Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots
ABSTRACT While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium ox...
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| Format: | Artikel |
| Sprache: | English |
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American Society for Microbiology
2022-08-01
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| Schriftenreihe: | Microbiology Spectrum |
| Schlagworte: | |
| Online Zugang: | https://journals.asm.org/doi/10.1128/spectrum.01226-22 |
| _version_ | 1828358199208574976 |
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| author | Enoch Narh Kudjordjie Kourosh Hooshmand Rumakanta Sapkota Behrooz Darbani Inge S. Fomsgaard Mogens Nicolaisen |
| author_facet | Enoch Narh Kudjordjie Kourosh Hooshmand Rumakanta Sapkota Behrooz Darbani Inge S. Fomsgaard Mogens Nicolaisen |
| author_sort | Enoch Narh Kudjordjie |
| collection | DOAJ |
| description | ABSTRACT While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium oxysporum f.sp. mathioli (FOM) inoculation, Landsberg erecta (Ler-0) being susceptible and Col-0 being resistant against FOM. By using bacterial and fungal amplicon sequencing and targeted metabolite analysis, we observed highly dynamic microbiome and metabolome profiles across FOM host progression, while being markedly different between FOM-inoculated and noninoculated Col-0 and Ler-0. Co-occurrence network analysis revealed more robust microbial networks in the resistant Col-0 compared to Ler-0 during FOM infection. Correlation analysis revealed distinct metabolite-OTU correlations in Ler-0 compared with Col-0 which could possibly be explained by missense variants of the Rfo3 and Rlp2 genes in Ler-0. Remarkably, we observed positive correlations in Ler-0 between most of the analyzed metabolites and the bacterial phyla Proteobacteria, Bacteroidetes, Planctomycetes, Acidobacteria, and Verrucomicrobia, and negative correlations with Actinobacteria, Firmicutes, and Chloroflexi. The glucosinolates 4-methyoxyglucobrassicin, glucoerucin and indole-3 carbinol, but also phenolic compounds were strongly correlating with the relative abundances of indicator and hub OTUs and thus could be active in structuring the A. thaliana root-associated microbiome. Our results highlight interactive effects of host plant defense and root-associated microbiota on Fusarium infection and progression. Our findings provide significant insights into plant interomic dynamics during pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control. IMPORTANCE Plant health and fitness are determined by plant-microbe interactions which are guided by host-synthesized metabolites. To understand the orchestration of this interaction, we analyzed the distinct interomic dynamics in resistant and susceptible Arabidopsis ecotypes across different time points after infection with Fusarium oxysporum (FOM). Our results revealed distinct microbial profiles and network resilience during FOM infection in the resistant Col-0 compared with the susceptible Ler-0 and further pinpointed specific microbe-metabolite associations in the Arabidopsis microbiome. These findings provide significant insights into plant interomics dynamics that are likely affecting fungal pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control. |
| first_indexed | 2024-04-14T03:26:19Z |
| format | Article |
| id | doaj.art-775c9d0db1e94056ac7d68cadffaa2e5 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-14T03:26:19Z |
| publishDate | 2022-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-775c9d0db1e94056ac7d68cadffaa2e52022-12-22T02:15:10ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.01226-22Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana RootsEnoch Narh Kudjordjie0Kourosh Hooshmand1Rumakanta Sapkota2Behrooz Darbani3Inge S. Fomsgaard4Mogens Nicolaisen5Department of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkDepartment of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkDepartment of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkDepartment of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkDepartment of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkDepartment of Agroecology, Faculty of Technical Sciences, Aarhus University, Slagelse, DenmarkABSTRACT While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium oxysporum f.sp. mathioli (FOM) inoculation, Landsberg erecta (Ler-0) being susceptible and Col-0 being resistant against FOM. By using bacterial and fungal amplicon sequencing and targeted metabolite analysis, we observed highly dynamic microbiome and metabolome profiles across FOM host progression, while being markedly different between FOM-inoculated and noninoculated Col-0 and Ler-0. Co-occurrence network analysis revealed more robust microbial networks in the resistant Col-0 compared to Ler-0 during FOM infection. Correlation analysis revealed distinct metabolite-OTU correlations in Ler-0 compared with Col-0 which could possibly be explained by missense variants of the Rfo3 and Rlp2 genes in Ler-0. Remarkably, we observed positive correlations in Ler-0 between most of the analyzed metabolites and the bacterial phyla Proteobacteria, Bacteroidetes, Planctomycetes, Acidobacteria, and Verrucomicrobia, and negative correlations with Actinobacteria, Firmicutes, and Chloroflexi. The glucosinolates 4-methyoxyglucobrassicin, glucoerucin and indole-3 carbinol, but also phenolic compounds were strongly correlating with the relative abundances of indicator and hub OTUs and thus could be active in structuring the A. thaliana root-associated microbiome. Our results highlight interactive effects of host plant defense and root-associated microbiota on Fusarium infection and progression. Our findings provide significant insights into plant interomic dynamics during pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control. IMPORTANCE Plant health and fitness are determined by plant-microbe interactions which are guided by host-synthesized metabolites. To understand the orchestration of this interaction, we analyzed the distinct interomic dynamics in resistant and susceptible Arabidopsis ecotypes across different time points after infection with Fusarium oxysporum (FOM). Our results revealed distinct microbial profiles and network resilience during FOM infection in the resistant Col-0 compared with the susceptible Ler-0 and further pinpointed specific microbe-metabolite associations in the Arabidopsis microbiome. These findings provide significant insights into plant interomics dynamics that are likely affecting fungal pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control.https://journals.asm.org/doi/10.1128/spectrum.01226-22plant pathogenroot microbiomeglucosinolatesphenylpropanoidsphytohormonesmicrobial co-occurrence networks |
| spellingShingle | Enoch Narh Kudjordjie Kourosh Hooshmand Rumakanta Sapkota Behrooz Darbani Inge S. Fomsgaard Mogens Nicolaisen Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots Microbiology Spectrum plant pathogen root microbiome glucosinolates phenylpropanoids phytohormones microbial co-occurrence networks |
| title | Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots |
| title_full | Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots |
| title_fullStr | Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots |
| title_full_unstemmed | Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots |
| title_short | Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots |
| title_sort | fusarium oxysporum disrupts microbiome metabolome networks in arabidopsis thaliana roots |
| topic | plant pathogen root microbiome glucosinolates phenylpropanoids phytohormones microbial co-occurrence networks |
| url | https://journals.asm.org/doi/10.1128/spectrum.01226-22 |
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