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Autotoxin Rg₁ Induces Degradation of Root Cell Walls and Aggravates Root Rot by Modifying the Rhizospheric Microbiome.

ABSTRACT: Management of crop root rot disease is one of the key factors in ensuring sustainable development in agricultural production. The accumulation of autotoxins and pathogens in soil has been reported as a primary driver of root rot diseases; however, less is known about the correlation of plants, their associated pathogens and microbiome mediated by autotoxins as well as the contributions autotoxins make to the occurrence of root rot disease. Here, we integrated metabolomic, transcriptomic, and rhizosphere microbiome analyses to identify the root cell wall degradants cellobiose and d-galacturonic acid as being induced by the autotoxic ginsenoside Rg₁ of Panax notoginseng, and we found that exogenous cellobiose and d-galacturonic acid in addition to Rg₁ could aggravate root rot disease by modifying the rhizosphere microbiome. Microorganisms that correlated positively with root rot disease were enriched and those that correlated negatively were suppressed by exogenous cellobiose, d-galacturonic acid, and Rg₁. In particular, they promoted the growth and infection of the soilborne pathogen Ilyonectria destructans by upregulating pathogenicity-related genes. Cellobiose showed the highest ability to modify the microbiome and enhance pathogenicity, followed by Rg₁ and then d-galacturonic acid. Collectively, autotoxins damaged root systems to release a series of cell wall degradants, some of which modified the rhizosphere microbiome so that the host plant became more susceptible to root rot disease. IMPORTANCE The accumulation of autotoxins and pathogens in soil has been reported as a primary driver of root rot disease and one of the key factors limiting sustainable development in agricultural production. However, less is known about the correlation of plants, their associated pathogens, and the microbiome mediated by autotoxins, as well as the contributions autotoxins make to the occurrence of root rot disease. In our study, we found that autotoxins can damage root systems, thus releasing a series of cell wall degradants, and both autotoxins and the cell wall degradants they induce could aggravate root rot disease by reassembling the rhizosphere microbiome, resulting in the enrichment of pathogens and microorganisms positively related to the disease but the suppression of beneficial microorganisms. Deciphering this mechanism among plants, their associated pathogens, and the microbiome mediated by autotoxins will advance our fundamental knowledge of and ability to degrade autotoxins or employ microbiome to alleviate root rot disease in agricultural systems.

SUBMITTER: Xu Y

PROVIDER: S-EPMC8672892 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:To explore the causal pathogen and the correlated rhizosphere soil microecology of sugarcane root rot, we sampled the sugarcane root materials displaying different disease severity, and the corresponding rhizosphere soil, for systematic root phenotype and microbial population analyses. We found that with increased level of disease severity reflected by above-ground parts of sugarcane, the total root length, total root surface area and total volume were significantly reduced, accompanied with changes in the microbial population diversity and structure in rhizosphere soil. Fungal community richness was significantly lower in the rhizosphere soil samples from mildly diseased plant than that from either healthy plant, or severely diseased plant. Particularly, we noticed that a peculiar decrease of potential pathogenic fungi in rhizosphere soil, including genera Fusarium, Talaromyces and Neocosmospora, with increased level of disease severity. As for bacterial community, Firmicutes was found to be of the highest level, while Acidobacteria and Chloroflexi of the lowest level, in rhizosphere soil from healthy plant compared to that from diseased plant of different severity. FUNGuild prediction showed that the proportion of saprophytic fungi was higher in the rhizosphere soil of healthy plants, while the proportion of pathogenic fungi was higher in the rhizosphere soil of diseased plants. By co-occurrence network analysis we demonstrated the Bacillus and Burkholderia were in a strong interaction with Fusarium pathogen(s). Consistently, the biocontrol and/or growth-promoting bacteria isolated from the rhizosphere soil were mostly (6 out of 7) belonging to Bacillus and Burkholderia species. By confrontation culture and pot experiments, we verified the biocontrol and/or growth-promoting property of the isolated bacterial strains. Overall, we demonstrated a clear correlation between sugarcane root rot severity and rhizosphere soil microbiome composition and function, and identified several promising biocontrol bacteria strains with strong disease suppression effect and growth-promoting properties.

Project description:The stability of microbial communities, especially among core taxa, is essential for supporting plant health. However, the impacts of disease infection on the stability of rhizosphere fungal core microbiome remain largely unexplored. In this study, we delved into the effects of root rot infestation on the community structure, function, network complexity, and stability of Sanqi fungal core microbiomes, employing amplicon sequencing combined with co-occurrence network and cohesion analyses. Our investigation revealed that root rot disease led to a decrease in the α-diversity but an increase in the β-diversity of the Sanqi fungal core microbiomes in the rhizosphere. Notably, Ilyonectria, Plectosphaerella, and Fusarium emerged as indicator species in the rhizosphere core microbiome of root rot-infected Sanqi plants, while Mortierella predominated as the dominant biomarker taxa in healthy soils. Additionally, root rot diminished the complexity and modularity of the rhizosphere networks by reducing the metrics associated with nodes, edges, degrees, and modularity. Furthermore, root rot resulted in a reduction in the proportion of negative connections in the network and the negative/positive cohesion of the entire core fungal microbiome. Particularly noteworthy was the observation that root rot infection destabilized the rhizosphere core fungal microbiome by weakening the negative connectivity associated with beneficial agents. Collectively, these results highlight the significance of the negative connectivity of beneficial agents in ensuring the stability of core microbial community.IMPORTANCERoot rot disease has been reported as the most devastating disease in the production process of artificial cultivated Sanqi ginseng, which seriously threatens the Sanqi industry. This study provides valuable insights into how root rot influences microbial relationships within the community. These findings open up opportunities for disease prevention and the promotion of plant health by regulating microbial interactions. In summary, the research sheds light on the ecological consequences of root rot on rhizosphere fungal microbiomes and offers potential strategies for managing soil-borne diseases and enhancing plant health.

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Autotoxin Rg₁ Induces Degradation of Root Cell Walls and Aggravates Root Rot by Modifying the Rhizospheric Microbiome.

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Autotoxin Rg₁ Induces Degradation of Root Cell Walls and Aggravates Root Rot by Modifying the Rhizospheric Microbiome.