The Structure of Rhizosphere Fungal Communities of Wild and Domesticated Rice: Changes in Diversity and Co-occurrence Patterns

Abstract

The rhizosphere fungal community affects the ability of crops to acquire nutrients and their susceptibility to pathogen invasion. However, the effects of rice domestication on the diversity and interactions of rhizosphere fungal community still remain largely unknown. Here, internal transcribed spacer amplicon sequencing was used to systematically analyze the structure of rhizosphere fungal communities of wild and domesticated rice. The results showed that domestication increased the alpha diversity indices of the rice rhizosphere fungal community. The changes of alpha diversity index may be associated with the enrichment of Acremonium, Lecythophora, and other specific rare taxa in the rhizosphere of domesticated rice. The co-occurrence network showed that the complexity of wild rice rhizosphere fungal community was higher than that of the domesticated rice rhizosphere fungal community. Arbuscular mycorrhizal fungi (AMF) and soilborne fungi were positively and negatively correlated with more fungi in the wild rice rhizosphere, respectively. For restructuring the rhizomicrobial community of domesticated crops, we hypothesize that microbes that hold positive connections with AMF and negative connections with soilborne fungi can be used as potential sources for bio-inoculation. Our findings provide a scientific basis for reshaping the structure of rhizomicrobial community and furthermore create potential for novel intelligent and sustainable agricultural solutions.

Keywords: arbuscular mycorrhizal fungi; co-occurrence patterns; domestication; rhizosphere; soil-borne fungi.

FIGURE 1

(A) The permutational multivariate analysis of variance (PERMANOVA) output showing the importance of rice domestication, rice species, and origins factors shaping the rhizosphere fungal community. (B) Compositional changes of fungal communities in the rhizospheres of wild and domesticated rice. (C,D) Alpha diversity indices of fungi in the rhizospheres of wild and domesticated rice. The pseudo-F value was used as a proxy for the importance of the factor (A). For the PERMANOVA of domestication factor, all samples were separated into two groups: wild and domesticated rice. For the PERMANOVA of accessions factor, all samples were separated into 12 groups: 12 rice species as described in section “Materials and Methods”. For the PERMANOVA of origins factor, all samples were separated into two groups: African rice and Asian rice. Principal coordinates analysis (PCoA) was performed based on the Bray–Curtis dissimilarity matrix at operational taxonomic units (OTUs) level across all the samples (B). Ellipses demonstrate the mean ± 1 SD, wild rice in purple and domesticated rice in blue. In panels (C,D), wild rice rhizosphere samples, n = 24; domesticated rice rhizosphere samples, n = 35. Different letters within each column indicated significant differences between wild and domesticated rice based on a one-way ANOVA with a Tukey test at the P < 0.05 level.

FIGURE 2

Relative abundances of the dominant fungal phyla (A) and fungal genera (B) in the rhizospheres of wild and domesticated rice. Relative abundance of the dominant fungal phyla and genera were identified by BLAST searching the representative sequence set against the UNITE database, and the sequences not assigned to kingdom fungi were classified as “unknown.” Treatments included the rhizospheres of wild and domesticated rice. The relative abundance of Zygomycota was highest in bulk soil, while the relative abundance of Ascomycota was highest in the rhizosphere of wild and domesticated rice. The relative abundance of Acaulospora was highest in bulk soil, while the relative abundance of Acremonium was highest in the rhizosphere of wild and domesticated rice.

FIGURE 3

Morphology of the arbuscular mycorrhizal fungi-colonized roots of wild (A) and domesticated (B) rice. Colonization rate of the arbuscular mycorrhizal fungi in roots of the rice plants (C).

FIGURE 4

Co-occurrence analysis of the rhizosphere fungal community of wild and domesticated rice. The co-occurrence networks of the rhizosphere fungal community of wild (A) and domesticated (B) rice were constructed based on the SparCC correlation coefficients. An edge stands for a significant positive correlation (SparCC r > 0.5, P < 0.05, red line) or significant negative correlation (SparCC r < –0.5, P < 0.05, blue line). The nodes represent taxa affiliated at the genus level with at least one significant correlation. The size of the node is proportional to the degree (the number of connections). Each node was colored by phyla. The nodes circled by red, white, and black outlines are arbuscular mycorrhizal fungi, hub fungi, and potential plant pathogens, respectively. The nodes representing hub fungi taxa were labeled. The hub taxa of the rhizosphere fungal community of wild (C) and domesticated (D) rice were nodes showing a high degree and betweenness centrality. The dashed lines indicated the threshold values (top 2%). The nodes representing hub fungi taxa were labeled.