Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice
Nitrogen (N) and Water (W) - two resources critical for crop productivity – are becoming increasingly limited in soils globally. To address this issue, we aim to uncover the gene regulatory networks (GRNs) that regulate nitrogen use efficiency (NUE) - as a function of water availability - in Oryza s...
| Autores principales: | , , , , , , , , , |
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| Formato: | Journal Article |
| Lenguaje: | Inglés |
| Publicado: |
Frontiers Media
2022
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| Materias: | |
| Acceso en línea: | https://hdl.handle.net/10568/127525 |
| _version_ | 1855514556568174592 |
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| author | Shanks, Carly M. Huang, Ji Cheng, Chia-Yi Shih, Hung-Jui S. Brooks, Matthew D. Álvarez, José M. Araus, Viviana Swift, Joseph Henry, Amelia Coruzzi, Gloria M. |
| author_browse | Araus, Viviana Brooks, Matthew D. Cheng, Chia-Yi Coruzzi, Gloria M. Henry, Amelia Huang, Ji Shanks, Carly M. Shih, Hung-Jui S. Swift, Joseph Álvarez, José M. |
| author_facet | Shanks, Carly M. Huang, Ji Cheng, Chia-Yi Shih, Hung-Jui S. Brooks, Matthew D. Álvarez, José M. Araus, Viviana Swift, Joseph Henry, Amelia Coruzzi, Gloria M. |
| author_sort | Shanks, Carly M. |
| collection | Repository of Agricultural Research Outputs (CGSpace) |
| description | Nitrogen (N) and Water (W) - two resources critical for crop productivity – are becoming increasingly limited in soils globally. To address this issue, we aim to uncover the gene regulatory networks (GRNs) that regulate nitrogen use efficiency (NUE) - as a function of water availability - in Oryza sativa, a staple for 3.5 billion people. In this study, we infer and validate GRNs that correlate with rice NUE phenotypes affected by N-by-W availability in the field. We did this by exploiting RNA-seq and crop phenotype data from 19 rice varieties grown in a 2x2 N-by-W matrix in the field. First, to identify gene-to-NUE field phenotypes, we analyzed these datasets using weighted gene co-expression network analysis (WGCNA). This identified two network modules ("skyblue" & "grey60") highly correlated with NUE grain yield (NUEg). Next, we focused on 90 TFs contained in these two NUEg modules and predicted their genome-wide targets using the N-and/or-W response datasets using a random forest network inference approach (GENIE3). Next, to validate the GENIE3 TF→target gene predictions, we performed Precision/Recall Analysis (AUPR) using nine datasets for three TFs validated in planta. This analysis sets a precision threshold of 0.31, used to "prune" the GENIE3 network for high-confidence TF→target gene edges, comprising 88 TFs and 5,716 N-and/or-W response genes. Next, we ranked these 88 TFs based on their significant influence on NUEg target genes responsive to N and/or W signaling. This resulted in a list of 18 prioritized TFs that regulate 551 NUEg target genes responsive to N and/or W signals. We validated the direct regulated targets of two of these candidate NUEg TFs in a plant cell-based TF assay called TARGET, for which we also had in planta data for comparison. Gene ontology analysis revealed that 6/18 NUEg TFs - OsbZIP23 (LOC_Os02g52780), Oshox22 (LOC_Os04g45810), LOB39 (LOC_Os03g41330), Oshox13 (LOC_Os03g08960), LOC_Os11g38870, and LOC_Os06g14670 - regulate genes annotated for N and/or W signaling. Our results show that OsbZIP23 and Oshox22, known regulators of drought tolerance, also coordinate W-responses with NUEg. This validated network can aid in developing/breeding rice with improved yield on marginal, low N-input, drought-prone soils. |
| format | Journal Article |
| id | CGSpace127525 |
| institution | CGIAR Consortium |
| language | Inglés |
| publishDate | 2022 |
| publishDateRange | 2022 |
| publishDateSort | 2022 |
| publisher | Frontiers Media |
