Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis
Plant root symbiosis with Arbuscular mycorrhizal (AM) fungi improves uptake of water and mineral nutrients, improving plant development under stressful conditions. Unraveling the unified transcriptomic signature of a successful colonization provides a better understanding of symbiosis. We developed...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2018-11-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2018.01550/full |
| _version_ | 1819053196702646272 |
|---|---|
| author | Manijeh Mohammadi-Dehcheshmeh Manijeh Mohammadi-Dehcheshmeh Ali Niazi Mansour Ebrahimi Mohammadreza Tahsili Zahra Nurollah Reyhaneh Ebrahimi Khaksefid Reyhaneh Ebrahimi Khaksefid Mahdi Ebrahimi Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie |
| author_facet | Manijeh Mohammadi-Dehcheshmeh Manijeh Mohammadi-Dehcheshmeh Ali Niazi Mansour Ebrahimi Mohammadreza Tahsili Zahra Nurollah Reyhaneh Ebrahimi Khaksefid Reyhaneh Ebrahimi Khaksefid Mahdi Ebrahimi Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie |
| author_sort | Manijeh Mohammadi-Dehcheshmeh |
| collection | DOAJ |
| description | Plant root symbiosis with Arbuscular mycorrhizal (AM) fungi improves uptake of water and mineral nutrients, improving plant development under stressful conditions. Unraveling the unified transcriptomic signature of a successful colonization provides a better understanding of symbiosis. We developed a framework for finding the transcriptomic signature of Arbuscular mycorrhiza colonization and its regulating transcription factors in roots of Medicago truncatula. Expression profiles of roots in response to AM species were collected from four separate studies and were combined by direct merging meta-analysis. Batch effect, the major concern in expression meta-analysis, was reduced by three normalization steps: Robust Multi-array Average algorithm, Z-standardization, and quartiling normalization. Then, expression profile of 33685 genes in 18 root samples of Medicago as numerical features, as well as study ID and Arbuscular mycorrhiza type as categorical features, were mined by seven models: RELIEF, UNCERTAINTY, GINI INDEX, Chi Squared, RULE, INFO GAIN, and INFO GAIN RATIO. In total, 73 genes selected by machine learning models were up-regulated in response to AM (Z-value difference > 0.5). Feature weighting models also documented that this signature is independent from study (batch) effect. The AM inoculation signature obtained was able to differentiate efficiently between AM inoculated and non-inoculated samples. The AP2 domain class transcription factor, GRAS family transcription factors, and cyclin-dependent kinase were among the highly expressed meta-genes identified in the signature. We found high correspondence between the AM colonization signature obtained in this study and independent RNA-seq experiments on AM colonization, validating the repeatability of the colonization signature. Promoter analysis of upregulated genes in the transcriptomic signature led to the key regulators of AM colonization, including the essential transcription factors for endosymbiosis establishment and development such as NF-YA factors. The approach developed in this study offers three distinct novel features: (I) it improves direct merging meta-analysis by integrating supervised machine learning models and normalization steps to reduce study-specific batch effects; (II) seven attribute weighting models assessed the suitability of each gene for the transcriptomic signature which contributes to robustness of the signature (III) the approach is justifiable, easy to apply, and useful in practice. Our integrative framework of meta-analysis, promoter analysis, and machine learning provides a foundation to reveal the transcriptomic signature and regulatory circuits governing Arbuscular mycorrhizal symbiosis and is transferable to the other biological settings. |
| first_indexed | 2024-12-21T12:31:53Z |
| format | Article |
| id | doaj.art-d9cb24661334447e926ac727717b0d40 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-21T12:31:53Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-d9cb24661334447e926ac727717b0d402022-12-21T19:04:01ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-11-01910.3389/fpls.2018.01550386326Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-AnalysisManijeh Mohammadi-Dehcheshmeh0Manijeh Mohammadi-Dehcheshmeh1Ali Niazi2Mansour Ebrahimi3Mohammadreza Tahsili4Zahra Nurollah5Reyhaneh Ebrahimi Khaksefid6Reyhaneh Ebrahimi Khaksefid7Mahdi Ebrahimi8Esmaeil Ebrahimie9Esmaeil Ebrahimie10Esmaeil Ebrahimie11Esmaeil Ebrahimie12Esmaeil Ebrahimie13Australian Centre for Antimicrobial Resistance Ecology, School of Animal and Veterinary Sciences, The University of Adelaide, Adelaide, SA, AustraliaInstitute of Biotechnology, Shiraz University, Shiraz, IranInstitute of Biotechnology, Shiraz University, Shiraz, IranDepartment of Biology, University of Qom, Qom, IranDepartment of Biology, University of Qom, Qom, IranDepartment of Biotechnology, Shahrekord University, Shahrekord, IranDepartment of Biotechnology, Shahrekord University, Shahrekord, IranSchool of Agriculture Food and Wine, Department of Plant Science, The University of Adelaide, Adelaide, SA, AustraliaMax-Planck-Institute for Informatics, Saarbrucken, GermanyAustralian Centre for Antimicrobial Resistance Ecology, School of Animal and Veterinary Sciences, The University of Adelaide, Adelaide, SA, AustraliaInstitute of Biotechnology, Shiraz University, Shiraz, IranAdelaide Medical School, The University of Adelaide, Adelaide, SA, AustraliaDivision of Information Technology, Engineering and the