Insect chemical ecology: chemically mediated interactions and novel applications in agriculture

Forum PaperInsect chemical ecology (ICE) evolved as a discipline concerned with plant–insect interactions, and also with a strong focus on intraspecific pheromone-mediated communication. Progress in this field has rendered a more complete picture of how insects exploit chemical information in their surroundings in order to survive and navigate their world successfully. Simultaneously, this progress has prompted new research questions about the evolution of insect chemosensation and related ecological adaptations, molecular mechanisms that mediate commonly observed behaviors, and the consequences of chemically mediated interactions in different ecosystems. Themed meetings, workshops, and summer schools are ideal platforms for discussing scientific advancements as well as identifying gaps and challenges within the discipline. From the 11th to the 22nd of June 2018, the 11th annual PhD course in ICE was held at the Swedish University of Agricultural Sciences (SLU) Alnarp, Sweden. The course was made up of 35 student participants from 22 nationalities (Fig. 1a) as well as 32 lecturers. Lectures and laboratory demonstrations were supported by literature seminars, and four broad research areas were covered: (1) multitrophic interactions and plant defenses, (2) chemical communication focusing on odor sensing, processing, and behavior, (3) disease vectors, and (4) applied aspects of basic ICE research in agriculture. This particular article contains a summary and brief synthesis of these main emergent themes and discussions from the ICE 2018 course. In addition, we also provide suggestions on teaching the next generation of ICE scientists, especially during unprecedented global situationsinfo:eu-repo/semantics/publishedVersio

The impact of Spodoptera exigua herbivory on Meloidogyne incognita-induced root responses depends on the nematodes’ life cycle stages

13 páginas, 4 figurasInduced responses to above-ground and below-ground herbivores may interact via systemic signalling in plants. We investigated whether the impact of above-ground herbivory on root-knot nematode-induced responses depends on the nematode’s life cycle stages. Tomato plants were infected with the nematode (Meloidogyne incognita) for 5, 15 or 30 days before receiving Spodoptera exigua caterpillars above-ground. We collected root materials after 24 h of caterpillar feeding. We investigated phytohormones and α-tomatine levels, and the expression of defence and glycoalkaloid metabolism (GAME) marker genes in tomato roots. Nematode infection alone increased the endogenous root levels of jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), α-tomatine and the expression of the GLYCOALKALOID METABOLISM 1 (GAME1) gene mostly at 30 days post-nematode inoculation. Caterpillar feeding alone upregulated Lipoxygenase D and downregulated Basic-β-1-glucanase and GAME1 expression in roots. On nematode-infected plants, caterpillar feeding decreased JA levels, but it increased the expression of Leucine aminopeptidase A. The induction patterns of ABA and SA suggest that caterpillars cause cross-talk between the JA-signalling pathway and the SA and ABA pathways. Our results show that caterpillar feeding attenuated the induction of the JA pathway triggered by nematodes, mostly in the nematodes’ reproduction stage. These results generate a better understanding of the molecular and chemical mechanisms underlying frequent nematode–plant–caterpillar interactions in natural and agricultural ecosystems.Peer reviewe

Root infection by the nematode Meloidogyne incognita modulates leaf antiherbivore defenses and plant resistance to Spodoptera exigua depending on the nematode's infection cycle

18 páginas, 7 figuras, 2 tablasStudies on plant-mediated interactions between root parasitic nematodes and aboveground herbivores are rapidly increasing. However, the outcomes for the interacting organisms vary, and the mechanisms involved remain ambiguous. We hypothesized that the impact of root infection by the root-knot nematode Meloidogyne incognita on the performance of the aboveground caterpillar Spodoptera exigua is modulated by the nematode's infection cycle. We challenged root-knot nematode infected tomato plants with caterpillars when the nematode's infection cycle was either at the invasion, galling, or reproduction stage. We found that M. incognita root infection enhanced S. exigua performance during the galling stage, while it did not affect the caterpilar's performance at the invasion and reproduction stages. Molecular and chemical analyses performed at the different stages of the nematode infection cycle revealed that M. incognita root infection systemically affected the jasmonic acid-, salicylic acid- and abscisic acid-related responses, as well as changes in the leaf metabolome during S. exigua feeding. The M. incognita induced leaf responses significantly varied over the nematode's root infection cycle. These findings suggest that specific leaf responses triggered systemically by the nematode at its different life-cycle stages underlie the differential impact of M. incognita on plant resistance against the caterpillar S. exigua.All authors gratefully acknowledge the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (DFG-FZT 118, 202548816). CMM acknowledges the Deutscher Akademischer Austauschdienst (DAAD) for a doctoral research grant (research grant No: 91607343). AMM acknowledges funding from the program for attracting talent to Salamanca from the Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca; the program to support junior researchers to obtain thirdparty funding from Friedrich-Schiller-Universitat Jena (DRM/2015-02); Junta de Castilla y León and European Union (ERDF “Europe drives our growth”; CLU-2019-05 - IRNASA/ CSIC Unit of Excellence); and the research network RED2018-102407-T from the Spanish Ministry of Science and Innovation and Feder fundsPeer reviewe

