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Sugar wars: Glucose-mediated activation, neutralization and re-activation of defensive metabolites in a soil tritrophic system

English title Sugar wars: Glucose-mediated activation, neutralization and re-activation of defensive metabolites in a soil tritrophic system
Applicant Turlings Théodoor
Number 160786
Funding scheme Sinergia
Research institution Institut de Biologie Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Botany
Start/End 01.10.2015 - 30.09.2019
Approved amount 2'145'147.00
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All Disciplines (6)

Discipline
Botany
Zoology
Molecular Biology
Organic Chemistry
Ecology
Biochemistry

Keywords (5)

plant-insect interactions; detoxification by insect herbivores; plant defence chemistry; crop protection; interspecific metabolic networks

Lay Summary (German)

Lead
Pflanzliche Giftstoffe können von spezialisierten Insekten entgiftet werden. Die Mechanismen dieser Entgiftung und deren Einfluss auf die natürlichen Frassfeinde der Insekten ist nur begrenzt bekannt. Wir erforschen, wie der Maiswurzelbohrer mit den Hauptabwehrstoffen des Mais umgeht und wie dies die Effizienz von Nützlingen beeinflusst. Mit dieser Arbeit leisten wir einen Beitrag zum fundamentalen Verständnis der Biologie eines wichtigen Schadinsekts und seiner natürlichen Feinde.
Lay summary

Eine verbreitete Verteidigungsstrategie der Pflanzen gegen Fressfeinde besteht darin, dass Abwehrstoffe als harmlose Glykoside, d.h. in an Zucker gebundener Form, gespeichert werden und bei einem Angriff durch Abspaltung des Zuckers in giftige oder abschreckende Substanzen verwandelt werden. Nun können aber spezialisierte Pflanzenfresser diese Giftstoffe durch Wiederanfügen eines Zuckers (Re-Glykosylierung) inaktivieren und für ihre eigene Abwehr gegen Feinde einlagern. Unser Projekt möchte beitragen zu einem umfassenden Verständnis dieses Phänomens, der Glukomodulation, sowohl in Bezug auf die zugrundeliegenden biochemischen Mechanismen als auch im Hinblick auf seine ökologischen Konsequenzen. Dieses Ziel soll mittels eines interdisziplinären Ansatzes erreicht werden, wobei analytische Chemie, Biochemie, molekulare Physiologie und Ökologie kombiniert werden. Ein tritrophisches System im Boden, das bereits in einem früheren Sinergiaprojekt erforscht wurde, eignet sich in idealer Weise für diese Fragestellung und umfasst die folgenden Organismen: Maispflanzen, den westlichen Maiswurzelbohrer (Diabrotica virgifera) und dessen natürliche Feinde wie etwa entomopathogene Nematoden (Fadenwürmer). Benzoxazinoide (BXD) sind die wichtigsten chemischen Faktoren der Insektenresistenz von Maiswurzeln. Sie werden als Glukoside gespeichert und aktiviert durch Glukose-abspaltende Enzyme der Pflanzen. Die spezialisierten Wurzelbohrerlarven sind gegenüber BXDs tolerant und benutzen sie sogar, um sich im Boden zu orientieren. Unser Ziel ist es, die Mechanismen dieser Toleranz zu verstehen und zu erforschen, ob und wie die natürlichen Feinde des Wurzelbohrers durch Benzoxazinoide beeinflusst werden. Unser Fokus wird dabei auf entomopathogenen Nematoden liegen. Ein besseres Verständnis dieses Schlüsselprozesses könnte helfen, die durch Diabrotica verursachten enormen Probleme in der Landwirtschaft zu lösen.

