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Conclusion & Perspectives Identification of elicitors inducing resistance in wheat against Zymoseptoria tritici and characterization of the subsequent triggered defense-signaling pathways Géraldine LE MIRE - 2 - COMMUNAUTÉ FRANÇAISE DE BELGIQUE UNIVERSITÉ DE LIÈGE – GEMBLOUX AGRO-BIO TECH Identification of elicitors inducing resistance in wheat against Zymoseptoria tritici and characterization of the subsequent triggered defense- signaling pathways Géraldine LE MIRE Dissertation originale présentée en vue de l’obtention du grade de docteur en sciences agronomiques et ingénierie biologique Promoteur : Mohammed Haissam JIJAKLI Année civile : 2018 - 3 - Copyright. Aux termes de la loi belge du 30 juin 1994 sur le droit d’auteur et les droits voisins, seul l’auteur a le droit de reproduire partiellement ou complètement cet ouvrage de quelque façon et forme que ce soit ou d’en autoriser la reproduction partielle ou complète de quelque manière et sous quelque forme que ce soit. Toute photocopie ou reproduction sous autre forme est donc faite en violation de ladite loi et des modifications ultérieures. - 4 - ABSTRACT The implementation of biocontrol products in integrated pest management strategies is a major challenge today in the transition to sustainable and environment-friendly agro-ecosystems. In particular, the use of natural elicitors, also called plant resistance inducers, represents an interesting alternative to conventional fungicides. Elicitors are natural immune-stimulating compounds which offer the advantage to indirectly target a broad spectrum of pathogens by enhancing the defensive state of the plant. Yet today, wheat is one of the most cultivated crops in the European Union and still requires fungicide protection every year for the control of a harmful disease: Septoria tritici Blotch (STB), caused by the fungal pathogen Zymoseptoria tritici. At a time when few elicitor products are available on the market for the sustainable management of crop diseases, the objective of this thesis project was to screen and identify innovative elicitors able to preventively protect wheat against the STB disease. Greenhouse trials successfully demonstrated the ability of λ-carrageenan, cytosine-phosphate-guanine oligodesoxynucleotide motifs (CpG-ODN), Spirulina platensis, glycine betaine and ergosterol to protect wheat by up to 70 % against the pathogen Z. tritici. These results are promising as previous research has indeed demonstrated the elicitor properties of these five compounds on other plant species and/or animals. Besides, no direct anti-fungal activity was recorded during in vitro experiments towards the disease. The risk of resistance development of the pathogen to these potential elicitors can thus be considered as low. Furthermore, the defense mechanisms of wheat were successfully demonstrated to be significantly induced following treatment with each of these formulated compounds. The relative expression of 23 plant defense genes was analyzed by qRT-PCR at 1, 2 and 3 days after plant treatment. Defense mechanisms involving the two hormones salicylic acid (SA) and jasmonic acid (JA) were triggered in treated wheat. These hormones play a key role in the transduction of defense signals throughout the plant. In addition, the protection efficacy of the two preferential candidates (λ-carrageenan and Spirulina) was investigated in the field during two successive years. Numerous parameters, among which environmental conditions, plant developmental stage, plant genotype and disease pressure, can indeed cause a variability of elicitor protection efficacy under practical conditions. Unfortunately, important contrasts in disease pressures and extreme weather conditions did not allow confirming the elicitor potential of the corresponding treatments on field. Finally, the potential effect of the formulation on the eliciting activity was characterized in order to rule out the possibility of interference by the selected adjuvants. Additional greenhouse experiments showed that a water solution containing only the adjuvants was as efficient to protect wheat against STB as plants treated with formulated or non-formulated λ-carrageenan. These last results highlighted the necessity of developing an appropriate formulation at an early stage before elicitor screening. Overall, the findings of this research study could open the way to the development of innovating biocontrol products based on λ-carrageenan for the sustainable protection of wheat against Zymoseptoria tritici. - 5 - - 6 - RÉSUMÉ L’intégration de produits de biocontrôle dans les stratégies de lutte intégrée contre les ennemis des cultures représente aujourd’hui un enjeu majeur pour développer des agro-écosystèmes durables et respectueux de l’environnement. En particulier, l’utilisation