A transcription factor ensemble orchestrates bundle sheath expression in rice
Abstract C4 photosynthesis has evolved in over sixty plant lineages and improves photosynthetic efficiency by ~50%. One unifying character of C4 plants is photosynthetic activation of a compartment such as the bundle sheath, but gene regulatory networks controlling this cell type are poorly understo...
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Nature Portfolio
2025-07-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-62087-0 |
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| author | Lei Hua Na Wang Susan Stanley Ruth M. Donald Satish Kumar Eeda Kumari Billakurthi Ana Rita Borba Julian M. Hibberd |
| author_facet | Lei Hua Na Wang Susan Stanley Ruth M. Donald Satish Kumar Eeda Kumari Billakurthi Ana Rita Borba Julian M. Hibberd |
| author_sort | Lei Hua |
| collection | DOAJ |
| description | Abstract C4 photosynthesis has evolved in over sixty plant lineages and improves photosynthetic efficiency by ~50%. One unifying character of C4 plants is photosynthetic activation of a compartment such as the bundle sheath, but gene regulatory networks controlling this cell type are poorly understood. In Arabidopsis, a bipartite MYC-MYB transcription factor module restricts gene expression to these cells, but in grasses the regulatory logic allowing bundle sheath gene expression has not been defined. Using the global staple and C3 crop rice, we find that the SULFITE REDUCTASE promoter is sufficient for strong bundle sheath expression. This promoter encodes an intricate cis-regulatory logic with multiple activators and repressors acting combinatorially. Within this landscape we identify a distal cis-regulatory module (CRM) activated by an ensemble of transcription factors from the WRKY, G2-like, MYB-related, DOF, IDD and bZIP families. This module is necessary and sufficient to pattern gene expression to the rice bundle sheath. Oligomerisation of the CRM and fusion to core promoters containing Y-patches allow activity to be increased 220-fold. This CRM generates bundle sheath-specific expression in Arabidopsis indicating deep conservation in function between monocotyledons and dicotyledons. In summary, we identify an ancient, short, and tuneable CRM patterning expression to the bundle sheath that we anticipate will be useful for engineering this cell type in various crop species. |
| format | Article |
| id | doaj-art-c5b65c643a35406aa2ed18e06e6bc81c |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-c5b65c643a35406aa2ed18e06e6bc81c2025-08-20T03:05:05ZengNature PortfolioNature Communications2041-17232025-07-0116111710.1038/s41467-025-62087-0A transcription factor ensemble orchestrates bundle sheath expression in riceLei Hua0Na Wang1Susan Stanley2Ruth M. Donald3Satish Kumar Eeda4Kumari Billakurthi5Ana Rita Borba6Julian M. Hibberd7Department of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeDepartment of Plant Sciences, University of CambridgeAbstract C4 photosynthesis has evolved in over sixty plant lineages and improves photosynthetic efficiency by ~50%. One unifying character of C4 plants is photosynthetic activation of a compartment such as the bundle sheath, but gene regulatory networks controlling this cell type are poorly understood. In Arabidopsis, a bipartite MYC-MYB transcription factor module restricts gene expression to these cells, but in grasses the regulatory logic allowing bundle sheath gene expression has not been defined. Using the global staple and C3 crop rice, we find that the SULFITE REDUCTASE promoter is sufficient for strong bundle sheath expression. This promoter encodes an intricate cis-regulatory logic with multiple activators and repressors acting combinatorially. Within this landscape we identify a distal cis-regulatory module (CRM) activated by an ensemble of transcription factors from the WRKY, G2-like, MYB-related, DOF, IDD and bZIP families. This module is necessary and sufficient to pattern gene expression to the rice bundle sheath. Oligomerisation of the CRM and fusion to core promoters containing Y-patches allow activity to be increased 220-fold. This CRM generates bundle sheath-specific expression in Arabidopsis indicating deep conservation in function between monocotyledons and dicotyledons. In summary, we identify an ancient, short, and tuneable CRM patterning expression to the bundle sheath that we anticipate will be useful for engineering this cell type in various crop species.https://doi.org/10.1038/s41467-025-62087-0 |
| spellingShingle | Lei Hua Na Wang Susan Stanley Ruth M. Donald Satish Kumar Eeda Kumari Billakurthi Ana Rita Borba Julian M. Hibberd A transcription factor ensemble orchestrates bundle sheath expression in rice Nature Communications |
| title | A transcription factor ensemble orchestrates bundle sheath expression in rice |
| title_full | A transcription factor ensemble orchestrates bundle sheath expression in rice |
| title_fullStr | A transcription factor ensemble orchestrates bundle sheath expression in rice |
| title_full_unstemmed | A transcription factor ensemble orchestrates bundle sheath expression in rice |
| title_short | A transcription factor ensemble orchestrates bundle sheath expression in rice |
| title_sort | transcription factor ensemble orchestrates bundle sheath expression in rice |
| url | https://doi.org/10.1038/s41467-025-62087-0 |
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