Environmental factors and host genotype control foliar epiphytic microbial community of wild soybeans across China

Abstract

Introduction: The microbiome inhabiting plant leaves is critical for plant health and productivity. Wild soybean (Glycine soja), which originated in China, is the progenitor of cultivated soybean (Glycine max). So far, the community structure and assembly mechanism of phyllosphere microbial community on G. soja were poorly understood.

Methods: Here, we combined a national-scale survey with high-throughput sequencing and microsatellite data to evaluate the contribution of host genotype vs. climate in explaining the foliar microbiome of G. soja, and the core foliar microbiota of G. soja were identified.

Results: Our findings revealed that both the host genotype and environmental factors (i.e., geographic location and climatic conditions) were important factors regulating foliar community assembly of G. soja. Host genotypes explained 0.4% and 3.6% variations of the foliar bacterial and fungal community composition, respectively, while environmental factors explained 25.8% and 19.9% variations, respectively. We further identified a core microbiome thriving on the foliage of all G. soja populations, including bacterial (dominated by Methylobacterium-Methylorubrum, Pantoea, Quadrisphaera, Pseudomonas, and Sphingomonas) and fungal (dominated by Cladosporium, Alternaria, and Penicillium) taxa.

Conclusion: Our study revealed the significant role of host genetic distance as a driver of the foliar microbiome of the wild progenitor of soya, as well as the effects of climatic changes on foliar microbiomes. These findings would increase our knowledge of assembly mechanisms in the phyllosphere of wild soybeans and suggest the potential to manage the phyllosphere of soya plantations by plant breeding and selecting specific genotypes under climate change.

Keywords: core microbiome; foliar microbiome; host genotype; microbial community assembly; wild soybean.

Figure 1

Relative abundance at genus level of bacterial taxa (A) and fungal taxa (B) in the foliar microbiome of eight genotypes of wild soybean. The total relative abundance of low-abundant bacteria and fungi that accounted for less than 0.5% is indicated as low abundance in darkgrey, and unidentified taxonomic groups are indicated in light grey. At each sampling site, there were three to five technical replicates sampled from three to five plants with the same genotype. Abbreviations for the sample name are depicted in Table S1. The NMDS analysis of bacterial (C) and fungal (D) community at genus level based on Bray-Curtis distances categorized by host genotypes.

Figure 2

Correlation between the dissimilarity of the bacterial (A) and fungal (B) communities and host genetic distance. The distance-decay relationships between dissimilarity of the bacterial (C) and fungal (D) communities and geographical distance.

Figure 3

The neighbor-joining tree of wild soybean populations (left panel) and dendrogram of hierarchical clustering of Bray–Curtis dissimilarity of the bacterial (A) and fungal (B) communities (right panel). The eight genotypes of the microbial community were averaged using biological replicates.

Figure 4

The individual effect of the environmental and host genetic distance variables to explain the variation of bacterial (A) and fungal (B) communities at genus level in the foliar microbiome of wild soybean (“*,” 0.01 < p < 0.05, “**,” 0.01 < p < 0.001, “***,” p < 0.001). The relative importance of individual variables was calculated using rdacca.hp package. GD, genetic distance; MAP, mean annual precipitation; MAT, mean annual temperature; and GHI, global horizontal irradiance. The effects of explanatory variables (geographical, climatic, and host genotype) on bacterial (C) and fungal (D) communities were estimated using variation partition analysis. Shared effects are indicated by the overlap of circles. Geographical factors include longitude and latitude. Climatic factors include MAP, MAT, and GHI. The host genotype represents the host genetic distance.

Figure 5

The core microbes of eight genotypes of bacterial (A) and fungal (B) communities. The relative abundance at the genus level of the core bacterial (C) and fungal (D) taxa in the foliar microbiome of wild soybean. The non-core taxa are indicated in green.

Figure 6

The neighbor-joining (NJ) phylogenetic tree showing the core bacterial (A) and fungal (B) ASVs of the foliar microbiome of wild soybeans.