d’éliciteurs naturels, aussi appelés stimulateurs de défense des plantes, représente une alternative intéressante aux fongicides conventionnels. Les éliciteurs sont des molécules capables d’assurer un contrôle indirect des ennemis des cultures en induisant la résistance des plantes à un large spectre de pathogènes. Pourtant, le blé représente actuellement une des céréales les plus cultivées dans l’Union Européenne et requiert chaque année l’utilisation de fongicides chimiques pour contrôler une maladie fortement nuisible au rendement: la septoriose, causée par le champignon pathogène Zymoseptoria tritici. A l’heure actuelle, un faible nombre de produits éliciteurs sont disponibles sur le marché pour contribuer à une protection durable des plantes céréalières. Dans ce contexte, l’objectif de ce travail de thèse était de cribler et d’identifier des éliciteurs des défenses naturelles du blé innovants et permettant de protéger cette céréale majeure contre la maladie de la septoriose à titre préventif. Des essais en serre ont permis de montrer avec succès que le λ- carrageenan, les motifs cytosine-phosphate-guanine oligodesoxynucleotide (CpG- ODN), Spirulina platensis, la glycine betaine et l’ergosterol avaient chacun la capacité de protéger la plante de blé jusqu’à 70 % contre Z. tritici. Ces résultats sont prometteurs étant donné que des études antérieures ont démontré les propriétés élicitrices de ces composés sur d’autres espèces de plantes et/ou sur des animaux. De plus, aucune activité fongicide directe vis-à-vis de Z. tritici n’a été observée lors de tests en laboratoire. Le risque d’apparition de résistance du champignon pathogène à l’encontre de ces éliciteurs potentiels peut donc être considérée comme acceptable. En outre, la stimulation des défenses du blé suite à l’application de chacun des composés formulés a été démontrée avec succès. L’expression relative de 23 gènes de défense du blé a en effet été analysée par qRT-PCR à 1, 2 et 3 jours après traitement. Des mécanismes de défense impliquant les deux hormones acide salicylique (SA) et acide jasmonique (JA) ont été induits dans les plantes de blé traitées. Ces deux protéines jouent un rôle majeur dans la tranduction des signaux de défense au sein des plantes. Par ailleurs, l’éfficacité de protection des deux candidats préférentiels (λ-carrageenan and spiruline) a été étudiée au champ sur 2 ans. De nombreux facteurs tels que les conditions environmentales, le stade de développement de la plante et son génotype, ainsi que la pression parasitaire peuvent en effet entrainer une variabilité de l’efficacité de protection des éliciteurs appliqués au champ. Toutefois, des conditions climatiques extrêmes et des pressions parasitaires très contrastées n’ont pas permis de confirmer le maintien de l’éfficacité de protection des deux composés en conditions pratiques. Enfin, l’effet de la formulation a été évalué afin de confirmer l’absence d’interférence des adjuvants utilisés. Des essais supplémentaires en serre ont ainsi démontré que les adjuvants appliqués seuls protégeaient le blé aussi efficacement que des traitements à base de λ-carrageenan formulé ou non. Ces derniers résultats soulignent l’importance de mettre au point une formulation appropriée au plus tôt avant le criblage d’éliciteurs. Dans l’ensemble, les résultats de ce projet de recherche pourraient ouvrir la voie au développement de produits de biocontrôle innovants à base de λ-carrageenan pour une protection durable du blé contre Zymoseptoria tritici. - 7 - - 8 - ACKNOWLEDGEMENTS First of all, I would like to thank Pr. M. Haissam Jijakli for the great opportunity to make my PhD in his research unit and also for his kind support and supervision throughout those four years. I am also very thankful for Gembloux Agro Bio Tech and especially AgricultureIsLife for the economic support in my research and for giving me the chance to take part in useful and interesting courses, symposiums and congresses. I would also like to thank all the members of the AgricultureIsLife platform, especially Sarah Garré, Aman Paul, Malik Hamaidia, and Marie Chélin for all the nice moments we shared together in a lovely team spirit. In addition, I wish to say a big thank you to all the members of the unit of Integrated and Urban Phytopathology. Thank you Gladys Rufflard for all those nice talks in your office, Thanks to you Caroline Leclercq for kindly understanding the tough moments a PhD student sometimes experiences. Thank you Frederic Dresen for your helpful advice in the matter of fungal cultivation and plant growth! Your expertise was always highly appreciated. Thanks to Angelo, Thibault and Jimmy with whom I loved to share a big laugh in between two experiments at the lab. And thanks to all of you for helping me water those
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