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Olfactory response of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) to volatiles induced by transgenic maize

Published online by Cambridge University Press:  16 June 2021

P. T. Nascimento Open the ORCID record for P. T. Nascimento [Opens in a new window] ,
M. A. M. Fadini Open the ORCID record for M. A. M. Fadini [Opens in a new window] ,
M. S. Rocha Open the ORCID record for M. S. Rocha [Opens in a new window] ,
C. S. F. Souza Open the ORCID record for C. S. F. Souza [Opens in a new window] ,
B. A. Barros Open the ORCID record for B. A. Barros [Opens in a new window] ,
J. O. F. Melo Open the ORCID record for J. O. F. Melo [Opens in a new window] ,
R. G. Von Pinho Open the ORCID record for R. G. Von Pinho [Opens in a new window]  and
F. H. Valicente Open the ORCID record for F. H. Valicente [Opens in a new window]
P. T. Nascimento*
Affiliation:
Universidade Federal de Lavras – UFLA, Lavras, Brasil
M. A. M. Fadini
Affiliation:
Universidade Federal de São João del-Rei – UFSJ, São João del-Rei, Brasil
M. S. Rocha
Affiliation:
Universidade Federal de São João del-Rei – UFSJ, São João del-Rei, Brasil
C. S. F. Souza
Affiliation:
Universidade Federal de Lavras – UFLA, Lavras, Brasil
B. A. Barros
Affiliation:
Empresa Brasileira de Pesquisa Agropecuária – Embrapa Milho e Sorgo, Sete Lagoas, Brasil
J. O. F. Melo
Affiliation:
Universidade Federal de São João del-Rei – UFSJ, São João del-Rei, Brasil
R. G. Von Pinho
Affiliation:
Universidade Federal de Lavras – UFLA, Lavras, Brasil
F. H. Valicente
Affiliation:
Empresa Brasileira de Pesquisa Agropecuária – Embrapa Milho e Sorgo, Sete Lagoas, Brasil
*
Author for correspondence: P. T. Nascimento, Email: priscillatavares2@hotmail.com
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Abstract

Plants not only respond to herbivorous damage but adjust their defense system after egg deposition by pest insects. Thereby, parasitoids use oviposition-induced plant volatiles to locate their hosts. We investigated the olfactory behavioral responses of Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) to volatile blends emitted by maize (Zea mays L.) with singular and stacked events after oviposition by Spodoptera frugiperda Smith, 1797 (Hymenoptera: Trichogrammatidae) moths. Additionally, we examined possible variations in gene expression and on oviposition-induced volatiles. We used a Y-tube olfactometer to test for the wasp responses to volatiles released by maize plants oviposited by S. frugiperda and not-oviposited plants. Using the real-time PCR technique (qRT-PCR), we analyzed the expression of lipoxygenase and three terpene synthases genes, which are enzymes involved in the synthesis of volatile compounds that attract parasitoids of S. frugiperda. Olfactometer tests showed that T. pretiosum is strongly attracted by volatiles from transgenic maize emitted by S. frugiperda oviposition (VTPRO 3, more than 75% individuals were attracted). The relative expression of genes TPS10, LOX e STC was higher in transgenic hybrids than in the conventional (isogenic line) hybrids. The GC-MS analysis revealed that some volatile compounds are released exclusively by transgenic maize. This study provides evidence that transgenic hybrids enhanced chemical cues under oviposition-induction and helped to increase T. pretiosum efficiency in S. frugiperda control. This finding shows that among the evaluated hybrids, genetically modified hybrids can improve the biological control programs, since they potentialize the egg parasitoid foraging, integrating pest management.

