Outbreaks of Root Rot Disease in Different Aged American Ginseng Plants Are Associated With Field Microbial Dynamics

Abstract

American ginseng (Panax quinquefolium L.) is a perennial plant that is cultivated for medicinal purposes. Unfortunately, outbreaks of root rot disease in American ginseng (AG) reduce yields and result in serious economic losses. Information on the dynamics of soil microbial communities associated with healthy and diseased AG of different ages is limited. The present study explored the differences in field soil microbial community structure, composition, interaction, and their predictive functions associated with healthy and diseased AG at different growth ages. Changes in soil physicochemical properties were also examined to determine the possible reasons for disease outbreaks. Results revealed that in different growth years, the genera of soil-borne pathogens, such as Alternaria, Botrytis, Cladosporium, Sarocladium, and Fusarium, were increased in diseased AG soil samples in comparison with those in the healthy AG soil samples. In contrast, the abundance of some key and potentially beneficial microbes, such as Bacillus, Chaetomium, Dyella, Kaistobacter, Paenibacillus, Penicillium, and Trichoderma, was decreased. Additionally, as AG plants age, the relative abundance of symbiotic fungi tended to decrease, while the relative abundance of potential plant pathogenic fungi gradually increased. Various soil properties, such as available phosphorus, the ratio of total nitrogen to total phosphorus (N/P), and pH, were significantly (P < 0.05) associated with microbial community composition. Our findings provide a scientific basis for understanding the relationship among the root rot disease outbreaks in American ginseng as well as their corresponding soil microbial communities and soil physicochemical properties.

Keywords: American ginseng; disease outbreaks; microbial communities; pathogens; soil physicochemical properties.

FIGURE 1

Chao1 and Shannon indices of bacterial (A,B) and fungal (C,D) communities. Different letters above the bars indicate significant differences among samples. Significant differences between sample groups were determined by one-way ANOVA followed by Duncan’s multiple range test, P < 0.05; Venn diagrams of bacteria (E) and fungi (F) at the genus level in soils obtained from different aged healthy and diseased AG plants. H2, soils obtained from 2-year-old healthy AG plants; D2, soils obtained from 2-year-old diseased AG plants; H3, soils obtained from 3-year-old healthy AG plants; D3, soils obtained from 3-year-old diseased AG plants; H4, soils obtained from 4-year-old healthy AG plants; D4, soils obtained from 4-year-old diseased AG plants.

FIGURE 2

Between-class analysis of bacterial (A) and fungal (B) communities (OTU level) and their co-inertia (C). H2, soils obtained from 2-year-old healthy AG plants; D2, soils obtained from 2-year-old diseased AG plants; H3, soils obtained from 3-year-old healthy AG plants; D3, soils obtained from 3-year-old diseased AG plants; H4, soils obtained from 4-year-old healthy AG plants; D4, soils obtained from 4-year-old diseased AG plants.

FIGURE 3

Relative abundances of the top 10 most abundant bacteria (A) and fungi (B) at the phylum level in soil samples obtained from different aged healthy and diseased AG plants. Relative abundances of symbiotic (C) and pathogenic (D) fungi detected in the soil of different aged healthy and diseased AG plants based on FUNGuild analysis. The error bars represent standard deviations of the means. Different letters above the bars indicate significant differences among samples at P < 0.05 based on one-way ANOVA followed by Duncan’s multiple range test. H2, soils obtained from 2-year-old healthy AG plants; D2, soils obtained from 2-year-old diseased AG plants; H3, soils obtained from 3-year-old healthy AG plants; D3, soils obtained from 3-year-old diseased AG plants; H4, soils obtained from 4-year-old healthy AG plants; D4, soils obtained from 4-year-old diseased AG plants.

FIGURE 4

Biomarkers of healthy and diseased AG microbiota at different plant ages, calculated using the LEfSe method. Only results with | LDA| > 2, P < 0.05, in Tukey’s honestly significant difference test are shown. (A,C,E) Represent the bacterial biomarkers in soil samples obtained from 2-, 3-, and 4-year-old AG plants, respectively, (B,D,F), represent the fungal biomarkers in soil samples obtained from 2-, 3-, and 4-year-old AG plants, respectively. H2, soils obtained from 2-year-old healthy AG plants; D2, soils obtained from 2-year-old diseased AG plants; H3, soils obtained from 3-year-old healthy AG plants; D3, soils obtained from 3-year-old diseased AG plants; H4, soils obtained from 4-year-old healthy AG plants; D4, soils obtained from 4-year-old diseased AG plants.

FIGURE 5

Potential “driver taxa” in the soil obtained from 2-year-old AG plants as determined in microbial co-occurrence networks between soils obtained from healthy and diseased AG plants. Node sizes are proportional to their scaled NESH (neighbor shift) score (a score identifying important microbial taxa of microbial association networks), and a node is colored red if its betweenness increases when comparing soil microbiomes associated with healthy and diseased plants. As a result, large red nodes denote particularly important driver taxa, and these taxa names are shown in red color. Green edges: association present only in healthy ginseng microbiomes; red edges: association present only in diseased plant microbiomes; blue edges: association present in both healthy and diseased plant microbiomes.

FIGURE 6

RDA of the correlation between bacterial (A) and fungal (B) communities (OTU level) with physicochemical factors of the obtained soil samples (*0.01 < P ≤ 0.05, **0.5 < P ≤ 0.01, and ***0.01 < P ≤ 0.001. AP, available phosphorus; AK, available potassium; KMnO₄-C, KMnO₄-oxidizable carbon; EC, electrical conductivity; C/N, the ratio of soil organic matter to soil total nitrogen; N/P, the ratio of soil total nitrogen to soil total phosphorus). H2, soils obtained from 2-year-old healthy AG plants; D2, soils obtained from 2-year-old diseased AG plants; H3, soils obtained from 3-year-old healthy AG plants; D3, soils obtained from 3-year-old diseased AG plants; H4, soils obtained from 4-year-old healthy AG plants; D4, soils obtained from 4-year-old diseased AG plants.