Plant development influences dynamic shifts in the root compartment microbiomes of wild and domesticated finger millet cultivars

Abstract

Background: Plant-microbe interactions in the rhizosphere and endosphere are crucial for maintaining plant health and ecosystem dynamics. These interactions are shaped by several factors, including the plant's developmental stage, domestication, and specific root compartments. Different plant cultivars influence unique microbial communities by secreting root exudates that either support beneficial symbionts or inhibit pathogens. This study examined the microbial community structures in the endosphere and rhizosphere of wild-type finger millet and five domesticated cultivars at two developmental stages.

Results: Our results revealed that the plant developmental stage, root compartment, and domestication significantly influence the root-associated microbiomes. Interestingly, only about 8% of the core microbiota was consistently shared between the soil and plants, indicating that 92% shifted dynamically depending on plant type and developmental stage. Pseudomonadota, Actinomycedota, and Bacteroidota were the dominant bacterial phyla, while Ascomycota and Basidiomycota were the primary fungal phyla across all samples, displaying distinct abundance patterns. Notably, an increase in Actinomycedota in the endosphere correlated with a reduction in Pseudomonadota. The most significant shifts in microbial community composition occurred in the rhizosphere during the flowering stage, primarily driven by the genus Pseudomonas. These findings demonstrate that plant developmental stages and domestication influence the recruitment of specific microbial taxa to meet the plant's needs, particularly in various root compartments. This selective recruitment highlights the active role of plants in shaping their microbiomes, providing insights into the potential for manipulating these communities to enhance crop productivity sustainably.

Conclusion: Our results indicate that both the host developmental stage and domestication significantly influence the assembly and structure of the plant microbiome. Plant root compartments can selectively recruit specific taxa from associated core microbial communities to meet their needs, depending on the plant's developmental stage and the particular root compartment involved. These findings demonstrate that the deterministic selection pressures exerted by plants during their growth and development greatly affect their microbial communities. This has important implications for developing sustainable farming practices, reducing reliance on chemical fertilizers and pesticides, and enhancing future crop productivity.

Keywords: Amplicon sequencing; Domestication; Endosphere; Finger millet; Flowering stage; Microbiome; Plant microbiology; Plant microbiome; Rhizosphere; Seedling stage.

Fig. 1

Comparative Analysis of Bacteriota and Mycobiota Across Plant Compartments. This figure shows the top ten bacterial phyla (A), all detected fungal phyla (B), the top ten bacterial genera (C), and the top ten fungal genera (D) identified in the endosphere and rhizosphere of plants during the seedling and flowering stages. The samples compared include control (soil without plantation), wild type (Africana), and five different cultivars (Wama, Tessema, Tadesse, Padet and Axum). Relative abundances > 0 are shown in the heat maps of (C) and (D). The X-axis represents the sample’s names, and the Y-axis indicates the relative abundance values of the corresponding phylum and genus level in percentage

Fig. 2

UpSet plot showing the results of core microbiome analyses of the bacterial genera (A) and fungal genera (B) present in the endosphere and rhizosphere of wild-type plants (WT; Africana), five different cultivars (Wama, Tessema, Tadesse, Padet, and Axum), and control soil (soil without plantation) during the seedling and flowering stages. The bars in the lower left corner and the columns at the top indicate the number of detected and shared genera. Connected dots represent genera shared among sample types (control, wild type, and cultivars), while single dots represent species unique to a specific sample type

Fig. 3

Changes in Alpha Diversity of Bacteriota and Mycobiota. This figure shows the alpha diversity (Shannon index on the Y axis) of bacteriota (A) and mycobiota (B), estimated using Shannon’s diversity index. The alpha diversity in the rhizosphere was clearly lower than in the endosphere during both the seedling (p = 0.049) and flowering stages (p < 0.001). Moreover, the alpha diversity of the rhizosphere declined significantly during the flowering stage (p < 0.001). No significant changes were observed in the endosphere or among with mycobiota (p = 0.186). The data are represented using median values for each sample type, including control (soil without plantation), wild type (Africana), and five domesticated cultivars (Wama, Tessema, Tadesse, Padet, and Axum). All p-values were adjusted for multiple comparisons

Fig. 4

Differences in Beta Diversity of Bacteriota and Mycobiota. This figure shows the beta diversity of bacteriota (A) and mycobiota (B) in two plant compartments and plant developmental stages. Significant differences were found in all pairwise comparisons (p < 0.05; p values were corrected for multiple comparisons)