Keywords

Egg parasitoidgenetic manipulationqRT-PCRtrait stackingtritrophic interaction
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 6 , December 2021 , pp. 674 - 687
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Aljbory, Z and Chen, MS (2018) Indirect plant defense against insect herbivores: a review. Insect Science 25, 2–23.CrossRefGoogle ScholarPubMed
Beyaert, I, Köpke, D, Stiller, J, Hammerbacher, A, Yoneya, K, Schmidt, A, Gershenzon, J and Hilker, M et al. 2011) Can insect egg deposition ‘warn’ a plant of future feeding damage by herbivorous larvae? Proceedings of the Royal Society of London. Series B 279, 101–108. doi: http://doi.org/10.1098/rspb.2011.0468Google ScholarPubMed
Bonaventure, G, van Doorn, A and Baldwin, IT (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sciences 16, 294–299.CrossRefGoogle ScholarPubMed
Bravo, A, Gillb, SS and Soberón, M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon, Amsterdam 49, 423–435.CrossRefGoogle ScholarPubMed
Bruce, TJA (2010) Tackling the threat to food security caused by crop pests in the new millennium. Food Security 2, 133–141.CrossRefGoogle Scholar
Chen, MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Science 15, 101–114.CrossRefGoogle Scholar
Colazza, S, Fucarino, A, Peri, E, Salerno, G, Conti, E, et al. (2004) Insect oviposition induces volatile emission in herbaceous plants that attracts the egg parasitoid Trissolcus basalis. Journal of Experimental Biology 207, 47–53.CrossRefGoogle Scholar
Coll, AMV, Jacobi, VG, Fernandez, PC, Luft, AE, Virla, EG, Hill, JG and Catalán, CAN (2019) Volatiles mediate host-selection in the corn hoppers Dalbulus maidis (Hemiptera: Cicadellidae) and Peregrinus maidis (Hemiptera: Delphacidae). Bulletin of Entomological Research 8, 1–10.Google Scholar
Comas, C, Lumbierres, B, Pons, X and Albajes, R (2014) No effects of Bacillus thuringiensis maize on nontarget organisms in the field in Southern Europe: a metaanalysis of 26 arthropod taxa. Transgenic Research 23, 135–143.CrossRefGoogle Scholar
Crawley, MJ (2013) The R Book, 2nd Edn. Chichester: JohnWiley & Sons.Google Scholar
Cruz, I, Figueiredo, MLC, Silva, RB, Silva, IF, Paula, CS and Foster, JE (2012) Using sex pheromone traps in the decision-making process for pesticide application against fall armyworm (Spodoptera frugiperda [Smith] [Lepidoptera: Noctuidae]) larvae in maize. International Journal of Pest Management 58, 83–90.CrossRefGoogle Scholar
Dean, JM and De Moraes, CM (2006) Effects of genetic modification on herbivore-induced volatiles from maize. Journal of Chemical Ecology 32, 713–724.CrossRefGoogle ScholarPubMed
Dicke, M and Baldwin, IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15, 167–175.CrossRefGoogle ScholarPubMed
Dicke, M, van Beek, TA, Posthumus, MA, Ben, DN, van Bokhoven, H and de Groot, AE (1990) Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Involvement of host plant in its production. Journal of Chemical Ecology 16, 381–396.CrossRefGoogle Scholar
Diezel, C, von Dahl, CC, Gaquerel, E and Baldwin, IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiology 150, 1576–1586.CrossRefGoogle ScholarPubMed
Doss, RP, Oliver, JE, Proebsting, WM, Potter, SW, Kuy, SR, Clement, SL, Williamson, RT, Carney, JR and Devilbiss, ED (2000) Bruchins: insect-derived plant regulators that stimulate neoplasm formation. Proceedings of the National Academy of Sciences of the USA 97, 6218–6223.CrossRefGoogle ScholarPubMed
Fatouros, NE, Pashalidou, FG, Aponte Cordero, WV, van Loon, JJA, Mumm, R, Dicke, M, Hilker, M and Huigens, ME (2009) Anti-aphrodisiac compounds of male butterflies increase the risk of egg parasitoid attack by inducing plant synomone production. Journal of Chemical Ecology 35, 1373–1381.CrossRefGoogle ScholarPubMed
Fatouros, NE, Bukovinszkine'Kiss, G, Kalkers, LA, Soler, GR, Dicke, M, et al. (2005) Oviposition-induced plant cues: do they arrest Trichogramma wasps during host location? Entomologia Experimentalis et Applicata 115, 207–215.CrossRefGoogle Scholar
Fatouros, NE, Lucas-Barbosa, D, Weldegergis, BT, Pashalidou, FG, van Loon, JJA, et al. (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7, e43607.CrossRefGoogle ScholarPubMed
