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Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean.

ABSTRACT: Over the past century, plant breeding programs have substantially improved plant growth and health, but have not yet considered the potential effects on the plant microbiome. Here, we conducted metatranscriptome analysis to determine if and how breeding for resistance of common bean against the root pathogen Fusarium oxysporum (Fox) affected gene expression in the rhizobacterial community. Our data revealed that the microbiome of the Fox-resistant cultivar presented a significantly higher expression of genes associated with nutrient metabolism, motility, chemotaxis, and the biosynthesis of the antifungal compounds phenazine and colicin V. Network analysis further revealed a more complex community for Fox-resistant cultivar and indicated Paenibacillus as a keystone genus in the rhizosphere microbiome. We suggest that resistance breeding in common bean has unintentionally co-selected for plant traits that strengthen the rhizosphere microbiome network structure and enrich for specific beneficial bacterial genera that express antifungal traits involved in plant protection against infections by root pathogens.

SUBMITTER: Mendes LW

PROVIDER: S-EPMC6246553 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean.

Mendes Lucas William LW Mendes Rodrigo R Raaijmakers Jos M JM Tsai Siu Mui SM

The ISME journal 20180717 12

Over the past century, plant breeding programs have substantially improved plant growth and health, but have not yet considered the potential effects on the plant microbiome. Here, we conducted metatranscriptome analysis to determine if and how breeding for resistance of common bean against the root pathogen Fusarium oxysporum (Fox) affected gene expression in the rhizobacterial community. Our data revealed that the microbiome of the Fox-resistant cultivar presented a significantly higher expres ...[more]

PMID: 30018368

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Project description:Negative plant-soil feedback (NPSF) due to the buildup of soilborne pathogens in soil is a major obstacle in sustainable agricultural systems. Beneficial rhizosphere microfloras are recruited by plants, and mediating this has become a strategic priority to manipulate plant health. Here, we found that foliar infection of Panax notoginseng by Alternaria panax changed plant-soil feedback from negative to positive. Foliar infection modified the rhizosphere soil microbial community and reversed the direction of the buildup of the soilborne pathogen Ilyonectria destructans and beneficial microbes, including Trichoderma, Bacillus, and Streptomyces, in rhizosphere soil. These beneficial microbes not only showed antagonistic ability against the pathogen I. destructans but also enhanced the resistance of plants to A. panax. Foliar infection enhanced the exudation of short- and long-chain organic acids, sugars, and amino acids from roots. In vitro and in vivo experiments validated that short- and long-chain organic acids and sugars play dual roles in simultaneously suppressing pathogens but enriching beneficial microbes. In summary, foliar infection could change root secretion to drive shifts in the rhizosphere microbial community to enhance soil health, providing a new strategy to alleviate belowground disease in plants through aboveground inducement. IMPORTANCE Belowground soilborne disease is the main factor limiting sustainable agricultural production and is difficult to manage due to the complexity of the soil environment. Here, we found that aboveground parts of plants infected by foliar pathogens could enhance the secretion of organic acids, sugars, and amino acids in root exudates to suppress soilborne pathogens and enrich beneficial microbes, eventually changing the plant and soil feedback from negative to positive and alleviating belowground soilborne disease. This is an exciting strategy by which to achieve belowground soilborne disease management by manipulating the aboveground state through aboveground stimulation.

Project description:RNA stable isotope probing and high-throughput sequencing were used to characterize the active microbiomes of bacteria and fungi colonizing the roots and rhizosphere soil of oilseed rape to identify taxa assimilating plant-derived carbon following 13CO2 labeling. Root- and rhizosphere soil-associated communities of both bacteria and fungi differed from each other, and there were highly significant differences between their DNA- and RNA-based community profiles. Verrucomicrobia, Proteobacteria, Planctomycetes, Acidobacteria, Gemmatimonadetes, Actinobacteria, and Chloroflexi were the most active bacterial phyla in the rhizosphere soil. Bacteroidetes were more active in roots. The most abundant bacterial genera were well represented in both the 13C- and 12C-RNA fractions, while the fungal taxa were more differentiated. Streptomyces, Rhizobium, and Flavobacterium were dominant in roots, whereas Rhodoplanes and Sphingomonas (Kaistobacter) were dominant in rhizosphere soil. "Candidatus Nitrososphaera" was enriched in 13C in rhizosphere soil. Olpidium and Dendryphion were abundant in the 12C-RNA fraction of roots; Clonostachys was abundant in both roots and rhizosphere soil and heavily 13C enriched. Cryptococcus was dominant in rhizosphere soil and less abundant, but was 13C enriched in roots. The patterns of colonization and C acquisition revealed in this study assist in identifying microbial taxa that may be superior competitors for plant-derived carbon in the rhizosphere of Brassica napusIMPORTANCE This microbiome study characterizes the active bacteria and fungi colonizing the roots and rhizosphere soil of Brassica napus using high-throughput sequencing and RNA-stable isotope probing. It identifies taxa assimilating plant-derived carbon following 13CO2 labeling and compares these with other less active groups not incorporating a plant assimilate. Brassica napus is an economically and globally important oilseed crop, cultivated for edible oil, biofuel production, and phytoextraction of heavy metals; however, it is susceptible to several diseases. The identification of the fungal and bacterial species successfully competing for plant-derived carbon, enabling them to colonize the roots and rhizosphere soil of this plant, should enable the identification of microorganisms that can be evaluated in more detailed functional studies and ultimately be used to improve plant health and productivity in sustainable agriculture.

Dataset Information

Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean.

Publications

Breeding for soil-borne pathogen resistance impacts active rhizosphere microbiome of common bean.

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