Rhizosphere microbiome structure alters to enable wilt resistance in tomato

Kwak, Min Jung; Kong, Hyun Gi; Choi, Kihyuck; Kwon, Soon Kyeong; Song, Ju Yeon; Lee, Jidam; Lee, Pyeong An; Choi, Seok Reyol; Seo, Minseok; Lee, Hyoung Ju; Jung, Eun Joo; Park, Hyein; Roy, Nazish; Kim, Heebal; Lee, Myeong Min; Rubin, Edward M.; Lee, Seon-Woo; Kim, Jihyun F.

doi:10.1038/nbt.4232

Cited by 584 publications

(485 citation statements)

References 64 publications

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“…Although this type of investigation is not novel per se in tomato (Toju et al, 2019), our results revealed fundamentally novel insights into plant’s adaptation to nitrogen fertilisers and the implication for crop yield. Similar to what has recently been postulated for tomato pathogen protection (Kwak et al, 2018), our results predicts that the use of field-derived, sequencing data will allow scientists to identify “signatures” of the plant microbiota that can be targeted to enhance plant performance. This approach, which we define as lab-in-the-field, will be key towards the rationalisation of nitrogen (and other treatments) application in agriculture and we anticipate will pave the way for the effective exploitation of the plant microbiota for agricultural purposes (Schlaeppi and Bulgarelli, 2015; Toju et al, 2018).…”

Section: Discussionsupporting

confidence: 81%

“…Perhaps not surprisingly, tomato is gaining momentum as an experimental system to study host-microbiota interactions in crop plants. Recent investigations revealed novel insights into the assembly cues of the microbiota associated to this plant (Bergna et al, 2018; Toju et al, 2019) and the contribution of microbes thriving at the tomato root-soil interface to pathogen protection (Chialva et al, 2018; Kwak et al, 2018). However, the composition and functional potential of the tomato microbiota and their interdependency from nitrogen fertilisers remain to be elucidated.…”

Section: Introductionmentioning

confidence: 99%

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Nitrogen Fertilisers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants

Caradonia

Ronga

Catellani

et al. 2019

Preprint

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The microbial communities thriving at the root-soil interface have the potential to improve plant growth and sustainable crop production. Yet, how agricultural practices, such as the application of either mineral or organic nitrogen fertilisers, impact on the composition and functions of these communities remains to be fully elucidated. By deploying a two-pronged 16S rRNA gene sequencing and predictive metagenomics approach we demonstrated that the bacterial microbiota of field-grown tomato (Solanum lycopersicum) plants is the product of a selective process that progressively differentiates between rhizosphere and root microhabitats. This process initiates as early as plants are in a nursery stage and it is then more marked at late developmental stages, in particular at harvest. This selection acts on both the bacterial relative abundances and phylogenetic assignments, with a bias for the enrichment of members of the phylum Actinobacteria in the root compartment. Digestate-based and mineral-based nitrogen fertilisers trigger a distinct bacterial enrichment in both rhizosphere and root microhabitats. This compositional diversification mirrors a predicted functional diversification of the root-inhabiting communities, manifested predominantly by the differential enrichment of genes associated to ABC transporters and the two-component system. Together, our data suggest that the microbiota thriving at the tomato root-soil interface is modulated by and in responses to the type of nitrogen fertiliser applied to the field.

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Section: Discussionsupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Nitrogen Fertilisers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants

Caradonia

Ronga

Catellani

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Following our previous finding that rhizosphere concentrations of daidzein remain high even after the key period for establishment of rhizobial symbiosis, we found that daidzein has additional functions in shaping the bacterial community in the rhizosphere, answering a long‐unresolved question. Plants modulate the rhizosphere microbial community, assembling beneficial microbes to reduce damage from pathogens (Kwak et al, ; Stringlis et al, ) and enhance uptake of nutrients (Castrillo et al, ). It is tempting to speculate that soybean secretes daidzein into the soil within the vicinity of the root surface, where daidzein helps to assemble a beneficial microbial community by acting as more of a repellant than an attractant.…”

Section: Discussionmentioning

confidence: 99%

Rhizosphere modelling reveals spatiotemporal distribution of daidzein shaping soybean rhizosphere bacterial community

