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Manipulation of plant defenses by insect eggs

English title Manipulation of plant defenses by insect eggs
Applicant Reymond Philippe
Number 169278
Funding scheme Project funding
Research institution Dépt de Biologie Moléculaire Végétale Faculté de Biologie et de Médecine Université de Lausanne
Institution of higher education University of Lausanne - LA
Main discipline Molecular Biology
Start/End 01.01.2017 - 28.02.2021
Approved amount 549'166.00
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All Disciplines (2)

Discipline
Molecular Biology
Botany

Keywords (7)

insect; egg elicitors; innate immunity; pathway crosstalk; oviposition; defense gene expression; Arabidopsis thaliana

Lay Summary (French)

Lead
Le but de ce projet est de comprendre comment les oeufs d'insectes manipulent les défenses de la plante
Lay summary

Les plantes sont attaquées par une multitude d'insectes et ont mis en place des stratégies contre ces agressions. A l'inverse, les insectes ont évolué des mécanismes pour bloquer les défenses de la plante en détournant les voies de transmission de signaux à leur avantage. Les oeufs d'insectes représentent une menace car les larves qui éclosent vont se nourrir de feuilles. Nos recherches ont montré que la plante Arabidopsis thaliana détecte la présence de molécules d'oeufs de Pieris brassicae et qu'elle active une réponse immunitaire qui est modulée par le signal acide salicylique (SA) et se manifeste par l'expression de centaines de gènes de défense. Cette découverte est surprenante car il est connu que le SA est engagé pour résister aux attaques bactériennes et fongiques alors que le signal acide jasmonique (JA) est responsable de la défense contre les insectes. Cependant, nous avons montré que l'accumulation de SA sous les oeufs protège la plante contre la bactérie pathogène Pseudomonas syringae et permet un meilleur développement des larves. Ceci suggère que ce phénomène a évolué pour empêcher un effet néfaste d'une infection sur les jeunes larves. De plus, l'accumulation de SA bloque détruit des facteurs de transcription MYCs essentiels pour activer des gènes de défenses qui dépendent du JA, permettant également un meilleur développement des larves. Le but de ce projet est 1) d'identifier la structure des molécules de l'oeuf responsables des effets observés, 2) de comprendre l'importance biologique de la protection induite contre des pathogènes, 3) de caractériser les étapes moléculaires qui régulent la destruction des facteurs MYCs. Nous espérons découvrir de nouvelles stratégies de lutte contre les insectes nuisibles en se basant sur des processus biologiques.

