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Microbial diversity and pathogen-microbiome interactions in crop residues : the case of Zymoseptoria tritici and Leptosphaeria maculans in a wheat-oilseed rape system

Abstract : Crop residues, a transient half-plant/half-soil compartment, are a key fully-fledged ecological niche with major biological impact on agrosystems when maintained at the surface of the cultivated soil. They also contribute to the development of plant disease epidemics as main and recurrent source of primary inoculum. To deepen our understanding of this crop residue compartment and its importance regarding the management of residue-borne diseases, we investigated the interactions between the residue microbiome and two important residue-borne fungal pathogens in wheat-oilseed rape rotations systems, Zymoseptoria tritici and Leptosphaeria maculans. Firstly, we characterized the temporal dynamics of fungal and bacterial communities associated with a large set of residues sampled in three wheat-oilseed rape rotation plots over a two-year period. The communities were characterized by metabarcoding and complementary isolations. Beyond the constitution of fungal and bacterial reference collections, this allowed the comparison between the effectiveness of cultivation-independent and dependent methods. The impact of plant species, seasonality (cropping season and degradation), and rotation on the microbiome of crop residues was demonstrated for both fungal and bacterial communities. The impact of plant species on the residue microbiome decreased over time, with the replacement of plant-specific genera by more generalist taxa originating from the soil. The cultivation-dependent method used for bacteria enabled to isolate most of the abundant taxa identified by metabarcoding (unlike fungi, due to technical biases) demonstrating the complementarity of both methods. Secondly, the effect of the presence of Z. tritici and L. maculans on the wheat and oilseed rape residue microbiome, respectively, was assessed by combining linear discriminant analyses (LDA) and ecological network analyses (ENA). For wheat, we compared the bacterial and fungal communities associated with residues, with and without preliminary Z. tritici inoculation, in or without contact with the soil, on four sampling dates during two consecutive years. The number of microorganisms promoted or inhibited by Z. tritici infection decreased over time, and was smaller for residues in contact with the soil. Although many microorganisms were impacted by the infection with the pathogen, few interacted directly with Z. tritici, despite it was considered as a keystone taxa in ENA. In parallel, the effect of L. maculans on oilseed rape residue microbiome was assessed over one year using two isogenic oilseed rape lines ‘Darmor’ and ‘Darmor-Rlm11’ carrying a resistance gene against L. maculans. As for wheat, microbial communities changed as residues degraded. Despite close communities, LDA highlighted numerous microorganisms impacted by the Rlm11 gene. However, L. maculans was not considered as keystone taxa in ENA. Finally, our results provide essential information on microbial community alterations in wheat and oilseed rape residues induced by fungal pathogens. In particular, species already described as pathogens (e.g. Blumeria graminis, Fusarium, Cladosporium, and Alternaria) or as biocontrol agents (e.g. Trichoderma, Epicoccum, Cryptococcus, Chaetomium) were affected by the presence of both pathogens. Metabarcoding, previously developed for plant and soil compartments, should now benefit from new applied developments to crop residues in order to identify beneficial microorganisms naturally present. The complexity and transience of interactions shows that the use of biological control agents against these diseases seems difficult to implement on residues. Further studies would be needed to use these interactions in a more applied perspective.
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Lydie Kerdraon. Microbial diversity and pathogen-microbiome interactions in crop residues : the case of Zymoseptoria tritici and Leptosphaeria maculans in a wheat-oilseed rape system. Agricultural sciences. Université Paris Saclay (COmUE), 2019. English. ⟨NNT : 2019SACLA011⟩. ⟨tel-03537777⟩

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