A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis
Abstract Background Beneficial associations between plants and microbes are widespread in nature and have been studied extensively in the microbial-dominant environment of the rhizosphere. Such associations are highly advantageous for the organisms involved, benefiting soil microbes by providing the...
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| Format: | Article |
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BMC
2021-08-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-021-01104-2 |
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| author | Ena Šečić Silvia Zanini Daniel Wibberg Lukas Jelonek Tobias Busche Jörn Kalinowski Sabrine Nasfi Jennifer Thielmann Jafargholi Imani Jens Steinbrenner Karl-Heinz Kogel |
| author_facet | Ena Šečić Silvia Zanini Daniel Wibberg Lukas Jelonek Tobias Busche Jörn Kalinowski Sabrine Nasfi Jennifer Thielmann Jafargholi Imani Jens Steinbrenner Karl-Heinz Kogel |
| author_sort | Ena Šečić |
| collection | DOAJ |
| description | Abstract Background Beneficial associations between plants and microbes are widespread in nature and have been studied extensively in the microbial-dominant environment of the rhizosphere. Such associations are highly advantageous for the organisms involved, benefiting soil microbes by providing them access to plant metabolites, while plant growth and development are enhanced through the promotion of nutrient uptake and/or protection against (a)biotic stresses. While the establishment and maintenance of mutualistic associations have been shown to require genetic and epigenetic reprogramming, as well as an exchange of effector molecules between microbes and plants, whether short RNAs are able to effect such changes is currently unknown. Here, we established an interaction between the model grass species Brachypodium distachyon (Bd, Pooideae) and the beneficial fungal root endophyte Serendipita indica (Si, syn. Piriformospora indica, Sebacinales) to elucidate RNA interference-based regulatory changes in gene expression and small (s)RNA profiles that occurred during establishment of a Sebacinalean symbiosis. Results Colonization of Bd roots with Si resulted in higher grain yield, confirming the mutualistic character of this interaction. Resequencing of the Si genome using the Oxford Nanopore technique, followed by de novo assembly yielded in 57 contigs and 9441 predicted genes, including putative members of several families involved in sRNA production. Transcriptome analysis at an early stage of the mutualistic interaction identified 2963 differentially expressed genes (DEG) in Si and 317 in Bd line 21-3. The fungal DEGs were largely associated with carbohydrate metabolism, cell wall degradation, and nutrient uptake, while plant DEGs indicated modulation of (a)biotic stress responses and defense pathways. Additionally, 10% of the upregulated fungal DEGs encode candidate protein effectors, including six DELD proteins typical for Sebacinales. Analysis of the global changes in the sRNA profiles of both associated organisms revealed several putative endogenous plant sRNAs expressed during colonization belonging to known micro (mi)RNA families involved in growth and developmental regulation. Among Bd- and Si-generated sRNAs with putative functions in the interacting organism, we identified transcripts for proteins involved in circadian clock and flowering regulation as well as immunity as potential targets of fungal sRNAs, reflecting the beneficial activity of Si. Conclusions We detected beneficial effects of Si colonization on Bd growth and development, and established a novel plant-mutualist interaction model between these organisms. Together, the changes in gene expression and identification of interaction-induced sRNAs in both organisms support sRNA-based regulation of defense responses and plant development in Bd, as well as nutrient acquisition and cell growth in Si. Our data suggests that a Sebacinalean symbiosis involves reciprocal sRNA targeting of genes during the interaction. |
| first_indexed | 2024-12-22T10:01:38Z |
| format | Article |
| id | doaj.art-dc4384de7dae4b2a92b31d8ecd78b14f |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-22T10:01:38Z |
| publishDate | 2021-08-01 |
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| series | BMC Biology |