Leaf herbivory counteracts nematode-triggered repression of jasmonate-related defenses in tomato roots

17 páginas, 8 figurasShoot herbivores may influence the communities of herbivores associated with the roots via inducible defenses. However, the molecular mechanisms and hormonal signaling underpinning the systemic impact of leaf herbivory on root-induced responses against nematodes remain poorly understood. By using tomato (Solanum lycopersicum) as a model plant, we explored the impact of leaf herbivory by Manduca sexta on the performance of the root knot nematode Meloidogyne incognita. By performing glasshouse bioassays, we found that leaf herbivory reduced M. incognita performance in the roots. By analyzing the root expression profile of a set of oxylipin-related marker genes and jasmonate root content, we show that leaf herbivory systemically activates the 13-Lipoxigenase (LOX) and 9-LOX branches of the oxylipin pathway in roots and counteracts the M. incognita-triggered repression of the 13-LOX branch. By using untargeted metabolomics, we also found that leaf herbivory counteracts the M. incognita-mediated repression of putative root chemical defenses. To explore the signaling involved in this shoot-to-root interaction, we performed glasshouse bioassays with grafted plants compromised in jasmonate synthesis or perception, specifically in their shoots. We demonstrated the importance of an intact shoot jasmonate perception, whereas having an intact jasmonate biosynthesis pathway was not essential for this shoot-to-root interaction. Our results highlight the impact of leaf herbivory on the ability of M. incognita to manipulate root defenses and point to an important role for the jasmonate signaling pathway in shoot-to-root signaling.This research was supported by the German Research Foundation (DFG–FZT 118, 202548816), by the program for attracting talent to Salamanca from Fundacio´n Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca (to A.M.M.), by the program to support junior researchers to obtain third-party funding from FriedrichSchiller-Universita¨t Jena (DRM/2015-02, to A.M.M.) y the Deutscher Akademischer Austauschdienst (DAAD 91607343, to C.M.M); by Junta de Castilla y León and European Union (ERDF “Europe drives our growth”; CLU-2019-05 – IRNASA/CSIC Unit of Excellence); and the research network RED2018-102407-T from the Spanish Ministry of Science and Innovation and Feder funds.Peer reviewe

Induced Local and Systemic Defense Responses in Tomato Underlying Interactions Between the Root-Knot Nematode Meloidogyne incognita and the Potato Aphid Macrosiphum euphorbiae.

16 páginas, 1 tablas, 6 figurasPlants mediate interactions between different herbivores that attack simultaneously or sequentially aboveground (AG) and belowground (BG) organs. The local and systemic activation of hormonal signaling pathways and the concomitant accumulation of defense metabolites underlie such AG-BG interactions. The main plant-mediated mechanisms regulating these reciprocal interactions via local and systemic induced responses remain poorly understood. We investigated the impact of root infection by the root-knot nematode (RKN) Meloidogyne incognita at different stages of its infection cycle, on tomato leaf defense responses triggered by the potato aphid Macrosiphum euphorbiae. In addition, we analyzed the reverse impact of aphid leaf feeding on the root responses triggered by the RKN. We focused specifically on the signaling pathways regulated by the phytohormones jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), and indole-3-acetic acid (IAA) as well as steroidal glycoalkaloids as induced defense compounds. We found that aphid feeding did not induce AG hormonal signaling, but it repressed steroidal glycoalkaloids related responses in leaves, specifically when feeding on plants in the vegetative stage. Root infection by the RKN impeded the aphid-triggered repression of the steroidal glycoalkaloids-related response AG. In roots, the RKN triggered the SA pathway during the entire infection cycle and the ABA pathway specifically during its reproduction stage. RKN infection also elicited the steroidal glycoalkaloids related gene expression, specifically when it was in the galling stage. Aphid feeding did not systemically alter the RKN-induced defense responses in roots. Our results point to an asymmetrical interaction between M. incognita and Ma. euphorbiae when co-occurring in tomato plants. Moreover, the RKN seems to determine the root defense response regardless of a later occurring attack by the potato aphid AG.All authors gratefully acknowledge the support of German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (DFG – FZT 118, 202548816). CMM acknowledges the Deutscher Akademischer Austauschdienst (DAAD) for a doctoral research grant (research grant No: 91607343). EMA acknowledges the DAAD Short-Term Scholarship Program (GERSS) scholarship awarded to her to conduct part of her Master of Science Research at iDiv. AMM further acknowledges funding from the program for attracting talent to Salamanca from Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca.Peer reviewe