Domaines de recherche

We mainly study the chemical ecology of plant-insect interactions. By unraveling how plants defend themselves against insect attacks and how specialized insects have evolved to circumvent these defenses, we hope to provide ideas for novel, sustainable strategies for the control of agricultural pests.

Quite some years ago, we revealed that plants under attack by caterpillars initiate a systemic release of specific volatiles. This plant response results in an odour that serves as a signal used by parasitic wasps to locate their hosts, whereas several herbivorous insects are repelled by the odour. Studies into the mechanisms of the plant response showed that it is greatly enhanced by factors in the oral secretions of herbivorous insects. This work initially started at the USDA in Gainesville, Florida, where we eventually isolated and identified a powerful elicitor from the regurgitant of Spodoptera larvae, a fatty acid-amino acid conjugate, which was named volicitin. We also studied how caterpillar-induced volatiles can prime neighboring plants to prepare for incoming attack, and we identified indole as a key inducible volatile in such interactions among maize plants.

Our work at the University of Neuchâtel on root signals revealed that root feeding by larvae of the important maize pest Diabrotica virgifera virgifera results in the release of E-(β)-caryophyllene. This sesquiterpene was identified with the help of our collaborators at the Max Planck Institute for Chemical Ecology in Jena and was found to be highly attractive to entomopatogenic nematodes. Many American maize lines do not release this signal and this is reflected in poor attraction of and infection by the nematodes in field experiments conducted with the help of scientists at CABI Bioscience, Switzerland. By genetically transforming a non-emitting maize line we obtained ultimate evidence for the key role of E-(β)-caryophyllene in the attraction of entomopathogenic nematodes.

Now that we have obtained considerable insight into the ecology and the mechanisms of these above- and belowground multi-trophic level interactions, we are applying this knowledge to better understand the evolutionary, ecological and applicable aspects of chemical signalling between plants and insects. It is envisioned that our studies will contribute to the development of sustainable pest management practices inspired by nature. 

Our current work revolves around four objectives:

• Deciphering the odorous language used by plants that are under insect or pathogen attack, with the ultimate objective to use sensors for odour-based, real-time detection of pest and diseases.
• Understanding the inducible volatile signals that cotton plants emit and that trigger defense responses in neighboring plants.
• Develop, in collaboration with CABI-Switzerland, a new formulation of entomopathogenic nematodes against the invasive fall armyworm, which is devastating maize fields in Africa and Asia.
• Unraveling the intricacies of how different stages of Diabrotica beetles sequester defense compounds for their own protection.

Publications

Complete publication list

ORCiD

scopus author ID

Publication list for the last five years

2023

Zhou A, Zhao J, Jing, Liu Y, Zhang Z, Wang M, Turlings TCJ, Zhang P-J 2023. Mealybug salivary microbes inhibit inducible plant defenses. Pest Management Science (in press)

Briones-May Y, Quijano-Medina T, Pérez-Niño B, Benrey B, Turlings TCJ, Bustos-Segura C, Abdala-Roberts L 2023. Soil salinization disrupts the effect of plant-plant signaling on extra-floral nectar induction in wild cotton. Oecologia (accepted).

Chappuis L, Egger A, Roeder G, Glauser G, Jaffuel G, Benrey B, Abdala-Roberts L, Clancy MV, Turlings TCJ, Bustos-Segura C 2023. Experimental growth conditions affect direct and indirect defences in two cotton species. Journal of Chemical Ecology (in press)

Liu Q, Turlings TCJ, YLi Y 2023. Can herbivores sharing the same host plant be mutualists? Trends in Ecology & Evolution Forum paper Online: https://doi.org/10.1016/j.tree.2023.01.018

Zeng J, Ye W, Hu W, Kuai P, Xiao W, Jian Y, Turlings TCJ, Lou Y 2023. The N-terminal subunit of vitellogenin in planthopper eggs and saliva induces defenses in rice. New Phytologist Online: https://doi.org/10.1111/nph.18791

la Forgia D, Martin C, Turlings TCJ, Verheggen F 2023. 2‑Pentylfuran: an aggregation attractant for wireworms. Arthropod-Plant Interactions Online: https://doi.org/10.1007/s11829-023-09958-9

