Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

Oyserman, Ben O.; Flores, Stalin Sarango; Griffioen, Thom; Wijk, Elmar van der; Pronk, Lotte J U; Lokhorst, Wouter; Nurfikari, Azkia; Stopnišek, Nejc; Kupczok, Anne; Cordovez, Viviane; Carrión, Víctor J.; Ligterink, Wilco; Snoek, Basten L.; Medema, Marnix H.; Raaijmakers, J.M.

doi:10.1101/2021.12.20.473370

Cited by 6 publications

(10 citation statements)

References 99 publications

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“…S1, Data Set 10). The small QTL effects detected by GEA are similar to the QTL effect sizes identified in GWAS and traditional linkage mapping studies on microbiota (Bergelson, Brachi, et al 2021;Oyserman et al 2022), albeit a larger range of QTL effects was identified in our study. For instance, the top SNP located on position 19,335,417bp on chromosome 2 (SNP 2_19335471), SNP 1_12691514 and SNP 5_5191015 explained a substantial fraction of the presence/absence of OTU4 (root compartment in fall), microbiota diversity (leaf compartment in spring (December)) and pathobiota composition (leaf compartment in fall), respectively (fig.…”

Section: The Relative Importance Of Host Genetics and Ecology In Expl...supporting

confidence: 86%

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The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

Roux

Frachon

Bartoli

2022

Preprint

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Understanding the role of host genome in modulating microbiota variation is a need to shed light into the holobiont theory and overcome the current limits on the description of host-microbiota interactions at the genomic and molecular levels. However, the host genetic architecture structuring microbiota is only partly described in plants. In addition, most association genetic studies on microbiota are often carried out outside the native habitats where the host evolve and the identification of signatures of local adaptation on the candidate genes has been overlooked. To fill these gaps and dissect the genetic architecture driving adaptive plant-microbiota interactions, we adopted a Genome-Environmental-Association (GEA) analysis on 141 whole-genome sequenced natural populations of Arabidopsis thaliana characterized in situ for their leaf and root bacterial communities and a large range of environmental descriptors (i.e. climate, soil and plant communities). Across 194 microbiota traits, a much higher fraction of among-population variance was explained by the host genetics than by ecology, with the plant neighborhood as the main ecological driver of microbiota variation. Importantly, the relative importance of host genetics and ecology expressed a phylogenetic signal at the family and genus level. In addition, the polygenic architecture of adaptation to bacterial communities was highly flexible between plant compartments and seasons. Relatedly, signatures of local adaptation were stronger on QTLs of the root microbiota in spring. Finally, we provide evidence that plant immunity, in particular the FLS2 gene, is a major source of adaptive genetic variation structuring bacterial assemblages in A. thaliana.

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Section: The Relative Importance Of Host Genetics and Ecology In Expl...supporting

confidence: 86%

“…These GWAS revealed a highly polygenic architecture, suggesting a control of natural microbiota assembly by an extensive number of Quantitative Trait Loci (QTLs) with a small effect. A similar result was recently obtained with traditional linkage mapping performed in barley (Escudero-Martinez et al 2022) and tomato (Oyserman et al 2022).…”

Section: Introductionsupporting

confidence: 88%

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

Roux

Frachon

Bartoli

2022

Preprint

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“…Our observations join other studies that performed comparative microbiome analysis of resistant and susceptible plants to soil-borne pathogens (Kwak et al 2018;Mendes et al 2018;Lazcano et al 2021). Collectively, these studies, including the present, suggest the importance of plant genetic traits in the assembly of the rhizosphere and root microbiomes that could mediate disease resistance and prevent pathogen invasion (Escudero-Martinez et al 2022;Oyserman et al 2022).…”

Section: Discussionsupporting

confidence: 85%

“…It is well known that the soil is the main microbial source of rhizosphere and root microbiomes (Bulgarelli et al 2012; Lundberg et al 2012). Hence, the capacity of plants to recruit beneficial microbial associates, that some could mediate disease resistance, is tightly related to their genetic traits (Escudero-Martinez et al 2022; Oyserman et al 2022). Here, we evaluated the response of the rhizosphere and root microbiomes of three strawberry cultivars (i.e.…”

