by T. absoluta.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Blackmer JL, Byrne DN (1999) The effect of Bemisia tabaci on amino acid balance in Cucumis melo. Entomol Exp Appl 93:315–319

    CAS  Google Scholar 

  • Bompard A, Jaworski C, Bearez P, Desneux N (2013). Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55:433–440

    Google Scholar 

  • Bostock RM (1999) Signal conflicts and synergies in induced resistance to multiple attackers. Physiol Mol Plant Path 55:99–109

    Article  Google Scholar 

  • Brown JK, Frohlich DR, Rosell RC (1995) The sweet potato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annu Rev Entomol 40:511–534

    Article  CAS  Google Scholar 

  • Cagnotti CL, Viscarret MM, Riquelme MB, Botto EN, Carabajal LZ, Segura DF, Lopez SN (2012) Effects of X-rays on Tuta absoluta for use in inherited sterility programmes. J Pest Sci 85:413–421

    Google Scholar 

  • Campos ML, De Almeida M, Rossi ML, Martinelli AP, Junior CGL, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60:4347–4361

    PubMed  Article  CAS  Google Scholar 

  • Cooper WR, Goggin FL (2005) Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae. Entomol Exp Appl 115:107–115

    Article  CAS  Google Scholar 

  • Desneux N, O’Neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. B Entomol Res 98:631–639

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond–the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    PubMed  Article  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    PubMed  Article  CAS  Google Scholar 

  • Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    PubMed  Article  CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    PubMed  Article  CAS  Google Scholar 

  • Inbar M, Doostdar H, Sonoda RM, Leibee GL, Mayer RT (1998) Elicitors of plant defensive systems reduce insect densities and disease incidence. J Chem Ecol 24:135–149

    Article  CAS  Google Scholar 

  • Inbar M, Doostdar H, Leibee GL, Mayer RT (1999) The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. J Chem Ecol 25:1961–1979

    Article  CAS  Google Scholar 

  • Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448

    PubMed  Article  CAS  Google Scholar 

  • Jiao XG, Xie W, Wang SL, Wu QJ, Zhou L, Pan HP, Liu BM, Zhang YJ (2012) Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. J Pest Sci 85:423–430

    Google Scholar 

  • Jones H, Whipps JM, Gurr SJ (2001) The tomato powdery mildew fungus Oidium neolycopersici. Mol Plant Pathol 2:303–309

    PubMed  Article  CAS  Google Scholar 

  • Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Kaplan I, Thaler JS (2012) Phytohormone-mediated plant resistance and predation risk act independently on the population growth and wing formation of potato aphids, Macrosiphum euphorbiae. Arthropod Plant Interact 6:181–186

    Article  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    PubMed  Article  Google Scholar 

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

    Book  Google Scholar 

  • Kawazu K, Mochizuki A, Yukie S, Sugeno W, Murata M, Seo S, Mitsuhara I (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod Plant Interact 6:221–230

    Article  Google Scholar 

  • Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs: similarities and distinctions in responses to aphids. Plant Physiol 143:849–865

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Kessler A, Halitschke R (2007) Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Curr Opin Plant Biol 10:409–414

    PubMed  Article  CAS  Google Scholar 

  • Li C, Bai Y, Jacobsen E, Visser R, Lindhout P, Bonnema G (2006) Tomato defense to the powdery mildew fungus: differences in expression of genes in susceptible, monogenic- and polygenic resistance responses are mainly in timing. Plant Mol Biol 62:127–140

    PubMed  Article  CAS  Google Scholar 

  • Lynch ME, Kaplan I, Dively GP, Denno RF (2006) Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes. Ecol Appl 16:855–864

    PubMed  Article  Google Scholar 

  • Mayer RT, Inbar M, McKenzie CL, Shatters R, Borowicz V, Albrecht U, Powell CA, Doostdar H (2002) Multitrophic interactions of the silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Arch Insect Biochem 51:151–169

    Article  CAS  Google Scholar 

  • Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6:e18840

    PubMed  Article  CAS  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol S 36:81–105

    Article  Google Scholar 

  • Ohgushi T (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol Exp Appl 128:217–229

    Article  Google Scholar 

  • Orians CM (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242

    PubMed  Article  CAS  Google Scholar 

  • Orians CM, Pomerleau J, Ricco R (2000) Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485

    Article  CAS  Google Scholar 

  • Parrella G, Scassillo L, Giorgini M (2012) Evidence for a new genetic variant in the Bemisia tabaci species complex and the prevalence of the biotype Q in southern Italy. J Pest Sci 85:227–238