Direct link to Lay Summary Last update: 01.09.2015

Lay Summary (English)

Lead
Plant toxins can be detoxified by specialized insects. The mechanisms of this detoxification process and its influence on the natural enemies of the herbivorous insects are not yet understood. We investigate how the western corn rootworm deals with the main defence compounds of maize and how this affects the efficiency of beneficial organisms that kill the pest. This work will contribute to a fundamental understanding of the biology of an important pest insect and its natural enemies.
Lay summary

Many plants defend themselves with chemicals that they store in their tissues in a non-toxic form. When these tissues are damaged by, for instance, plant-eating insects the stored compounds are converted to a toxic form to ward off the attackers. In maize plants and other grasses the main chemical defense compounds are so-called benzoxazinoids (BXDs). They are stored as glucosides, which means that there is a sugar (glucose) attached to the molecule, rendering it non-toxic. Upon tissue disruption enzymes are liberated that cleave off the sugar and the BXDs become toxic. Our project builds on our discovery that specialized insects have evolved highly sophisticated mechanisms that make them immune to this maize defense. Certain caterpillars are able to reattach a sugar to BXDs in a position that makes the molecule much more stable and invulnerable to the enzymes. Highly specialized beetle larvae that feed on the roots of maize plants can even use BXDs as foraging cues and are fully resistant to these toxic metabolites. We aim to unravel the mechanisms that allow this important pest of maize to withstand BXDs and to explore if and how the insect’s enemies are affected by the toxins. The focus will be on entomopathogenic nematodes (EPN), tiny roundworms that develop and reproduce inside insect bodies and kill them within days. The work will not only generate fundamental new knowledge on chemical defenses in plants and insects, it also has great potential for pest control as it may lead to the discovery of highly effective EPN strains for the biological control of one of the world’s most destructive maize pests.