Mamin M, Vallat A, Turlings TCJ 2023. Cotton plants as ideal models for teaching and research on inducible direct plant defenses. Frontiers Ecology and Evolution 11: 1119472. https://doi.org/10.3389/fevo.2023.1119472

Machado RAR, Bhat AH, Fallet P, Turlings TCJ, Kajuga J, Yan X, Toepfer S 2023. Xenorhabdus bovienii subsp. africana subsp. nov., isolated from Steinernema africanum entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology 54: e2022-1. https://doi.org/10.2478/jofnem-2022-0049

Xu T, Zhang N, Xu M, Glauser G, Turlings TCJ, Chen L 2023. Revisiting the trail pheromone components of the red imported fire ant, Solenopsis invicta Buren. Insect Science 30: 161-172. https://doi.org/10.1111/1744-7917.13047

Yao C, Du L, Liu QG, Hu X, Ye W, Turlings TCJ, Li Y 2023. Stemborer-induced rice plant volatiles boost direct and indirect resistance in neighboring plants. New Phytologist 237: 2375-2387. https://doi.org/10.1111/nph.18548

Clancy MV, Mamin M, Flückiger G, Quijano-Medina T, Pérez Niño B, Abdala-Roberts L, Turlings TCJ, Bustos-Segura C 2023. Terpene chemotypes in wild cotton (Gossypium hirsutum) from the Yucatan Peninsula. Phytochemistry 205: 113454

2022

Duhin A, Machado RAR, Turlings TCJ, Röder G 2022. Early land plants: Plentiful but neglected nutritional resources for herbivores? Ecology and Evolution 12: e9617 https://doi.org/10.1002/ece3.9617

Machado RAR, Bhat AH, Abolafia J, E. Shokoohi, Fallet P, Turlings TCJ, Tarasco E, Půža V, Kajuga J, Yan X, Toepfer S 2022. Steinernema africanum n. sp. (Rhabditida, Steinernematidae), a new entomopathogenic nematode species isolated from the Republic of Rwanda. Journal of Nematology 54: e2022-1, DOI: 10.2478/jofnem-2022-0049  

Fallet P, Bazagwira D, Guenat JM, Bustos-Segura CKarangwa P, Mukundwa IP, Kajuga J, Degen T, Toepfer S, Turlings TCJ 2022. Laboratory and field trials reveal the potential of a gel formulation of entomopathogenic nematodes for the biological control of fall armyworm caterpillars (Spodoptera frugiperda). Biological Control 176: https://doi.org/10.1016/j.biocontrol.2022.105086

Turlings TCJ, Degen T 2022. The role of herbivore-induced plant volatiles in trophic interactions: The Swiss Connection. Chimia 76, 900, https://doi.org/10.2533/chimia.2022.900

Bruno P, Arce CCM, Machado RAR, Besomi G, Spescha A, Glauser G, Jaccard C, Benrey B, Turlings TCJ 2022. Sequestration of cucurbitacins from cucumber plants by Diabrotica balteata larvae provides little protection against biological control agents. Journal of Pest Science: https://doi.org/10.1007/s10340-022-01568-3

Chen C, Q. Su, G. Yuan, X. Shi, T.C.J. Turlings, Y. Zhang 2022. Suppression of terpenoid synthesis in tomato plants by a begomovirus enhances the attraction of its vector. Authorea Preprints: DOI: 10.22541/au.165163867.73463070/v1

Ye W, Bustos-Segura C, Degen T, Erb M, Turlings TCJ 2022. Belowground and aboveground herbivory differentially affect the transcriptome in roots and shoots of maize. Plant Direct 6(7): e426  https://doi.org/10.1002/pld3.426

Fallet P, De Gianni L, Machado RAR, Bruno P, Bernal J, Karangwa P, Kajuga J, Waweru B, Bazagwira D, Degen T, Toepfer S, Turlings TCJ 2022. Comparative screening of Mexican, Rwandan and commercial entomopathogenic nematodes to be used against invasive fall armyworm,Spodoptera frugiperda. Insects 13: 205 

Jaccard C, Marguier NT, Arce CCM, Bruno P, Glauser G, Turlings TCJ, Benrey B 2022. The effect of squash domestication on a belowground tritrophic interaction. Plant-Environment Interactions 3: 28-39. https://doi.org/10.1002/pei3.10071