Direct link to Lay Summary Last update: 26.09.2016

Responsible applicant and co-applicants

Employees

Publications

Publication
Arabidopsis natural variation in insect egg-induced cell death reveals a role for LECTIN RECEPTOR KINASE-I.1
Groux Raphaël, Stahl Elia, Gouhier-Darimont Caroline, Kerdaffrec Envel, Jimenez-Sandoval Pedro, Santiago Julia, Reymond Philippe (2021), Arabidopsis natural variation in insect egg-induced cell death reveals a role for LECTIN RECEPTOR KINASE-I.1, in Plant Physiology, 185, 440-455.
Phosphatidylcholines from Pieris brassicae eggs activate an immune response in Arabidopsis
Stahl Elia, Brillatz Théo, Ferreira Queiroz Emerson, Marcourt Laurence, Schmiesing André, Hilfiker Olivier, Riezman Isabelle, Riezman Howard, Wolfender Jean-Luc, Reymond Philippe (2020), Phosphatidylcholines from Pieris brassicae eggs activate an immune response in Arabidopsis, in eLife, 9, e60293.
Pieris brassicae eggs trigger inter‐plant systemic acquired resistance against a foliar pathogen in Arabidopsis
Orlovskis Zigmunds, Reymond Philippe (2020), Pieris brassicae eggs trigger inter‐plant systemic acquired resistance against a foliar pathogen in Arabidopsis, in New Phytologist, 228, 1652-1661.
Stress‐ and pathway‐specific impacts of impaired jasmonoyl‐isoleucine (JA‐Ile) catabolism on defense signaling and biotic stress resistance
Marquis Valentin, Smirnova Ekaterina, Poirier Laure, Zumsteg Julie, Schweizer Fabian, Reymond Philippe, Heitz Thierry (2020), Stress‐ and pathway‐specific impacts of impaired jasmonoyl‐isoleucine (JA‐Ile) catabolism on defense signaling and biotic stress resistance, in Plant, Cell & Environment, 43, 1578-1570.
Jasmonate-Related MYC Transcription Factors Are Functionally Conserved in Marchantia polymorpha
Peñuelas María, Monte Isabel, Schweizer Fabian, Vallat Armelle, Reymond Philippe, García-Casado Gloria, Franco-Zorrilla Jose M., Solano Roberto (2019), Jasmonate-Related MYC Transcription Factors Are Functionally Conserved in Marchantia polymorpha, in The Plant Cell, 31(10), 2491-2509.
The Arabidopsis Lectin Receptor Kinase LecRK-I.8 Is Involved in Insect Egg Perception
Gouhier-Darimont Caroline, Stahl Elia, Glauser Gaetan, Reymond Philippe (2019), The Arabidopsis Lectin Receptor Kinase LecRK-I.8 Is Involved in Insect Egg Perception, in Frontiers in Plant Science, 10(623), 1-10.
Ligand-receptor co-evolution shaped the jasmonate pathway in land plants
Monte Isabel, Ishida Sakiko, Zamarreño Angel M., Hamberg Mats, Franco-Zorrilla José M., García-Casado Gloria, Gouhier-Darimont Caroline, Reymond Philippe, Takahashi Kosaku, García-Mina José M., Nishihama Ryuichi, Kohchi Takayuki, Solano Roberto (2018), Ligand-receptor co-evolution shaped the jasmonate pathway in land plants, in Nature Chemical Biology, 14(5), 480-488.
The Cuticle Mutant eca2 Modifies Plant Defense Responses to Biotrophic and Necrotrophic Pathogens and Herbivory Insects
Blanc Catherine, Coluccia Fania, L’Haridon Floriane, Torres Martha, Ortiz-Berrocal Marlene, Stahl Elia, Reymond Philippe, Schreiber Lukas, Nawrath Christiane, Métraux Jean-Pierre, Serrano Mario (2018), The Cuticle Mutant eca2 Modifies Plant Defense Responses to Biotrophic and Necrotrophic Pathogens and Herbivory Insects, in Molecular Plant-Microbe Interactions, 31(3), 344-355.
Plant-arthropod interactions: who is the winner?
Stahl Elia, Hilfiker Olivier, Reymond Philippe (2018), Plant-arthropod interactions: who is the winner?, in The Plant Journal, 93(4), 703-728.
An OPR3-independent pathway uses 4,5-didehydrojasmonate for jasmonate synthesis
Chini Andrea, Monte Isabel, Zamarreño Angel M, Hamberg Mats, Lassueur Steve, Reymond Philippe, Weiss Sally, Stintzi Annick, Schaller Andreas, Porzel Andrea, García-Mina José M, Solano Roberto (2018), An OPR3-independent pathway uses 4,5-didehydrojasmonate for jasmonate synthesis, in Nature Chemical Biology, 14(2), 171-178.
Arabidopsis glucosinolates trigger a contrasting transcriptomic response in a generalist and a specialist herbivore
Schweizer Fabian, Heidel-Fischer Hanna, Vogel Heiko, Reymond Philippe (2017), Arabidopsis glucosinolates trigger a contrasting transcriptomic response in a generalist and a specialist herbivore, in Insect Biochemistry and Molecular Biology, 85, 21-31.