Direct link to Lay Summary Last update: 01.09.2015

Responsible applicant and co-applicants

Employees

Publications

Publication
Photorhabdus khanii subsp. guanajuatensis subsp. nov. isolated from Heterorhabditis atacamensis and Photorhabdus luminescens subsp. mexicana subsp. nov. isolated from H. mexicana entomopathogenic nema
Machado Ricardo A.R., Bruno Pamela, Arce Carla, Liechti N., Köhler Angela, Bernal Julio, Bruggmann R., Erb Matthias, Turlings Ted C.J. (2019), Photorhabdus khanii subsp. guanajuatensis subsp. nov. isolated from Heterorhabditis atacamensis and Photorhabdus luminescens subsp. mexicana subsp. nov. isolated from H. mexicana entomopathogenic nema, in International Journal of Systematic and Evolutionary Microbiology, 69, 652-661.
Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals
Li B., Förster C., Robert C. A. M., Züst T., Hu L., Machado R. A. R., Berset J.-D., Handrick V., Knauer T., Hensel G., Chen W., Kumlehn J., Yang P., Keller B., Gershenzon J., Jander G., Köllner T. G., Erb M. (2018), Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals, in Science Advances, 4(12), eaat6797-eaat6797.
Plant iron acquisition strategy exploited by an insect herbivore
Hu L., Mateo P., Ye M., Zhang X., Berset J. D., Handrick V., Radisch D., Grabe V., Köllner T. G., Gershenzon J., Robert C. A. M., Erb M. (2018), Plant iron acquisition strategy exploited by an insect herbivore, in Science, 361(6403), 694-697.
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
Hu Lingfei, Robert Christelle A. M., Cadot Selma, Zhang Xi, Ye Meng, Li Beibei, Manzo Daniele, Chervet Noemie, Steinger Thomas, van der Heijden Marcel G. A., Schlaeppi Klaus, Erb Matthias (2018), Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota, in NATURE COMMUNICATIONS, 9, 2738.
Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels
Robert Christelle AM, Zhang Xi, Machado Ricardo AR, Schirmer Stefanie, Lori Martina, Mateo Pierre, Erb Matthias, Gershenzon Jonathan (2017), Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels, in eLife, 6, e29307.
Root signals that mediate mutualistic interactions in the rhizosphere
Rasmann Sergio, Turlings Ted CJ (2016), Root signals that mediate mutualistic interactions in the rhizosphere, in Current Opinion in Plant Biology, 32, 62-68.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Annual MPICE Symposium Poster The role of beta-glucosidases and beta-glucosidase-aggregating factors in the activation of benzoxazinoids in maize roots (Poster Diana Radisch) 23.09.2019 Jena, Germany Gershenzon Jonathan; Radisch Diana;
10th Conference of Asia-Pacific Association of Chemical Ecologists (APACE) Individual talk Diabrotica virgifera virgifera females can sequester multiple plant toxins to protect their eggs against predators (Talk Carla Arce 10.09.2019 Hangzhou, China Turlings Théodoor; Robert Christelle; Erb Matthias; Marques Arce Carla Cristina;
Gordon Research Conference on Plant Metabolic Engineering Poster Flavonoid O-methyltransferases as targets for engineering pathogen resistance in maize (Poster Christiane Förster) 16.06.2019 Lucca, Italy Gershenzon Jonathan; Förster Christiane;
18th IMPRS Symposium Poster The role of beta-glucosidases and beta-glucosidase-aggregating factors in the activation of benzoxazinoids in maize roots (Poster Diana Radisch) 13.03.2019 Dornburg, Germany Gershenzon Jonathan; Radisch Diana;
18th IMPRS Symposium Talk given at a conference Fungal infestation induces O-methylation of flavonoids in maize (talk Christiane Förster) 13.03.2019 Dornburg, Germany Gershenzon Jonathan; Förster Christiane;
5th Annual meeting of the Latin American Society of Chemical Ecology Talk given at a conference Impact of benzoxazinoid sequestration by the Western Corn Rootworm on the biocontrol potential of entomopathogenic nematode isolates from Mexico (Pamela Bruno) 23.10.2018 Valparaíso, Chile Köhler Angela; Marques Arce Carla Cristina; Turlings Théodoor; Robert Christelle; Bruno Pamela; Erb Matthias;
Workshop of the section Natural Products of the German Society for Plant Sciences Poster Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals (Tobias Köllner) 01.10.2018 Warberg, Germany Förster Christiane; Gershenzon Jonathan;
Workshop of the section Natural Products of the German Society for Plant Sciences Talk given at a conference Fungal infestation induces O-methylation of flavonoids in maize (Christiane Förster) 01.10.2018 Warberg, Germany Förster Christiane; Gershenzon Jonathan;
SPP preparation meeting Talk given at a conference Engineering and optimization of the benzoxazinoid pathway in heterologous plant systems (Tobias Köllner, invited speaker) 24.09.2018 Halle (Saale), Germany Gershenzon Jonathan;
John Innes Centre Individual talk Biosynthesis of benzoxazinoids in maize: Beyond the core pathway (Tobias Köllner, invited speaker) 19.09.2018 Norwich, Great Britain and Northern Ireland Gershenzon Jonathan;