Section: Introductionmentioning

confidence: 99%

Microbiome network connectivity and composition linked to disease resistance in strawberry plants

Hassani

Gonzalez

Hunter

et al. 2022

Preprint

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Plant recruit diverse microbial communities from the soil biota. Inter-microbial interactions and connectivity in the root microbiome could play essential roles in plant health by promoting resistance to soil-borne pathogens. Yet, understanding these interactions under field conditions is still scarce. Using a strawberry crop model, we characterized the prokaryotic and fungal communities in the rhizosphere and roots of three strawberry cultivars displaying varying resistance degrees to the soil-borne fungal pathogen Macrophomina phaseolina. We tested the hypothesis that resistant cultivars assemble distinct bacterial and fungal communities that foster microbial connectivity and mediate disease resistance. Our results show that the soil-borne pathogen, M. phaseolina, does not perturb the root microbiome of the strawberry cultivars. Microbiome comparative analysis indicated that the highly susceptible cultivar, Sweet Ann, assembles a distinct microbiome that shows reduced network connectivity, whereas more resistant cultivars were enriched in potential beneficial microbes and showed higher network connectivity. Collectively, these results suggest the role of plant genetic traits in the assembly of beneficial microbiome members. Our study reinforces the eminent role of the plant microbiome as trait of selection in breeding programs and stresses further understandings of the genetic and biological mechanisms that mediate microbiome assembly. Uncovering these mechanisms will be key for future plant breeding programs.

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“…There is also evidence that plant genetic makeup influences microbiome assembly in the rhizosphere. Oyserman et al [5] reported that specific tomato quantitative trait loci are associated with bacterial genes involved in the metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, and Deng et al [6] found that sorghum plant loci control heritability of the rhizosphere microbiome. Furthermore, the rhizosphere microbiome is influenced by soil type, as soil chemical and physical characteristics (e.g., soil pH, texture, and nutrient availability) shape microbiome assembly within the rhizosphere [7][8][9][10][11][12].…”

Section: Introductionmentioning

confidence: 99%

Nitrogen, manganese, iron, and carbon resource acquisition are potential functions of the wild rice Oryza rufipogon core rhizomicrobiome

et al. 2022

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Background The assembly of the rhizomicrobiome, i.e., the microbiome in the soil adhering to the root, is influenced by soil conditions. Here, we investigated the core rhizomicrobiome of a wild plant species transplanted to an identical soil type with small differences in chemical factors and the impact of these soil chemistry differences on the core microbiome after long-term cultivation. We sampled three natural reserve populations of wild rice (i.e., in situ) and three populations of transplanted in situ wild rice grown ex situ for more than 40 years to determine the core wild rice rhizomicrobiome. Results Generalized joint attribute modeling (GJAM) identified a total of 44 amplicon sequence variants (ASVs) composing the core wild rice rhizomicrobiome, including 35 bacterial ASVs belonging to the phyla Actinobacteria, Chloroflexi, Firmicutes, and Nitrospirae and 9 fungal ASVs belonging to the phyla Ascomycota, Basidiomycota, and Rozellomycota. Nine core bacterial ASVs belonging to the genera Haliangium, Anaeromyxobacter, Bradyrhizobium, and Bacillus were more abundant in the rhizosphere of ex situ wild rice than in the rhizosphere of in situ wild rice. The main ecological functions of the core microbiome were nitrogen fixation, manganese oxidation, aerobic chemoheterotrophy, chemoheterotrophy, and iron respiration, suggesting roles of the core rhizomicrobiome in improving nutrient resource acquisition for rice growth. The function of the core rhizosphere bacterial community was significantly (p < 0.05) shaped by electrical conductivity, total nitrogen, and available phosphorus present in the soil adhering to the roots. Conclusion We discovered that nitrogen, manganese, iron, and carbon resource acquisition are potential functions of the core rhizomicrobiome of the wild rice Oryza rufipogon. Our findings suggest that further potential utilization of the core rhizomicrobiome should consider the effects of soil properties on the abundances of different genera.

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Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

Cited by 6 publications

References 99 publications

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

Microbiome network connectivity and composition linked to disease resistance in strawberry plants

Nitrogen, manganese, iron, and carbon resource acquisition are potential functions of the wild rice Oryza rufipogon core rhizomicrobiome

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