    Google Scholar 

  • Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Puthoff DP, Holzer FM, Perring TM, Walling LL (2010) Tomato pathogenesis-related protein genes are expressed in response to Trialeurodes vaporariorum and Bemisia tabaci biotype B feeding. J Chem Ecol 36:1271–1285

    PubMed  Article  CAS  Google Scholar 

  • Ramirez-Romero R, Desneux N, Chaufaux J, Kaiser L (2008) Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection. Pestic Biochem Phys 91:110–115

    Google Scholar 

  • Rodriguez-Saona C, Chalmers JA, Raj S, Thaler JS (2005) Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577

    PubMed  Article  Google Scholar 

  • Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175

    PubMed  Article  CAS  Google Scholar 

  • Soler R, Van der Putten WH, Harvey JA, Vet LEM, Dicke M, Bezemer TM (2012a) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. J Chem Ecol 38:755–767

    PubMed  Article  CAS  Google Scholar 

  • Soler R, Badenes-Pérez FR, Broekgaarden C, Zheng SJ, David A, Boland W, Dicke M (2012b) Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription. Funct Ecol 26:156–166

    Article  Google Scholar 

  • Soler R, Erb M, Kaplan I (2013) Long distance root–shoot signalling in plant–insect community interactions. Trends Plant Sci 18:149–156

    PubMed  Article  CAS  Google Scholar 

  • Stout MJ, Workman KV, Duffey SS (1996a) 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, Workman JS, Duffey SS (1996b) Temporal and ontogenetic aspects of protein induction in foliage of the tomato, Lycopersicon esculentum. Biochem Syst Ecol 24:611–625

    CAS  Google Scholar 

  • Stout MJ, Thaler JS, Thomma BPHJ (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689

    PubMed  Article  CAS  Google Scholar 

  • Tack AJM, Gripenberg S, Roslin T (2012) Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecol Lett 15:177–185

    PubMed  Article  Google Scholar 

  • Thaler JS, Fidantsef AL, Duffey SS, Bostock RM (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609

    Article  CAS  Google Scholar 

  • Thaler JS, Fidantsef AL, Bostock RM (2002) Antagonism between jasmonate- and salicylate- mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J Chem Ecol 28:1131–1159

    PubMed  Article  CAS  Google Scholar 

  • Thaler JS, Agrawal AA, Halitschke R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082

    PubMed  Article  Google Scholar 

  • Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629

    Article  Google Scholar 

  • Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Reg 19:195–216

    CAS  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    PubMed  Article  CAS  Google Scholar 

  • Zhang LP, Zhang GY, Zhang YJ, Zhang WJ, Liu Z (2005) Interspecific interactions between Bemisia tabaci (Hem., Aleyrodidae) and Liriomyza sativae (Dipt., Agromyzidae). J Appl Entom 129:443–446

    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 (USA) 106:21202–21207

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors declare that they have no conflict of interest and that all experiments were conducted in compliance with US law. We thank the editor (Roland Brandl), two anonymous reviewers for helpful comments on an earlier version of this manuscript, and Hélène Kazuro for assistance throughout the experiments. This work was supported by funds from the Environment and Agronomy department of INRA and from the French ministry of agriculture (CASDAR 10063) to ND.

Author information

Author notes

  1. Raphaëlle Mouttet

    Present address: Laboratoire de la Santé des Végétaux, unité entomologie et plantes invasives, ANSES, Campus international de Baillarguet, 34988, Montferrier-sur Lez, France

Affiliations

  1. French National Institute for Agricultural Research (INRA), ISA, 400 Route des Chappes, 06903, Sophia-Antipolis, France

    Raphaëlle Mouttet, Philippe Bearez, Edwige Amiens-Desneux & Nicolas Desneux

  2. Department of Entomology, Purdue University, 901 W. State St., West Lafayette, IN, USA

    Ian Kaplan

Authors
  1. Raphaëlle Mouttet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Bearez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edwige Amiens-Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicolas Desneux.

Additional information

Communicated by Roland Brandl.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mouttet, R., Kaplan, I., Bearez, P. et al. Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia 173, 1379–1386 (2013). https://doi.org/10.1007/s00442-013-2716-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2716-6

Keywords

  • Induced plant response
  • Invasive species
  • Plant–fungus–insect interactions
  • Trait-mediated indirect effects
  • Tripartite interactions