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Francesco Spinelli
University of Bologna: Universita di Bologna
Corresponding Author
ORCiD: https://orcid.org/0000-0003-3870-1227
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background
Cultivated strawberry (Fragaria × ananassa Duch., fam. Rosaceae) is an important fruit crop, greatly appreciated for its aroma and nutraceutical properties. Niche-specific characterisation of plant microbiome, from rhizosphere to aboveground plant organs, is crucial to understand the influence of structure and function of the microbial communities on plant phenotype, performances and disease resistance. Strawberry cultivation is challenged by a large variety of pathogens, which cause substantial economic losses and require the frequent application of pesticides. Biological control is a promising and safer alternative to the use of xenobiotic pesticides. Biological control agents isolated from the microbiome of the host plant may have a superior efficacy in comparison to non-indigenous microbial inoculants. Therefore, the characterization of the native microbiome along different plant compartments is a key step for the successful microbial manipulation in farmlands.
Results
Here, we provide the first comprehensive description of the soil, rhizosphere, root and aerial parts microbiome of three commercially important strawberry cultivars (‘Darselect’, ‘Elsanta’ and ‘Monterey’) under cultural conditions. The fungal and bacterial microbiomes were functionally characterised to investigate their influence on plant disease tolerance, plant mineral nutrient content and fruit quality. The core microbiome included 24 bacteria and 15 fungal operative taxon units which were present in all compartments and plant genotypes. However, both plant organ and genotype had a significant role in assembling the microbial communities. The microbial community assemblage across different soil and plant compartments significantly correlated with disease resistance, mineral nutrient content in the plant and with fruit quality parameters. Interestingly, only the disease tolerant genotype ‘Monterey’ was able to recruit Pseudomonas fluorescens in all plant organs and to establish symbiosis with the arbuscular mycorrhiza Rhizophagus irregularis. These two species include several strains acting as pathogen biocontrol agents, plant growth promoters and plant defence inducers.
Conclusions
Altogether, our study provides the first comprehensive view of strawberry microbiome in relation to plant genotype, health and nutritional status and fruit quality parameters, shedding light on potential practical applications to increase the sustainability of crop production.
Keywords
Fragaria x ananassa, Next Generation Sequencing, biological control, metagenome, plant growth promoting bacteria, arbuscular mycorrhiza, rhizosphere, phyllosphere, Pseudomonas fluorescens, Rhizophagus irregularis
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This is a list of supplementary files associated with this preprint. Click to download.
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS11.docx
- TableS11.docx
- TableS11.docx
- TableS10.docx
- TableS10.docx
- TableS10.docx
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
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Research
Francesco Spinelli
University of Bologna: Universita di Bologna
Corresponding Author
ORCiD: https://orcid.org/0000-0003-3870-1227
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Background
Cultivated strawberry (Fragaria × ananassa Duch., fam. Rosaceae) is an important fruit crop, greatly appreciated for its aroma and nutraceutical properties. Niche-specific characterisation of plant microbiome, from rhizosphere to aboveground plant organs, is crucial to understand the influence of structure and function of the microbial communities on plant phenotype, performances and disease resistance. Strawberry cultivation is challenged by a large variety of pathogens, which cause substantial economic losses and require the frequent application of pesticides. Biological control is a promising and safer alternative to the use of xenobiotic pesticides. Biological control agents isolated from the microbiome of the host plant may have a superior efficacy in comparison to non-indigenous microbial inoculants. Therefore, the characterization of the native microbiome along different plant compartments is a key step for the successful microbial manipulation in farmlands.