Jaffuel G, Krishnamani S, Machado RAR, Campos-Herrera R, Turlings TCJ 2022. Potent ant repellents emitted from nematode-infected insect cadavers. Journal of Chemical Ecology 48: 71-78. https://doi.org/10.1007/s10886-021-01320-8  

2021

Liu Q, Hu X, Su S, Peng Y, Ye G, Lou Y, Turlings TCJ, Li Y 2021. Cooperative herbivory between two important pests of rice. Nature Communication. https://doi.org/10.1038/s41467-021-27021-0  

Machado RAR, Hussain Bhat A, Abolafia J, Muller A, Bruno P, Fallet P, Arce CCM, Turlings TJC, Bernal JS, Kajuga J, Waweru B, Toepfer S 2021. Multi-locus phylogenetic analyses uncover species boundaries and revealed the occurrence of two new entomopathogenic nematode species, Heterorhabditis ruandica n. sp. and Heterorhabditis zacatecana n. sp. Journal of Nematology e2021-89 Vol. 53. https://doi.org/10.21307/jofnem-2021-089

Mann L, Laplanche D, Turlings TCJ, Desurmont GA 2021. Plant volatiles induced by insect and gastropod herbivory: a comparative study. Scientific Reports 11: 23698. https://doi.org/10.1038/s41598-021-02801-2

Xu T, Xu M, Lu Y, Zhang W, Sun J, Zeng R, Turlings TCJ, Chen L 2021. A trail pheromone mediates the mutualism between ants and aphids. Current Biology 21: 4738-4747.e4. https://doi.org/10.1016/j.cub.2021.08.032

Arce CM, Besomi G, Glauser G, Turlings TCJ 2021. Caterpillar-induced volatile emissions in cotton: The relative importance of damage and insect-derived factors. Frontiers in Plant Science 12: 709858. https://doi.org/10.3389/fpls.2021.709858

González-Mas N, Gutiérrez-Sánchez F, Sánchez-Ortiz A, Grandi L, Turlings TCJ, Muñoz-Redondo JM, Moreno-Rojas JM Quesada-Moraga E 2021. Endophytic colonization by the entomopathogenic fungus Beauveria Bassiana affects plant volatile emissions in the presence or absence of chewing and sap-sucking insects. Frontiers in Plant Science 12: 660460. https://doi.org/10.3389/fpls.2021.660460

Ling X., Gu S, Tian C, Guo H, Degen, Turlings TCJ, Ge F, Sun Y 2021. Differential levels of fatty acid-amino acid conjugates in the oral secretions of lepidopteran larvae account for the different profiles of volatiles produced by maize. Pest Management Science 77: 3970–3979. https://doi.org/10.1002/ps.6417

Lin T, Vrieling, K, Laplanche D, Klinkhamer PGL, Lou Y, Bekooy L, T.Degen T, Bustos-Segura C, Turlings TCJ, Desurmont G 2021. Evolutionary changes in an invasive plant support the defensive role of plant volatiles. Current Biology 15: 3450-3456.e5. https://doi.org/10.1016/j.cub.2021.05.055

Xia J, Guo Z, Yang Z, Han H, Wang S, Xu H, Yang X, Yang F, Wu Q, Xie W, Zhou X, Dermauw W, Turlings TCJ, Zhang Y 2021. Whitefly hijacks a plant detoxification gene that neutralizes plant toxins. Cell. https://www.sciencedirect.com/science/article/pii/S0092867421001641

Toepfer S, Fallet P, Kajuga J, Bazagwira D, Mukundwa IP, Szalai M, Turlings TCJ 2021. Streamlining leaf damage rating scales for the fall armyworm on maize. Journal of Pest Science. https://doi.org/10.1007/s10340-021-01359-2

Kim J, Hiltpold I, Jaffuel G, Sbaiti I, Hibbard BE, Turlings TCJ 2021. Calcium-alginate beads as a formulation for the application of entomopathogenic nematodes to control rootworms. Journal of Pest Science. https://doi.org/10.1007/s10340-021-01349-4

Moreira X, Granjel RR, de la Fuente M, Fernández-Conradi P, Pasch V, Soengas P, Turlings TCJ, Vázquez-González C, Abdala-Roberts L, Rasmann S 2021. Apparent inhibition of induced plant volatiles by a fungal pathogen prevents airborne communication between potato plants. Plant, Cell & Environment 44: 1192-1201.