Okutani

Hamamoto

Aoki

et al. 2020

Plant Cell & Environment

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Plant roots nurture a wide variety of microbes via exudation of metabolites, shaping the rhizosphere's microbial community. Despite the importance of plant specialized metabolites in the assemblage and function of microbial communities in the rhizosphere, little is known of how far the effects of these metabolites extend through the soil. We employed a fluid model to simulate the spatiotemporal distribution of daidzein, an isoflavone secreted from soybean roots, and validated using soybeans grown in a rhizobox. We then analysed how daidzein affects bacterial communities using soils artificially treated with daidzein. Simulation of daidzein distribution showed that it was only present within a few millimetres of root surfaces. After 14 days in a rhizobox, daidzein was only present within 2 mm of root surfaces. Soils with different concentrations of daidzein showed different community composition, with reduced α‐diversity in daidzein‐treated soils. Bacterial communities of daidzein‐treated soils were closer to those of the soybean rhizosphere than those of bulk soils. This study highlighted the limited distribution of daidzein within a few millimetres of root surfaces and demonstrated a novel role of daidzein in assembling bacterial communities in the rhizosphere by acting as more of a repellant than an attractant.

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“…Although we sampled healthy-looking plants in their natural habitats, we cannot exclude the possibility that some of these bacterial strains represent widespread pathogens that negatively affect plant fitness without causing disease symptoms in nature 36 . Alternatively, these taxa might carry out widespread and important beneficial functions for A. thaliana survival such as pathogen protection e.g., Pseudomonas, Pelomonas, Acidovorax, Flavobacterium 3, 35, 37 , abiotic stress tolerance, or plant growth promotion (e.g., Bradyrhizobium, Burkholderia 38, 39 ). It remains to be seen whether this widespread association between plant roots and bacteria is evolutionary ancient and the extent to which it has contributed to plant adaptation to terrestrial ecosystems.…”

Section: Discussionmentioning

confidence: 99%

Root microbiota assembly and adaptive differentiation among European Arabidopsis populations

Thiergart

Durán

Ellis

et al. 2019

Preprint

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20Factors that drive continental-scale variation in root microbiota and plant adaptation are poorly 21 understood. We monitored root-associated microbial communities in Arabidopsis thaliana and co-22 occurring grasses at 17 European sites across three years. Analysis of 5,625 microbial community 23 profiles demonstrated strong geographic structuring of the soil biome, but not of the root microbiota. 24Remarkable similarity in bacterial community composition in roots of A. thaliana and grasses was 25 explained by the presence of a few diverse and geographically widespread taxa that disproportionately 26 colonize roots across sites. In a reciprocal transplant between two A. thaliana populations in Sweden 27and Italy, we uncoupled soil from location effects and tested their respective contributions to root 28 2 microbiota variation and plant adaptation. The composition of the root microbiota was affected by 29 location and soil origin, and to a lesser degree by host genotype. The filamentous eukaryotes were 30 particularly strongly affected by location. Strong local adaptation between the two A. thaliana 31 populations was observed, with difference in soil properties and microbes of little importance for the 32 observed magnitude of adaptive differentiation. Our results suggest that, across large spatial scales, 33 climate is more important than are soil conditions for plant adaptation and variation in root-associated 34 filamentous eukaryotic communities. 35 36 differentiation among plant populations is still limited beyond classical examples of adaptation to 57 extreme soil conditions 25 . 58 59Here, we tested whether roots of A. thaliana and co-occurring grasses growing in various soils and 60 climatic environments establish stable associations with bacterial and filamentous eukaryotic 61 communities across a latitudinal gradient in Europe. In a reciprocal transplant between two A. thaliana 62 populations in Sweden and Italy, we uncoupled soil from location effects and experimentally tested the 63 hypothesis that soil properties and climate drive root microbiota assembly and adaptive differentiation 64 between the two A. thaliana populations. 65 66We found that a widespread set of bacteria, but not filamentous eukaryotes, establish stable associations 67 with roots of A. thaliana and grasses across 17 sites in Europe, despite strong geographical structuring 68 and variation in the surrounding soil communities. The reciprocal transplant of soil and plant genotypes 69 between two native A. thaliana populations in northern and southern Europe showed that the 70 composition of root microbiota was more affected by soil properties and location than by host genotype. 71The effect of soil was stronger than that of location for root-associated bacteria, whereas the effect of 72 location was stronger for root-associated fungi and oomycetes. Transplant location, rather than origin 73 of soil, also largely accounted for strong selection against the nonlocal A. thaliana genotype at each site. 74Our results suggest that climat...

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Rhizosphere microbiome structure alters to enable wilt resistance in tomato

Cited by 584 publications

References 64 publications

Nitrogen Fertilisers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants

Nitrogen Fertilisers Shape the Composition and Predicted Functions of the Microbiota of Field-Grown Tomato Plants

Rhizosphere modelling reveals spatiotemporal distribution of daidzein shaping soybean rhizosphere bacterial community

Root microbiota assembly and adaptive differentiation among European Arabidopsis populations

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