Results
Here, we provide the first comprehensive description of the soil, rhizosphere, root and aerial parts microbiome of three commercially important strawberry cultivars (‘Darselect’, ‘Elsanta’ and ‘Monterey’) under cultural conditions. The fungal and bacterial microbiomes were functionally characterised to investigate their influence on plant disease tolerance, plant mineral nutrient content and fruit quality. The core microbiome included 24 bacteria and 15 fungal operative taxon units which were present in all compartments and plant genotypes. However, both plant organ and genotype had a significant role in assembling the microbial communities. The microbial community assemblage across different soil and plant compartments significantly correlated with disease resistance, mineral nutrient content in the plant and with fruit quality parameters. Interestingly, only the disease tolerant genotype ‘Monterey’ was able to recruit Pseudomonas fluorescens in all plant organs and to establish symbiosis with the arbuscular mycorrhiza Rhizophagus irregularis. These two species include several strains acting as pathogen biocontrol agents, plant growth promoters and plant defence inducers.
Conclusions
Altogether, our study provides the first comprehensive view of strawberry microbiome in relation to plant genotype, health and nutritional status and fruit quality parameters, shedding light on potential practical applications to increase the sustainability of crop production.
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This is a list of supplementary files associated with this preprint. Click to download.
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS1.tif
Additional file 1 - Fig S1.tif - Figure S1. (A) Overall community composition and richness of bacteria and fungi based on relative abundance data. Rarefaction curves for (B) bacteria and (C) fungi are shown. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS2.tiff
Additional file 2 - Fig S2.tiff - Figure S2. Chao1 richness estimate for (A) bacteria and (B) fungi in different plant-soil compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- figS3.tif
Additional file 3 - figS3.tif - Figure S3. Nonmetric multidimensional scaling (NMDS) plot showing beneficial community composition similarity of beneficial bacteria (A) and fungi (B) among different soil and plant compartments and genotypes. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS4.tif
Additional file 4 - FigS4.tif - Figure S4. Detection of nifH gene in different plant-soil compartments of the three strawberry genotypes analysed by Polymerase Chain Reaction. Intensity of bands displayed after agarose gel electrophoresis is reported. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- FigS5.tiff
Additional file 5 - FigS5.tiff - Figure S5. Gel electrophoresis of PCR amplified products using species-specific primers for Pseudomonas fluorescens. Colonization of Monterey genotype has been investigated in bulk soil, rhizosphere, internal tissue of roots and above ground plant compartments; 4 replicates for each organ. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- figS6.pdf
Additional file 6 - figS6.pdf - Figure S6. Boxplots visualizing results for viable bacterial and fungal cells (colony-forming unit, CFU) present in plant and soil compartments of strawberry cultivars ‘Darselect’, ‘Elsanta’, ‘Monterey’. - Figure
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS1.docx
Additional file 7 - Table S1. Effect of genotype, soil and plant compartment on community composition of strawberry microbiome based on relative abundance data and Bray-Curtis distance measure. Nd = not determined; Significant P values are highlighted in bold. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS2.docx
Additional file 8 - Table S2. Bacterial (mainly Micrococcales) and fungal (mainly Ascomycota) OTUs detected in all 3 strawberry genotypes and in all plant-soil compartments. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS3.docx
Additional file 9 - Table S3. Number of OTUs belonging to particular bacterial or fungal functions assigned based on FAPROTAX and FUNguild, respectively. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS4.docx
Additional file 10 - Table S4. Identification of potential bacterial beneficial functions based on literature research. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS5.docx
Additional file 11 - Table S5. List of fungal OTUs identified at the species level, for which biological control or plant growth promoting activities have been described in literature. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS6.docx
Additional file 12 - Table S6. Nitrogen fixing bacterial genera detected in cultivated strawberry, wild strawberries and legume plants. - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS7.docx
Additional file 13 - Table S7. Symptoms rate of ‘Monterey’, ‘Elsanta’ and ‘Darselect’ cvs under cultural conditions., based on visual scale (0=no symptoms, 5=severe symptoms). - Table
- TableS11.docx
- TableS11.docx
- TableS11.docx
- TableS10.docx
- TableS10.docx
- TableS10.docx
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS8.docx
Additional file 14 - Table S8. Potential strawberry fungal pathogens (Unite Species Hypotheses). - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
- TableS9.docx
Additional file 15 - Table S9. Mineral composition of the fertigating solution of strawberry plants in this work. - Table
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