| publisherStr | Frontiers Media |
| record_format | dspace |
| spelling | CGSpace1275252025-12-08T10:29:22Z Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice Shanks, Carly M. Huang, Ji Cheng, Chia-Yi Shih, Hung-Jui S. Brooks, Matthew D. Álvarez, José M. Araus, Viviana Swift, Joseph Henry, Amelia Coruzzi, Gloria M. rice drought nitrogen genes Nitrogen (N) and Water (W) - two resources critical for crop productivity – are becoming increasingly limited in soils globally. To address this issue, we aim to uncover the gene regulatory networks (GRNs) that regulate nitrogen use efficiency (NUE) - as a function of water availability - in Oryza sativa, a staple for 3.5 billion people. In this study, we infer and validate GRNs that correlate with rice NUE phenotypes affected by N-by-W availability in the field. We did this by exploiting RNA-seq and crop phenotype data from 19 rice varieties grown in a 2x2 N-by-W matrix in the field. First, to identify gene-to-NUE field phenotypes, we analyzed these datasets using weighted gene co-expression network analysis (WGCNA). This identified two network modules ("skyblue" & "grey60") highly correlated with NUE grain yield (NUEg). Next, we focused on 90 TFs contained in these two NUEg modules and predicted their genome-wide targets using the N-and/or-W response datasets using a random forest network inference approach (GENIE3). Next, to validate the GENIE3 TF→target gene predictions, we performed Precision/Recall Analysis (AUPR) using nine datasets for three TFs validated in planta. This analysis sets a precision threshold of 0.31, used to "prune" the GENIE3 network for high-confidence TF→target gene edges, comprising 88 TFs and 5,716 N-and/or-W response genes. Next, we ranked these 88 TFs based on their significant influence on NUEg target genes responsive to N and/or W signaling. This resulted in a list of 18 prioritized TFs that regulate 551 NUEg target genes responsive to N and/or W signals. We validated the direct regulated targets of two of these candidate NUEg TFs in a plant cell-based TF assay called TARGET, for which we also had in planta data for comparison. Gene ontology analysis revealed that 6/18 NUEg TFs - OsbZIP23 (LOC_Os02g52780), Oshox22 (LOC_Os04g45810), LOB39 (LOC_Os03g41330), Oshox13 (LOC_Os03g08960), LOC_Os11g38870, and LOC_Os06g14670 - regulate genes annotated for N and/or W signaling. Our results show that OsbZIP23 and Oshox22, known regulators of drought tolerance, also coordinate W-responses with NUEg. This validated network can aid in developing/breeding rice with improved yield on marginal, low N-input, drought-prone soils. 2022-11-25 2023-01-19T11:11:55Z 2023-01-19T11:11:55Z Journal Article https://hdl.handle.net/10568/127525 en Open Access application/pdf Frontiers Media Shanks, C.M., Huang, J., Cheng, C.-Y., Shih, H.-J.S., Brooks, M.D., Alvarez, J.M., Araus, V., Swift, J., Henry, A. and Coruzzi, G.M. 2022. Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice. Frontiers in Plant Science 13:1006044. |
| spellingShingle | rice drought nitrogen genes Shanks, Carly M. Huang, Ji Cheng, Chia-Yi Shih, Hung-Jui S. Brooks, Matthew D. Álvarez, José M. Araus, Viviana Swift, Joseph Henry, Amelia Coruzzi, Gloria M. Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title | Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title_full | Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title_fullStr | Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title_full_unstemmed | Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title_short | Validation of a high-confidence regulatory network for gene-to-NUE phenotype in field-grown rice |
| title_sort | validation of a high confidence regulatory network for gene to nue phenotype in field grown rice |
| topic | rice drought nitrogen genes |
| url | https://hdl.handle.net/10568/127525 |
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