2020

Fattore S, Xiao Z, Godschalx AL, Röder G, Turlings TCJ, Le Bayon R-C, Rasmann S 2020. Bioturbation by endogeic earthworms facilitates entomopathogenic nematode movement toward herbivore-damaged maize roots. Scientific Reports 10:21316

Steinbrenner AD, Muñoz-Amatriaín M, Chaparro AF, Aguilar-Venegas JM, Lo S, Okuda S, Glauser G, Dongiovanni J, Shi D, Hall M, Crubaugh D, Holton N, Zipfel C, Abagyan R, Turlings TCJ, Close TJ, Huffaker A, Schmelz EA 2020. A receptor-like protein mediates plant immune responses to herbivore-associated molecular patterns. Proc. Natl. Acad. Science USA (online) (https://www.pnas.org/content/early/2020/11/20/2018415117)

La Forgia D, Campos Herrera R, Jaffuel G, Turlings TCJ, Verheggen F 2020. Efficiency of an attract-and-kill system with entomopathogenic nematodes against wireworms (Coleoptera: Elateridae). IOBC-WPRS Bulletin Vol. 150: 91-95

Hu X, Lia Y, Liu Q, Jiao Y, Peng Y, Li Y, Turlings TCJ 2020. Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper. eLife 2020;9:e55421

Quijano-Medina T, Turlings TCJ, Sosenski P, Grandi L, Cervera JC, Moreira X, Abdala-Roberts L 2020. Effects of soil salinity on the expression of direct and indirect defences in wild cotton (Gossypium hirsutum). Journal of Ecology (online) https://doi.org/10.1111/1365-2745.13483

Desurmont GA, von Arx M, Turlings TCJ, Schiestl FP 2020. Floral odors can interfere with the foraging behavior of parasitoids searching for hosts. Frontiers Ecology and Evolution https://doi.org/10.3389/fevo.2020.00148

Fallet P, Machado RAR, Toepfer S, Ye W, Kajuga J, Waweru B, Bazagwira D, Turlings TCJ 2020. A Rwandan survey of entomopathogenic nematodes that can potentially be used to control the fall armyworm. IOBC-WPRS Bulletin 150: 87-90

Kapranas A, Sbaiti I, Degen T, Turlings TJC 2020. Biological control of cabbage fly Delia radicum with entomopathogenic nematodes: selecting the most effective nematode species and testing a novel application method. Biological Control 144: 104212

Bruno P, Machado RAR, Glauser G, Köhler A, Campos-Herrera R, Bernal J, Toepfer S, Erb M, Robert CAM, Arce CC, Turlings TCJ 2020. Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Scientific Reports (in press).

De Lange ES, Laplanche D, Guo H, Xu W, Vlimant M, Erb M, Ton J, Turlings TCJ 2020. Spodoptera frugiperda caterpillars suppress herbivore-induced volatile emissions in maize. Journal of Chemical Ecology. (online: doi: 10.1007/s10886-020-01153-x)

Jaffuel G, Sbaiti I, Turlings CJT 2020. Encapsulated entomopathogenic nematodes can protect maize plants from Diabrotica balteata larvae. Insects11(1): 27; https://doi.org/10.3390/insects11010027

Xu H, Zhou G, Dötterl S, Schäffler I, Degen T, Chen L, Turlings TCJ 2020. Distinct roles of cuticular aldehydes as pheromonal cues in two Cotesiaparasitoids. Journal of Chemical Ecology 46:128-137

2019

Xu H, Zhou G, Dötterl S, Schäffler I, von Arx M, Roeder G, Degen T, Chen L, Turlings TCJ 2019. The combined use of an attractive and repellent sex pheromone by a gregarious parasitoid. Journal of Chemical Ecology 45: 559-569

Abdala-Roberts L, Quijano-Medina T, Moreira X, Parra-Tabla V, Berny-Mier y Teran J, Grandi L, Glauser G, Turlings TCJ, Benrey B 2019. Bottom-up effects of plant defenses and climate on geographic variation in insect herbivory on wild cotton (Gossypium hirsutum). American Journal of Botany 106:1059-1067

Zhang P-J, Wei J-N, Zhao C, Zhang Y-F, Li C-Y, Liu S-S, Dicke M, Yu X-P, Turlings TCJ 2019. Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. Proc. Natl. Acad. Science USA 116: 7387-7396