34th Annual meeting of the International Society of Chemical Ecology (ISCE) Talk given at a conference Diabrotica virgifera females use maize plant benzoxazinoids to protect their eggs against predators (Carla Arce) 12.08.2018 Budapest, Hungary Robert Christelle; Marques Arce Carla Cristina; Erb Matthias; Turlings Théodoor;
34th Annual meeting of the International Society of Chemical Ecology Poster Impact of benzoxazinoid sequestration by the Western Corn Rootworm on the biocontrol potential of entomopathogenic nematode isolates from Mexico (Pamela Bruno) 12.08.2018 Budapest, Hungary Marques Arce Carla Cristina; Turlings Théodoor; Robert Christelle; Köhler Angela; Bruno Pamela; Erb Matthias;
IMPRS workshop Poster Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals (Christiane Förster) 13.03.2018 Dornburg, Germany Gershenzon Jonathan; Förster Christiane;
Biology 18 Poster Survey of natural enemies of the Western Corn Rootworm in Central Mexico (Pamela Bruno) 15.02.2018 Neuchâtel, Switzerland Turlings Théodoor; Bruno Pamela; Erb Matthias; Köhler Angela; Marques Arce Carla Cristina;
Biology 18 Poster How do females of Diabrotica beetles defend their eggs? (Carla Arce) 15.02.2018 Neuchâtel, Switzerland Marques Arce Carla Cristina; Erb Matthias; Robert Christelle; Turlings Théodoor;
University of Hohenheim Individual talk The biochemistry of direct and indirect defense reactions against insect herbivores in maize and poplar (Tobias Köllner, invited speaker) 29.11.2017 Hohenheim, Germany Gershenzon Jonathan;
Helmholtz Zentrum München Individual talk Benzoxazinoids in maize and wheat: Defense compounds or chemical signals? (Tobias Köllner, invited speaker) 07.11.2017 München, Germany Gershenzon Jonathan;
CIRAD Individual talk Trophic interactions in the rhizosphere: applying chemical ecology to develop novel strategies for root pest control (invited lecture Ted Turlings). 15.09.2017 La Réunion, France Turlings Théodoor;
8th World Congress of Allelopathy Talk given at a conference Trophic interactions in the rhizosphere: applying chemical ecology to develop novel strategies for root pest control (plenary talk Ted Turlings) 24.07.2017 Marseille, France Turlings Théodoor;
16th International Symposium on Insect-Plant Relationships (SIP 2017) Poster Transfer of stabilized plant toxins to higher trophic level protects the western corn rootworm from its natural enemies (Christelle Erb-Robert)) 02.07.2017 Tours, France Gershenzon Jonathan; Robert Christelle; Erb Matthias;
2nd European Molecular Maize Symposium Talk given at a conference Biosynthesis of benzoxazinoids in maize: Beyond the core pathway (Tobias Köllner) 03.05.2017 Ghent, Belgium Gershenzon Jonathan;
2nd European Molecular Maize Symposium Poster The role of beta-glucosidases and beta-glucosidase-aggregating factors in the activation of benzoxazinoids in maize roots (Diana Radisch) 03.05.2017 Ghent, Belgium Radisch Diana; Gershenzon Jonathan;
2nd European Molecular Maize Symposium Poster The evolution of DIMBOA-Glc O-methyltransferases in the grasses (Christiane Förster) 03.05.2017 Ghent, Belgium Gershenzon Jonathan; Förster Christiane;
26th Conference of the International Working Group on Ostrinia and other maize pests (IWGO) Poster Survey of natural enemies of the Western Corn Rootworm in Central Mexico (Pamela Bruno) 10.04.2017 Beijing, China Marques Arce Carla Cristina; Köhler Angela; Turlings Théodoor; Bruno Pamela;
Entomology Congress Talk given at a conference Trophic interactions in the rhizosphere: applying chemical ecology to develop novel strategies for root pest control (keynote Ted Turlings)) 13.03.2017 Freising, Germany Turlings Théodoor;
13th Gordon Research Conference on Plant-Herbivore Interactions Talk given at a conference The western corn rootworm hijacks plant defenses (Christelle Robert) 12.02.2017 Ventura, California, United States of America Gershenzon Jonathan; Robert Christelle; Erb Matthias;
XXV International Congress of Entomology (ICE2016) Talk given at a conference An herbivore-induced plant volatile functions as a direct defense and within-plant priming signal (invited presentation Matthias Erb 25.09.2016 Orlando, United States of America Erb Matthias;
XXV International Congress of Entomology (ICE2016) Talk given at a conference Enhancing biological control of a root pest: Responses of entomopathogenic nematodes to chemical defenses of the western corn rootworm (Angela Köhler) 25.09.2016 Orlando, United States of America Robert Christelle; Köhler Angela; Turlings Théodoor; Erb Matthias;
9th Scandinavian Plant Physiology Society (SPPS) PhD Student Conference 2016 Talk given at a conference The Essential Roles of Plant Secondary Metabolites in Plant Environment Interactions (Key Note Lecture Matthias Erb) 21.06.2016 Oslo, Norway Erb Matthias;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions Entdeckt! Wir machen Abwehrstoffe im Mais sichtbar (Diane Radisch, 9. Forsche-Schüler-Tag, Jena) International 2018