Environment, School of Information Technology and Mathematical Sciences, University of South Australia, Adelaide, SA, AustraliaFaculty of Science and Engineering, School of Biological Sciences, Flinders University, Adelaide, SA, AustraliaPlant root symbiosis with Arbuscular mycorrhizal (AM) fungi improves uptake of water and mineral nutrients, improving plant development under stressful conditions. Unraveling the unified transcriptomic signature of a successful colonization provides a better understanding of symbiosis. We developed a framework for finding the transcriptomic signature of Arbuscular mycorrhiza colonization and its regulating transcription factors in roots of Medicago truncatula. Expression profiles of roots in response to AM species were collected from four separate studies and were combined by direct merging meta-analysis. Batch effect, the major concern in expression meta-analysis, was reduced by three normalization steps: Robust Multi-array Average algorithm, Z-standardization, and quartiling normalization. Then, expression profile of 33685 genes in 18 root samples of Medicago as numerical features, as well as study ID and Arbuscular mycorrhiza type as categorical features, were mined by seven models: RELIEF, UNCERTAINTY, GINI INDEX, Chi Squared, RULE, INFO GAIN, and INFO GAIN RATIO. In total, 73 genes selected by machine learning models were up-regulated in response to AM (Z-value difference > 0.5). Feature weighting models also documented that this signature is independent from study (batch) effect. The AM inoculation signature obtained was able to differentiate efficiently between AM inoculated and non-inoculated samples. The AP2 domain class transcription factor, GRAS family transcription factors, and cyclin-dependent kinase were among the highly expressed meta-genes identified in the signature. We found high correspondence between the AM colonization signature obtained in this study and independent RNA-seq experiments on AM colonization, validating the repeatability of the colonization signature. Promoter analysis of upregulated genes in the transcriptomic signature led to the key regulators of AM colonization, including the essential transcription factors for endosymbiosis establishment and development such as NF-YA factors. The approach developed in this study offers three distinct novel features: (I) it improves direct merging meta-analysis by integrating supervised machine learning models and normalization steps to reduce study-specific batch effects; (II) seven attribute weighting models assessed the suitability of each gene for the transcriptomic signature which contributes to robustness of the signature (III) the approach is justifiable, easy to apply, and useful in practice. Our integrative framework of meta-analysis, promoter analysis, and machine learning provides a foundation to reveal the transcriptomic signature and regulatory circuits governing Arbuscular mycorrhizal symbiosis and is transferable to the other biological settings.https://www.frontiersin.org/article/10.3389/fpls.2018.01550/fullmachine learningmeta-analysisregulatory mechanismsymbiosissystems biology |
| spellingShingle | Manijeh Mohammadi-Dehcheshmeh Manijeh Mohammadi-Dehcheshmeh Ali Niazi Mansour Ebrahimi Mohammadreza Tahsili Zahra Nurollah Reyhaneh Ebrahimi Khaksefid Reyhaneh Ebrahimi Khaksefid Mahdi Ebrahimi Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Esmaeil Ebrahimie Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis Frontiers in Plant Science machine learning meta-analysis regulatory mechanism symbiosis systems biology |
| title | Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis |
| title_full | Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis |
| title_fullStr | Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis |
| title_full_unstemmed | Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis |
| title_short | Unified Transcriptomic Signature of Arbuscular Mycorrhiza Colonization in Roots of Medicago truncatula by Integration of Machine Learning, Promoter Analysis, and Direct Merging Meta-Analysis |
| title_sort | unified transcriptomic signature of arbuscular mycorrhiza colonization in roots of medicago truncatula by integration of machine learning promoter analysis and direct merging meta analysis |
| topic | machine learning meta-analysis regulatory mechanism symbiosis systems biology |
| url | https://www.frontiersin.org/article/10.3389/fpls.2018.01550/full |
| work_keys_str_mv | AT manijehmohammadidehcheshmeh unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT manijehmohammadidehcheshmeh unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT aliniazi unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT mansourebrahimi unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT mohammadrezatahsili unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT zahranurollah unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT reyhanehebrahimikhaksefid unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT reyhanehebrahimikhaksefid unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT mahdiebrahimi unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT esmaeilebrahimie unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT esmaeilebrahimie unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT esmaeilebrahimie unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT esmaeilebrahimie unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis AT esmaeilebrahimie unifiedtranscriptomicsignatureofarbuscularmycorrhizacolonizationinrootsofmedicagotruncatulabyintegrationofmachinelearningpromoteranalysisanddirectmergingmetaanalysis |