| spelling | doaj.art-dc4384de7dae4b2a92b31d8ecd78b14f2022-12-21T18:30:07ZengBMCBMC Biology1741-70072021-08-0119112210.1186/s12915-021-01104-2A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosisEna Šečić0Silvia Zanini1Daniel Wibberg2Lukas Jelonek3Tobias Busche4Jörn Kalinowski5Sabrine Nasfi6Jennifer Thielmann7Jafargholi Imani8Jens Steinbrenner9Karl-Heinz Kogel10Institute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityCenter for Biotechnology - CeBiTec, Bielefeld UniversityInstitute of Bioinformatics and Systems Biology, Justus Liebig UniversityCenter for Biotechnology - CeBiTec, Bielefeld UniversityCenter for Biotechnology - CeBiTec, Bielefeld UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityInstitute of Phytopathology, Centre for BioSystems, Land Use and Nutrition, Justus Liebig UniversityAbstract Background Beneficial associations between plants and microbes are widespread in nature and have been studied extensively in the microbial-dominant environment of the rhizosphere. Such associations are highly advantageous for the organisms involved, benefiting soil microbes by providing them access to plant metabolites, while plant growth and development are enhanced through the promotion of nutrient uptake and/or protection against (a)biotic stresses. While the establishment and maintenance of mutualistic associations have been shown to require genetic and epigenetic reprogramming, as well as an exchange of effector molecules between microbes and plants, whether short RNAs are able to effect such changes is currently unknown. Here, we established an interaction between the model grass species Brachypodium distachyon (Bd, Pooideae) and the beneficial fungal root endophyte Serendipita indica (Si, syn. Piriformospora indica, Sebacinales) to elucidate RNA interference-based regulatory changes in gene expression and small (s)RNA profiles that occurred during establishment of a Sebacinalean symbiosis. Results Colonization of Bd roots with Si resulted in higher grain yield, confirming the mutualistic character of this interaction. Resequencing of the Si genome using the Oxford Nanopore technique, followed by de novo assembly yielded in 57 contigs and 9441 predicted genes, including putative members of several families involved in sRNA production. Transcriptome analysis at an early stage of the mutualistic interaction identified 2963 differentially expressed genes (DEG) in Si and 317 in Bd line 21-3. The fungal DEGs were largely associated with carbohydrate metabolism, cell wall degradation, and nutrient uptake, while plant DEGs indicated modulation of (a)biotic stress responses and defense pathways. Additionally, 10% of the upregulated fungal DEGs encode candidate protein effectors, including six DELD proteins typical for Sebacinales. Analysis of the global changes in the sRNA profiles of both associated organisms revealed several putative endogenous plant sRNAs expressed during colonization belonging to known micro (mi)RNA families involved in growth and developmental regulation. Among Bd- and Si-generated sRNAs with putative functions in the interacting organism, we identified transcripts for proteins involved in circadian clock and flowering regulation as well as immunity as potential targets of fungal sRNAs, reflecting the beneficial activity of Si. Conclusions We detected beneficial effects of Si colonization on Bd growth and development, and established a novel plant-mutualist interaction model between these organisms. Together, the changes in gene expression and identification of interaction-induced sRNAs in both organisms support sRNA-based regulation of defense responses and plant development in Bd, as well as nutrient acquisition and cell growth in Si. Our data suggests that a Sebacinalean symbiosis involves reciprocal sRNA targeting of genes during the interaction.https://doi.org/10.1186/s12915-021-01104-2Brachypodium distachyonGenome sequencingSebacinalean symbiosisSerendipita indicaSmall RNAs |
| spellingShingle | Ena Šečić Silvia Zanini Daniel Wibberg Lukas Jelonek Tobias Busche Jörn Kalinowski Sabrine Nasfi Jennifer Thielmann Jafargholi Imani Jens Steinbrenner Karl-Heinz Kogel A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis BMC Biology Brachypodium distachyon Genome sequencing Sebacinalean symbiosis Serendipita indica Small RNAs |
| title | A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis |
| title_full | A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis |
| title_fullStr | A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis |
| title_full_unstemmed | A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis |
| title_short | A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis |
| title_sort | novel plant fungal association reveals fundamental srna and gene expression reprogramming at the onset of symbiosis |
| topic | Brachypodium distachyon Genome sequencing Sebacinalean symbiosis Serendipita indica Small RNAs |
| url | https://doi.org/10.1186/s12915-021-01104-2 |
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