Head, GP, Carroll, MW, Evans, SP, Rule, DW, Willse, AR, Clark, TL, et al. (2017) Evaluation of SmartStax and SmartStax PRO maize against western cornrootworm and northern cornrootworm: efficacy and resistance management. Pest Management Science 73, 1883–1899.CrossRefGoogle ScholarPubMed
Hettenhausen, C, Baldwin, IT and Wu, J (2013) Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytologist 199, 787–799.CrossRefGoogle Scholar
Hilker, M and Meiners, T (2002) Chemoecology of Insect Eggs and Egg Deposition. Berlin: Blackwell Publishing.Google Scholar
Hilker, M and Meiners, T (2006) Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 26, 1379–1397.CrossRefGoogle Scholar
Hilker, M and Meiners, T (2010) How plants “notice” attack by herbivores. Biol Ver 85, 267–280.Google Scholar
Jiao, Y, Hu, X, Peng, Y, Wu, K, Romeis, J and Li, Y (2018) Bt rice plants may protect neighbouring non-Bt rice plants against the striped stem borer, Chilo suppressalis. Proceedings of the Royal Society of London. Series B 285, 20181283.Google Scholar
Kessler, A and Baldwin, IT (2002) Defensive function of herbivore-induced plant volatile emissions in nature. Science, Washington 291, 2141–2144.CrossRefGoogle Scholar
Kim, J, Tooker, JF, Luthe, DS, De Moraes, CM and Felton, GW (2012) Insect eggs can enhance wound response in plants: a study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS ONE 7, e37420.CrossRefGoogle ScholarPubMed
Leppik, E and Frérot, B (2014) Maize field odorscape during the oviposition flight of the European corn borer. Chemoecology 24, 221–228.CrossRefGoogle Scholar
Lin, C, Shen, B, Xu, Z, Kollner, TG, Degenhardt, J and Dooner, HK (2008) Characterization of the monoterpene synthase gene tps26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiology 146, 940–951.CrossRefGoogle ScholarPubMed
Liu, Q, Romeis, J, Yu, H, et al. (2015) Bt rice does not disrupt the host-searching behavior of the parasitoid Cotesia chilonis. Scientific Reports 5, 15295.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)). Method Methods 25, 402–408.CrossRefGoogle Scholar
Meiners, T and Hilker, M (2000) Induction of plant synomones by oviposition of a phytophagous insect. Journal of Chemical Ecology 26, 221–232.CrossRefGoogle Scholar
Michereff, MFF, Borges, M, Laumann, RA, Diniz, IR and Blassioli-Moraes, MC (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi. Entomologia Experimentalis et Applicata 147, 9–17. doi: 10.1111/eea.12043CrossRefGoogle Scholar
Moraes, MC, Laumann, RA, Aquino, MF, Paula, DP and Borges, M (2011) Effect of Bt genetic engineering on indirect defense in cotton via a tritrophic interaction. Transgenic Research 20, 99–107.CrossRefGoogle Scholar
Mumm, R and Dicke, M (2010) Variation in natural plant products and the attraction of bodyguards for indirect plant defense. Canadian Journal of Zoology 88, 628–667.CrossRefGoogle Scholar
Naranjo-Guevara, N, Peñaflor, MFGV, Cabezas-Guerrero, MF and Bento, JMS (2017) Nocturnal herbivore-induced plant volatiles attract the generalist predatory earwig Doru luteipes Scudder. Science of Nature 104, 77.CrossRefGoogle ScholarPubMed
Naranjo, SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Reviews Perspectives in Agriculture Veterinary Science Nutrition and Natural Resources 4, 11.CrossRefGoogle Scholar
Nascimento, PT, Fadini, MAM, Valicente, FH and Ribeiro, PEA (2018) Does Bacillus thuringiensis have adverse effects on the host egg location by parasitoid wasps?. Rev. Bras. entomol 62, 1–7.CrossRefGoogle Scholar
Nascimento, PT, Von Pinho, RG, Fadini, MAM, Souza, CSF and Valicente, FH (2020) Does singular and stacked corn affect choice behavior for oviposition and feed in Spodoptera frugiperda (Lepidoptera: Noctuidae)? Neotropical Entomology 49, 302–310.CrossRefGoogle ScholarPubMed
National Center for Information in Technology (NCBI, USA). Available at http://www.ncbi.nlm.nih.gov/Google Scholar
Nemchenko, A, Kunze, S, Feussner, I and Kolomiets, M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. Journal of Experimental Botany 57, 3767–3779.CrossRefGoogle ScholarPubMed
