Rhizosphere Soil Fungal Communities of Aluminum-Tolerant and -Sensitive Soybean Genotypes Respond Differently to Aluminum Stress in an Acid Soil

Abstract

Different soybean genotypes can differ in their tolerance toward aluminum stress depending on their rhizosphere-inhabiting microorganisms. However, there is limited understanding of the response of fungal communities to different aluminum concentrations across different genotypes. Here, we used metabarcoding of fungal ribosomal markers to assess the effects of aluminum stress on the rhizosphere fungal community of aluminum-tolerant and aluminum-sensitive soybean genotypes. Shifts in fungal community structure were related to changes in plant biomass, fungal abundance and soil chemical properties. Aluminum stress increased the difference in fungal community structure between tolerant and sensitive genotypes. Penicillium, Cladosporium and Talaromyces increased with increasing aluminum concentration. These taxa associated with the aluminum-tolerant genotypes were enriched at the highest aluminum concentration. Moreover, complexity of the co-occurrence network associated with the tolerant genotypes increased at the highest aluminum concentration. Collectively, increasing aluminum concentrations magnified the differences in fungal community structure between the two studied tolerant and sensitive soybean genotypes. This study highlights the possibility to focus on rhizosphere fungal communities as potential breeding target to produce crops that are more tolerant toward heavy metal stress or toxicity in general.

Keywords: aluminum toxicity; metabarcoding; network; rhizosphere fungal community; soybean genotypes.

FIGURE 1

Effects of Al addition (0 g kg^–1, 0.2 g kg^–1 and 0.4 g kg^–1 Al³⁺) on soybean biomass (A), abundance of soybean rhizosphere fungal ribosomal ITS1 copies (B), soybean rhizosphere soil fungal Chao1 estimated richness (C) and fungal Shannon diversity index (D). One-way ANOVA with Student’s t-test showed significant differences between the Al-T and Al-S (P < 0.05). Error bars on data points represent the standard error of the mean (n = 6). Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.

FIGURE 2

Non-metric multidimensional scale (NMDS) (A) and canonical analysis of principal coordinates (CAP) (B) based on Bray-Curtis dissimilarities showing differences in rhizosphere fungal community structures at 0 g kg^–1 0.2 g kg^–1, and 0.4 g kg^–1 Al concentrations The stress value for the NMDS as well as Pillai’s trace and the leave-one-out re-allocation success rate of the linear discriminant analysis for the CAP are provided in the plot corners. Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.

FIGURE 3

The relative abundance of rhizosphere fungi at the phylum level was detected in all soil samples. The color of the top half of the outer ring represents the corresponding soil sample group. The lower half of the outer ring is colored to represents different fungi at the phylum level. The thickness of lines was proportional to the relative abundance of rhizosphere fungi at the phylum level. Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.

FIGURE 4

Bipartite association network showing positive associations between the treatment groups and the 163 significantly (q < 0.1) associated OTUs. Node sizes represent relative abundance of the OTUs. Edges represent the associations of individual OTUs with the treatments. The network structure was generated using the edge-weighted (association strength) Fruchterman-Reingold algorithm such that OTUs with similar associations and treatments with similar structure are clustered. Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.

FIGURE 5

The relative abundance of the genera that associated to Al-tolerant soybean genotype. Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.

FIGURE 6

Co-occurrence network of the rhizosphere fungal community for different Al concentrations and soybean genotypes, i.e., 0 Al-T (A), 0 Al-S (B), 0.2 Al-T (C), 0.2 Al-S (D), 0.4 Al-T (E) and 0.4 Al-S (F). Nodes represent OTUs colored-coded by phyla and scaled proportional to the number of connections (node degree). Connections were drawn at r > 0.8 (positive correlations, red) or r < –0.8 (negative correlations, blue) and P < 0.05. Al-T: Al-tolerant soybean genotypes; Al-S: Al-sensitive soybean genotypes.