Collaboration

Group / person Country
Types of collaboration
Prof. Jean-Luc Wolfender, University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof Guido van den Ackeveken, Utrecht University Netherlands (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Roberto Solano, CSIC-CNB Madrid Spain (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Howard Riezman, University of Geneva Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
INRAE Effectome meeting XII Talk given at a conference Insect eggs manipulate plant defense 23.10.2019 Lauret, France Reymond Philippe;
IS-MPMI Congress Poster Plant Recognition of Insect Eggs triggers Systemic Acquired Resistance and SA-JA Crosstalk in Neighbouring Plants. 14.07.2019 Glasgow, Great Britain and Northern Ireland Orlovskis Zigmunds;
IS-MPMI XVIII Congress Talk given at a conference Molecular dialogue between insect eggs and Arabidopsis thaliana 14.07.2019 Glasgow, Great Britain and Northern Ireland Reymond Philippe;
LabEx Tulip Summerschool Talk given at a conference Molecular interactions betwenn plants and insect herbivores 07.07.2019 Lesponne en Pyrénées, France Reymond Philippe;
Rencontres de Virologie Végétale Talk given at a conference Molecular dialogue between insect eggs and Arabidopsis thaliana 27.01.2019 Aussois, France Reymond Philippe;
LabEx Tulip Summerschool Talk given at a conference Molecular dialogue between insect eggs and Arabidopsis thaliana 15.07.2018 Lesponne en Pyrénées, France Reymond Philippe;


Communication with the public

Communication Title Media Place Year
Other activities North Carolina Ag Tech Professional Forum International 2020
Media relations: radio, television 6h-9h le samedi RTS la première Western Switzerland 2019
Talks/events/exhibitions Plant defenses au Gymnase de Renens Western Switzerland 2019
Media relations: radio, television Couleurs locales RTS la première Western Switzerland 2018
Media relations: radio, television CQFD RTS la première Western Switzerland 2018

Associated projects

Number Title Start Funding scheme
118421 Oviposition-induced defense responses in Arabidopsis 01.10.2007 Project funding
132915 Suppression of plant defense responses by insect eggs 01.10.2010 Project funding
149286 Arabidopsis innate immunity against insect eggs 01.10.2013 Project funding
200372 Insect egg recognition and responses in Arabidopsis 01.06.2021 Project funding
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

Plants are challenged by numerous herbivorous insects and have developed sophisticated strategies to fend off these attackers. In turn, insects have evolved mechanisms to suppress plant defenses or to hijack signaling pathways for their own advantage. Eggs deposited on plants by insects represent a threat as they develop into feeding larvae. Earlier studies established that plants detect egg-associated elicitors and activate direct and indirect defenses. Recent years have seen progress in the molecular understanding of egg-induced responses in Arabidopsis thaliana. Genetic and biochemical analyses have revealed that egg perception triggers an innate immunity response that is regulated by the salicylic acid (SA) pathway. This finding was unexpected since the SA pathway is normally engaged to fight fungal and bacterial pathogens, whereas plants resist insect attack by activating jasmonic acid (JA)-dependent defenses. However, egg-induced SA accumulation was shown to protect plants against infection by the biotroph pathogen Pseudomonas syringae by activating a systemic acquired resistance (SAR). This SAR benefited the development of young hatching larvae and suggests that this phenomenon may have evolved as a strategy to prevent the detrimental effect of bacterial pathogens on feeding larvae. In addition, egg-induced SA accumulation suppressed JA-dependent gene expression by targeting key MYC transcription factors that are crucial for defense against feeding larvae. Again, this SA/JA cross talk enhanced larval performance. These intriguing findings constitute two independent examples of manipulation of a plant signaling pathway by the attacker. A major challenge is to identify egg-associated elicitors and plant receptors that lead to activation of the SA pathway. It is also necessary to better understand the biological relevance of egg-induced SAR and the precise regulation of SA/JA cross talk.The proposed research project has three objectives. The first objective is to identify a novel egg elicitor and how it is perceived by Arabidopsis. Preliminary work has identified a candidate molecule and a potential receptor that would represent the first known elicitor/receptor pair from a plant-insect interaction and would open the way for interesting structure/function analyses. The second objective is to characterize the importance of egg-induced SAR and its role against a range of biotic factors that interact with Arabidopsis. Results from this part may lead to interesting applied aspects. The third objective is to investigate how egg-induced SA/JA cross talk is modulated and the role of independent regulation steps. We also hope to identify new genes that participate in this process.This project aims at a better knowledge of plant-insect interactions. One emerging theme is that insect eggs have evolved distinct ways to highjack the SA pathway for the benefit of larvae. We hope to unveil interesting mechanisms that may apply to diverse interactions between plants and biotic factors.
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