Imperiali, N, Jaffuel G, Shelby K, Campos-Herrera R, Geisert R, Maurhofer M, Loper J, Keel C, Turlings TCJ, Hibbard BE 2019. Protecting maize from rootworm damage with the combined application of arbuscular mycorrhizal fungi, Pseudomonas bacteria and entomopathogenic nematodes. Scientific Reports 9, 3127

Abdala-Roberts L, Pérez Niño B, Moreira X, Parra-Tabla V, Grandi L, Glauser G, Benrey B, Turlings TCJ 2019. Effects of early-season insect herbivory on subsequent pathogen infection and ant abundance on wild cotton (Gossypium hirsutum). Journal of Ecology 107: 1518-1529

Jaffuel G, Půža V, Hug A-S, Meuli R G, Nermuť J, Turlings TCJ, Desurmont GA, Campos-Herrera R 2019. Molecular detection and quantification of slug parasitic nematodes from the soil and their hosts. Journal of invertebrate pathology 160: 18-25

Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings TCJ, Erb M, Herrero S 2019. Can herbivore-induced volatiles protect plants by increasing the herbivores' susceptibility to natural pathogens? Applied and Environmental Microbiology (online: DOI: 101128/AEM.01468-18)

Machado RAR, Bruno P, CC Marques Arce, Liechti N, Köhler A, Bernal J, Bruggmann R, Turlings TCJ 2019. Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminescens subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology (online: doi: 10.1099/ijsem.0.003154)

2018

Ye M, Veyrat N, Xu H, Turlings TCJ, Erb M 2018. An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars. Science Advances 4.

Xu H, Turlings TCJ 2018. Plant Volatiles as Mate-Finding Cues for Insects. Trends in Plant Science 23: 100-111.

Turlings TCJ, Erb M 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annual Review of Entomology 63: 433-452.

Sobhy IS, Bruce TJ, Turlings TC 2018. Priming of cowpea volatile emissions with defense inducers enhances the plant's attractiveness to parasitoids when attacked by caterpillars. Pest Management Science 74: 966-977.

Jaffuel G, Chappuis L, Guillarme D, Turlings TCJ, Glauser G 2018. Improved separation by at-column dilution in preparative hydrophilic interaction chromatography. Journal of Chromatography A 1532: 136-143.

Jaffuel G, Blanco-Pérez R, Hug A-S, Chiriboga X, Meuli RG, Mascher F, Turlings TCJ, Campos-Herrera R 2018. The evaluation of entomopathogenic nematode soil food web assemblages across Switzerland reveals major differences among agricultural, grassland and forest ecosystems. Agriculture, Ecosystems & Environment 262: 48-57.

Girod P, Rossignaud L, Haye T, Turlings TCJ, Kenis M 2018. Development of Asian parasitoids in larvae of Drosophila suzukii feeding on blueberry and artificial diet. Journal of Applied Entomology 142: 483-494.

Girod P, Lierhmann O, Urvois T, Turlings TCJ, Kenis M, Haye T 2018. Host specificity of Asian parasitoids for potential classical biological control of Drosophila suzukii. Journal of Pest Science.

Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ 2018. Fine-tuning the ‘plant domestication-reduced defense’ hypothesis: specialist vs generalist herbivores. New Phytologist 217: 355-366.

Desurmont GA, Guiguet A, Turlings TCJ 2018. Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning. Biological Invasions 20: 195-206.

de Lange ES, Farnier K, Degen T, Gaudillat B, Aguilar-Romero R, Bahena-Juárez F, Oyama K, Turlings TCJ 2018. Parasitic wasps can reduce mortality of teosinte plants infested with fall armyworm: support for a defensive function of herbivore-Induced plant volatiles. Frontiers in Ecology and Evolution 6.

Chiriboga M. X, Guo H, Campos-Herrera R, Röder G, Imperiali N, Keel C, Maurhofer M, Turlings TCJ 2018. Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding. Oecologia 187: 459-468.

Carrasco D, Desurmont GA, Laplanche D, Proffit M, Gols R, Becher PG, Larsson MC, Turlings TCJ, Anderson P 2018. With or without you: Effects of the concurrent range expansion of an herbivore and its natural enemy on native species interactions. Global Change Biology 24: 631-643.