Awards

Title Year
Best oral presentation at the Annual PhD meeting in Neuchâtel, organized by the Doctoral Program in Organismal Biology 2019
Egalité des chances Grant – UNINE (to cover a part of the costs to participate at the 5th Annual meeting of the Latin American Society of Chemical Ecology (ALAEQ), 23.-26.10.2018, Valparaíso, Chile. 2018
Egalité des chances Grant – UNINE (to cover the costs to participate at the ISCE 2018 conference in Hungary) 2018
Second place in the oral presentation student sessions for the talk "Impact of benzoxazinoid sequestration by the Western Corn Rootworm on the biocontrol potential of entomopathogenic nematode isolates from Mexico" given at the 5th Annual meeting of the Latin American Society of Chemical Ecology (ALAEQ), 23.-26.10.2018, Valparaíso, Chile. 2018

Associated projects

Number Title Start Funding scheme
166632 Exploring the Chemical Ecology of Gastropod-Insect-Plant Interactions 01.06.2016 Project funding (Div. I-III)
176191 Role of Plastoglobule Proteins in Photosynthesis and Plastoquinone Pool Regulation 01.03.2018 Project funding (Div. I-III)
155781 RNAi-controlled multitrophic processing of plant secondary metabolites 01.02.2015 Temporary Backup Schemes
136184 Benzoxazinoid derivatives at the plant-insect interface: An integrated approach to understand a metabolic network 01.10.2011 Sinergia
183365 Ultra High Performance Liquid Chromatography-High Resolution Tandem Mass Spectrometry (UHPLC-HRMS/MS) for metabolomics and identification of bioactive molecules 01.10.2019 R'EQUIP

Abstract

Activation of secondary metabolites by de-glycosylation is a widespread anti-herbivore defense strategy which allows plants to store harmless glycosides and hydrolyze them to toxic or deterrent products upon attack. However, various specialized herbivores can re-glycosylate the activated toxins and store them for self-defense. Although glyco-modulation has been described in a number of systems, a detailed understanding of the biochemical mechanisms and ecological consequences is lacking. The interactions among maize plants, the western corn rootworm (WCR) and its natural enemies, such as entomopathogenic nematodes (EPNs) and parasitoids are ideally suited to study the ecological as well as agricultural significance of defensive glyco-modulation (Figure 1). WCR is a key pest of maize, and entomopathogenic nematodes are highly promising biocontrol agents. The main insect resistance factors in maize roots are 1,4-benzoxazin-3-one derivatives (BXDs), which are stored as glucosides and activated by plant ß-glucosidases. During a previous Sinergia project, we have found that the specialized WCR larvae are fully tolerant to BXDs and accumulate stabilized BXD glycosides upon BXD ingestion. Larval tissue disruption results in the rapid re-activation by putative insect ß-glucosidases, which is associated with increased resistance against natural enemies. BXD glyco-modulation is therefore a key process that may explain the success of WCR as a maize pest. As a next step, this project will identify and characterize BXD glyco-modulation enzymes in maize and WCR, manipulate them using reverse genetics and investigate their role in tritrophic interactions below ground. To achieve this goal, we will combine expertise in analytical chemistry, biochemistry, molecular physiology and ecology to: 1) develop a next-generation analytical toolbox to identify and trace BXDs across cell organelles, tissues and trophic levels using cell fractionation, 2H labeled precursors and sensitive absolute quantification methods; 2) identify and analyze maize BXD ß-glucosidases and ß-glucosidase aggregating factors as well as WCR glycosyl transferases and ß-glycosidases; 3) generate maize mutants and transiently silenced WCR larvae that are defective in BXD glyco-modulation 4) use the generated transformants to assess how BXD glyco-modulation affects WCR resistance to natural enemies. The above activities will result in the following output: 1) A comprehensive integrative set of unique research tools, including novel analytical methods, chemical and biochemical reagents, maize mutants and transformed strains. 2) Knowledge on the mechanistic basis of glyco-modulation as a general phenomenon in plant herbivore-interactions. 3) A detailed understanding of the importance of secondary metabolite hijacking for soil tritrophic interactions and biological control. By investigating glyco-modulation in a molecular, multitrophic context using an interdisciplinary approach, we expect push the boundaries of an important frontier in plant-insect interactions.
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