Schizotrophic Sclerotinia sclerotiorum-Mediated Root and Rhizosphere Microbiome Alterations Activate Growth and Disease Resistance in Wheat

Abstract

Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, providing protection against Fusarium head blight and stripe rust and enhancing wheat yield. In this study, we found that wheat seed treatment with strain DT-8, infected with S. sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1) and used as a "plant vaccine" for brassica protection, could significantly increase the diversity of the fungal and bacterial community in rhizosphere soil, while the diversity of the fungal community was obviously decreased in the wheat root. Interestingly, the relative abundance of potential plant growth-promoting rhizobacteria (PGPR) and biocontrol agents increased significantly in the DT-8-treated wheat rhizosphere soil. These data might be responsible for wheat growth promotion and disease resistance. These results may provide novel insights for understanding the interaction between the schizotrophic microorganism and the microbiota of plant roots and rhizosphere, screening and utilizing beneficial microorganisms, and further reducing chemical pesticide utilization and increasing crop productivity. IMPORTANCE Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to increase world crop production. S. sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, providing protection against Fusarium head blight and stripe rust and enhancing wheat yield. In this study, we discovered that S. sclerotiorum treatment increased the diversity of the soil fungal and bacterial community in rhizosphere soil, while the diversity of the fungal community was obviously decreased in the wheat root. More importantly, the relative abundance of potential PGPR and bio-control agents increased significantly in the S. sclerotiorum-treated wheat rhizosphere soil. The importance of this work is that schizotrophic S. sclerotiorum promotes wheat growth and enhances resistance against fungal diseases via changes in the structure of the root and rhizosphere microbiome.

Keywords: PGPR; S. sclerotiorum; Schizotrophic microorganism; biocontrol agents; microbiome; wheat.

FIG 1

S. sclerotiorum promotes wheat growth. (A) Representative image of wheat plants treated with strain DT-8 in the field at the anthesis stage. (B) Detection of wheat root vigor at the anthesis stage (t test, P < 0.001). (C) Detection of the nitrogen content in wheat flag leaves at the anthesis stage (t test, P < 0.05). (D and E) The total nitrogen and available nitrogen content in the soil. Five replicates for the wheat samples and the soil samples were used. *, P < 0.05; ***, P < 0.001.

FIG 2

(A to H) α-Diversity of the fungi (A to D) and bacteria (E to H) in wheat communities. α-Diversity estimates of the fungi or bacteria in rhizosphere soil and root samples. SD, DT-8-treated wheat plant rhizosphere soil; SC, nontreated wheat plant rhizosphere soil; WRD, DT-8-treated wheat plant root; WRC, nontreated wheat plant root. Five replicates were included for the rhizosphere soil and root samples. *, P < 0.05; **, P < 0.01.

FIG 3

β-Diversity (NMDS) of the fungi and bacteria in wheat rhizosphere soil and root communities. (A and B) Nonmetric multidimensional scaling (NMDS) of fungi (stress = 0.079) (A) and bacteria (stress = 0.016) (B) communities. (C and D) Hierarchical clustering (group average linkage) of the fungus (C) and bacterium (D) samples based on Bray-Curtis similarity. NMDS and hierarchical clusters were based on 5 biological replicates (rhizosphere soil and root samples).

FIG 4

Microbiome composition at the phylum level of rhizosphere soil and root samples. (A) Relative sequence abundance of fungal phyla associated with the rhizosphere soil and the roots. The phylum Ascomycota has been described as 7 OTUs at the class level (Dothideomycetes, Sordariomycetes, Leotiomycetes, Eurotiomycetes, Arthoniomycetes, Pezizomycetes, and Saccharomycetes). (B) Relative sequence abundance of bacterial phyla associated with the rhizosphere soil and the roots. The phylum Proteobacteria has been described as 3 OTUs at the subclass level (Alpha-, Delta-, and Gammaproteobacteria). Biological replicates are displayed in separate stacked bars. Major contributing phyla are displayed in different colors, and minor contributing phyla are grouped and displayed in gray. Low-abundance taxonomic groups with less than 1% of total reads across all samples are highlighted in green.

FIG 5

Heatmap of the dominant fungi and bacteria at the genus level in the rhizosphere and root samples. (A and B) The differentially abundant genera of fungi in roots and the rhizosphere soil samples. (C and D) The differentially abundant genera of bacteria in roots and the rhizosphere soil samples (FDR P values < 0.05).

FIG 6

The overlaps of the wheat-associated microbiome at the OTU level in all samples. (A) Fungal OTUs in the rhizosphere soil and root samples. (B) Bacterial OTUs in the rhizosphere soil and root samples.