The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi

Ziye Wang; Lu Xu; Xiaoyue Lu; Ruidong Wang; Jie Han; Aihua Yan

doi:10.3389/fmicb.2024.1378273

The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi

Front Microbiol. 2024 Apr 11:15:1378273. doi: 10.3389/fmicb.2024.1378273. eCollection 2024.

Authors

Ziye Wang^{1

2}, Lu Xu^{2

3}, Xiaoyue Lu^{2

3}, Ruidong Wang^{2

3}, Jie Han^{2

3}, Aihua Yan^{2

4}

Affiliations

¹ Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Chinese Academy of Forestry, Ecology and Nature Conservation Institute, Beijing, China.
² College of Forestry, Hebei Agricultural University, Baoding, Hebei, China.
³ Hebei Province Key Laboratory of Forest Trees Germplasm Resources and Forest Protection, Baoding, Hebei, China.
⁴ Hebei Urban Forest Health Technology Innovation Center, Baoding, Hebei, China.

Abstract

The endophytic microbial community reassembles to participate in plant immune balance when the host plants are stressed by pathogens. However, it remains unclear whether this assembly is pathogen-specific and how regulatory pathways are coordinated in multi-pathogens. In order to investigate the effects of infection with Colletotrichum gloeosporioides (Cg treatment) and Fusarium proliferatum (Fp treatment) on walnut leaf endophytic microbiome in their assembly, co-occurrence pattern, and on comprehensive chemical function of the internal environment of leaf, an interaction system of the walnut-pathogenic fungi was constructed using seed embryo tissue culture technology. The study showed differences in the assembly of endophytic microbial communities in walnut trees across three groups (control group, Ck; Cg; Fp) after Cg and Fp treatments. Despite changes in relative abundances, the dominant communities in phyla and genera remained comparable during the infection of the two pathogens. Endophyte fungi were more sensitive to the pathogen challenge than endophyte bacteria. Both promoted the enrichment of beneficial bacteria such as Bacillus and Pseudomonas, changed the modularity of the community, and reduced the stability and complexity of the endophyte community. Pathogenic fungi infection mainly affects the metabolism of porphyrin and chlorophyll, purine metabolism, phenylpropane metabolism, and amino acid metabolism. However, there was no significant difference in the secondary metabolites for the different susceptible plants. By screening endogenous antagonistic bacteria, we further verified that Pseudomonas psychrotolerans and Bacillus subtilis had inhibitory effects on the two pathogenic fungi and participated in the interaction between the leaves and pathogenic fungi. The antibacterial substances may be 1-methylnaphthalene, 1,3-butadiene, 2,3-butanediol, and toluene aldehyde.

Keywords: endogenous antagonistic bacteria; endophytic microbiome; expression mode; metabolome; pathogenic fungi.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study received financial support from thethe National Key Research and Development Programme of China (2023YFD1401302); Science and Technology Research Project of Higher Education Institutions in Hebei Province (ZD2022061); Hebei Modern Agricultural Industrial Technology System Project HBCT2024190208; and the Hebei Provincial Key Research and Development Programme Project (19226515D).