Ozawa, R, Arimura, G, Takabayashi, J, Shimoda, T and Nishioka, T (2000) Involvement of jasmonate and salicylaterelated signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant & Cell Physiology 41, 391–398.CrossRefGoogle ScholarPubMed
Penãflor, MF, Erb, M, Robert, CA, Miranda, LA, Werneburg, AG, Alda, DFC, Turlings, TCJ and Bento, JM (2011) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234, 207–215.CrossRefGoogle ScholarPubMed
Querino, RB, Ranyse, B and Zucchi, RA (2003) Caracterização morfológica de dez espécies de Trichogramma (Hymenoptera: Trichogrammatidae) registradas na América do Sul. Neotrop Entomol [online] 32, 597–613.CrossRefGoogle Scholar
R Core Team (2014) A Language and Environment for Statistical Computing. New Delhi, India: R Foundation for statistical computing. Vienna, p. 977.Google Scholar
Saravitz, DM and Siedow, JN (1996) The differential expression of wound-inducible lipoxygenase genes in soybean leaves. Plant Physiology 110, 287–299.CrossRefGoogle ScholarPubMed
Schmelz, EA, LeClere, S, Carroll, MJ, Alborn, HT and Teal, PE (2007) Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiology 144, 793–805.CrossRefGoogle ScholarPubMed
Schuler, TH, Potting, RP, Denholm, I and Poppy, GM (1999) Parasitoid behaviour and Bt plants. Nature 400, 825–829.CrossRefGoogle ScholarPubMed
Shen, B, Zheng, Z and Dooner H, K (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. Proceedings of the National Academy of Sciences of the United States of America 97, 14807–14812.CrossRefGoogle ScholarPubMed
Shu, Y, Romeis, J and Meissle, M (2018) No interactions of stacked Bt maize with the non-target aphid Rhopalosiphum padi and the spider mite Tetranychus urticae. Frontiers in Plant Science 9, 39.CrossRefGoogle ScholarPubMed
Storer, NP, Kubiszak, ME, Ed King, J, Thompson, GD and Santos, AC (2012) Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. Journal of Invertebrate Pathology 110, 294–300.CrossRefGoogle ScholarPubMed
Takabayashi, J and Dicke, M (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science 1, 109–113.CrossRefGoogle Scholar
Tamiru, A, Bruce, TJA, Woodcock, CM, Caulfield, JC, Midega, CAO, et al. (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters 14, 1075–1083.CrossRefGoogle ScholarPubMed
Tellez-Rodriguez, P, Raymond, B, Morán-Bertot, I, Rodríguez-Cabrera, L, Wright, DJ, Borroto, CG, et al. (2014) Strong oviposition preference for Bt over non-Bt maize in Spodoptera frugiperda and its implications for the evolution of resistance. BMC Biology 12, 48.CrossRefGoogle ScholarPubMed
Torres, JB, Ruberson, JR and Adang, MJ (2006) Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: a tritrophic analysis. Agricultural and Forest Entomology 8, 191–202.CrossRefGoogle Scholar
Turlings, TCJ and Erb, M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles. Mechanisms, ecological relevance, and application potential. Annual Review of Entomology 63, 433–452.CrossRefGoogle ScholarPubMed
Turlings, TCJ, Tumlinson, JH and Lewis, WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science (New York, N.Y.) 250, 1251–1253.CrossRefGoogle ScholarPubMed
Turlings, TCJ, Davison, AC and Tamo, C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiological Entomology 29, 45–55.CrossRefGoogle Scholar
Turlings, TC, Jeanbourquin, PM, Held, M and Degen, T (2005) Evaluating the C-odour emission of a Bt maize and its attractiveness to parasitic wasps. Transgenic Research 14, 807–816.CrossRefGoogle Scholar
Valicente, FH and Barreto, MR (2003) Bacillus thuringiensis survey in Brazil: geographical distribution and insecticidal activity against Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Neotropical Entomology 32, 639–644.CrossRefGoogle Scholar
Wasternack, C and Hause, B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Annals of Botany 111, 1021–1058.CrossRefGoogle ScholarPubMed
Willett, DS, Alborn, HT, Stelinski, LL and Shapiro-Ilan, DI (2018) Risk taking of educated nematodes. PLoS ONE 13, e0205804.CrossRefGoogle ScholarPubMed
Wu, J and Baldwin, IT (2010) New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44, 1–24.CrossRefGoogle ScholarPubMed