Dataset Information

Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota.

ABSTRACT: BACKGROUND:Soils are a key component of agricultural productivity, and soil microbiota determine the availability of many essential plant nutrients. Agricultural domestication of soils, that is, the conversion of previously uncultivated soils to a cultivated state, is frequently accompanied by intensive monoculture, especially in the developing world. However, there is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domestication, including to what extent crop plants impact soil microbiota composition, and how changes in microbiota composition arising from cultivation affect crop performance. RESULTS:We show here that continuous monoculture (>?8 growing seasons) of the major food crop rice under flooded conditions is associated with a pronounced shift in soil bacterial and archaeal microbiota structure towards a more consistent composition, thereby domesticating microbiota of previously uncultivated sites. Aside from the potential effects of agricultural cultivation practices, we provide evidence that rice plants themselves are important drivers of the domestication process, acting through selective enrichment of specific taxa, including methanogenic archaea, in their rhizosphere that differ from those of native plants growing in the same environment. Furthermore, we find that microbiota from soils domesticated by rice cultivation contribute to plant-soil feedback, by imparting a negative effect on rice seedling vigor. CONCLUSIONS:Soil domestication through continuous monoculture cultivation of rice results in compositional changes in the soil microbiota, which are in part driven by the rice plants. The consequences include a negative impact on plant performance and increases in greenhouse gas emitting microbes.

SUBMITTER: Edwards J

PROVIDER: S-EPMC6814045 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota.

Edwards Joseph J Santos-Medellín Christian C Nguyen Bao B Kilmer John J Liechty Zachary Z Veliz Esteban E Ni Jiadong J Phillips Gregory G Sundaresan Venkatesan V

Genome biology 20191024 1

<h4>Background</h4>Soils are a key component of agricultural productivity, and soil microbiota determine the availability of many essential plant nutrients. Agricultural domestication of soils, that is, the conversion of previously uncultivated soils to a cultivated state, is frequently accompanied by intensive monoculture, especially in the developing world. However, there is limited understanding of how continuous cultivation alters the structure of prokaryotic soil microbiota after soil domes ...[more]

PMID: 31651356

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Project description:Backgrounds and aimsNegative plant-soil feedbacks (PSFs) are thought to promote species coexistence, but most evidence is derived from theoretical models and data from plant monoculture experiments.MethodsWe grew Anthoxanthum odoratum and Centaurea jacea in field plots in monocultures and in mixtures with three ratios (3:1, 2:2 and 1:3) for three years. We then tested in a greenhouse experiment the performance of A. odoratum and C. jacea in pots planted with monocultures and 1:1 mixtures and filled with live and sterile soils collected from the field plots.ResultsIn the greenhouse experiment, C. jacea produced less aboveground biomass in soil conditioned by C. jacea monocultures than in soil conditioned by A. odoratum monocultures, while the aboveground biomass of A. odoratum in general did not differ between the two monospecific soils. The negative PSF effect was greater in the 1:1 plant mixture than in plant monocultures for A. odoratum but did not differ for C. jacea. In the greenhouse experiment, the performance of C. jacea relative to A. odoratum in the 1:1 plant mixture was negatively correlated to the abundance of C. jacea in the field plot where the soil was collected from. This relationship was significant both in live and sterile soils. However, there was no relationship between the performance of A. odoratum relative to C. jacea in the 1:1 plant mixture in the greenhouse experiment and the abundance of A. odoratum in the field plots.ConclusionsThe response of a plant to PSF depends on whether the focal species grows in monocultures or in mixtures and on the identity of the species. Interspecific competition can exacerbate the negative plant-soil feedbacks compared to intraspecific competition when a plant competes with a stronger interspecific competitor. Moreover, the abundance of a species in mixed plant communities, via plant-soil feedback, negatively influences the relative competitiveness of that species when it grows later in interspecific competition, but this effect varies between species. This phenomenon may contribute to the coexistence of competing plants under natural conditions through preventing the dominance of a particular plant species.

Project description:Application of plant artificial cultivation substrates lead to alteration of rhizosphere environment. Whether this alteration could lead to root microbiome variation was limitedly investigated. This work aims to determine the diversity shifts in the root microbiome of cucumber under different plant cultivation substrates and predict corresponding function of these different root bacterial microbiota. Cucumber root samples cultivated with two artificial cultivation substrates and greenhouse soils were prepared. Subsequently, high throughput sequencing and bioinformatics analysis were applicated to compare the root bacterial diversity of cucumber cultivated in different substrates and their corresponding function. In total, 311,039 sequences were obtained, and they were annotated to 42 operational taxonomic units (OTUs), belonging to 28 genera, 18 families, 12 orders, four classes, and three phyla. The α and β diversity of samples from the two cultivation substrates and greenhouse soils were significantly different. Only 2-3 bacterial species were found to be discrepancy between cucumber root samples from artificial cultivation substrates and from greenhouse soils. The relative abundance of genus Asticcacaulis, Methylophilus, Massilia, Dyella, and Devosia in samples of artificial cultivation substrates was significantly higher than that of soils, while the relative abundance of genus Phenylobacterium, Noviherbaspirillum, and Arenimonas was significantly lower than that of soils. Besides, compared to cucumber root bacterial community cultivated in soils, the abundance of synthetic pathways for flavonoids and flavonols, bile acids, indole alkaloids, lactose, and neolactose increased by 41.6-, 28.7-, 5.9-, and 5.5-fold, respectively, in the bacterial community of the substrate 1-cultivated roots, and the abundance of clavulanic acid, receptor interaction, sesquiterpenoid, bile acid, flavonoid and flavonol, indole alkaloid, lactose, and neolactose synthetic pathways increased by 42.3-, 32.4-, 32.4-, 13.9-, 10.3-, 6.3-, and 5.2-fold, respectively, in the bacterial community of the substrate two-cultivated roots. This paper verified the diversity shifts in the root microbiome of cucumber under different plant cultivation substrates. Besides, the corresponding function difference of these different root bacterial microbiota was predicted. This work would provide theoretical support for discovering microbial resources and building artificial microbial flora.

Dataset Information

Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota.

Publications

Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota.

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