Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone
Plant cell wall composition is important for regulating growth rates, especially in roots. However, neither analyses of cell wall composition nor transcriptomes on their own can comprehensively reveal which genes and processes are mediating growth and cell elongation rates. This study reveals the be...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
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Frontiers Media
2015
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| Online Access: | https://eprints.nottingham.ac.uk/41647/ |
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| author | Wilson, Michael H. Holman, Tara J. Sørensen, Iben Cancho-Sanchez, Ester Wells, Darren M. Swarup, Ranjan Knox, J. Paul Willats, William G.T. Ubeda-Tomás, Susana Holdsworth, Michael J. Bennett, Malcolm J. Vissenberg, Kris Hodgman, T. Charlie |
| author_facet | Wilson, Michael H. Holman, Tara J. Sørensen, Iben Cancho-Sanchez, Ester Wells, Darren M. Swarup, Ranjan Knox, J. Paul Willats, William G.T. Ubeda-Tomás, Susana Holdsworth, Michael J. Bennett, Malcolm J. Vissenberg, Kris Hodgman, T. Charlie |
| author_sort | Wilson, Michael H. |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | Plant cell wall composition is important for regulating growth rates, especially in roots. However, neither analyses of cell wall composition nor transcriptomes on their own can comprehensively reveal which genes and processes are mediating growth and cell elongation rates. This study reveals the benefits of carrying out multiple analyses in combination. Sections of roots from five anatomically and functionally defined zones in Arabidopsis thaliana were prepared and divided into three biological replicates. We used glycan microarrays and antibodies to identify the major classes of glycans and glycoproteins present in the cell walls of these sections, and identified the expected decrease in pectin and increase in xylan from the meristematic zone (MS), through the rapid and late elongation zones (REZ, LEZ) to the maturation zone and the rest of the root, including the emerging lateral roots. Other compositional changes included extensin and xyloglucan levels peaking in the REZ and increasing levels of arabinogalactan-proteins (AGP) epitopes from the MS to the LEZ, which remained high through the subsequent mature zones. Immuno-staining using the same antibodies identified the tissue and (sub)cellular localization of many epitopes. Extensins were localized in epidermal and cortex cell walls, while AGP glycans were specific to different tissues from root-hair cells to the stele. The transcriptome analysis found several gene families peaking in the REZ. These included a large family of peroxidases (which produce the reactive oxygen species (ROS) needed for cell expansion), and three xyloglucan endo-transglycosylase/hydrolase genes (XTH17, XTH18, and XTH19). The significance of the latter may be related to a role in breaking and re-joining xyloglucan cross-bridges between cellulose microfibrils, a process which is required for wall expansion. Knockdowns of these XTHs resulted in shorter root lengths, confirming a role of the corresponding proteins in root extension growth. |
| first_indexed | 2025-11-14T19:46:09Z |
| format | Article |
| id | nottingham-41647 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| last_indexed | 2025-11-14T19:46:09Z |
| publishDate | 2015 |
| publisher | Frontiers Media |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-416472020-05-04T17:02:24Z https://eprints.nottingham.ac.uk/41647/ Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone Wilson, Michael H. Holman, Tara J. Sørensen, Iben Cancho-Sanchez, Ester Wells, Darren M. Swarup, Ranjan Knox, J. Paul Willats, William G.T. Ubeda-Tomás, Susana Holdsworth, Michael J. Bennett, Malcolm J. Vissenberg, Kris Hodgman, T. Charlie Plant cell wall composition is important for regulating growth rates, especially in roots. However, neither analyses of cell wall composition nor transcriptomes on their own can comprehensively reveal which genes and processes are mediating growth and cell elongation rates. This study reveals the benefits of carrying out multiple analyses in combination. Sections of roots from five anatomically and functionally defined zones in Arabidopsis thaliana were prepared and divided into three biological replicates. We used glycan microarrays and antibodies to identify the major classes of glycans and glycoproteins present in the cell walls of these sections, and identified the expected decrease in pectin and increase in xylan from the meristematic zone (MS), through the rapid and late elongation zones (REZ, LEZ) to the maturation zone and the rest of the root, including the emerging lateral roots. Other compositional changes included extensin and xyloglucan levels peaking in the REZ and increasing levels of arabinogalactan-proteins (AGP) epitopes from the MS to the LEZ, which remained high through the subsequent mature zones. Immuno-staining using the same antibodies identified the tissue and (sub)cellular localization of many epitopes. Extensins were localized in epidermal and cortex cell walls, while AGP glycans were specific to different tissues from root-hair cells to the stele. The transcriptome analysis found several gene families peaking in the REZ. These included a large family of peroxidases (which produce the reactive oxygen species (ROS) needed for cell expansion), and three xyloglucan endo-transglycosylase/hydrolase genes (XTH17, XTH18, and XTH19). The significance of the latter may be related to a role in breaking and re-joining xyloglucan cross-bridges between cellulose microfibrils, a process which is required for wall expansion. Knockdowns of these XTHs resulted in shorter root lengths, confirming a role of the corresponding proteins in root extension growth. Frontiers Media 2015-02-20 Article PeerReviewed Wilson, Michael H., Holman, Tara J., Sørensen, Iben, Cancho-Sanchez, Ester, Wells, Darren M., Swarup, Ranjan, Knox, J. Paul, Willats, William G.T., Ubeda-Tomás, Susana, Holdsworth, Michael J., Bennett, Malcolm J., Vissenberg, Kris and Hodgman, T. Charlie (2015) Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone. Frontiers in Cell and Developmental Biology, 3 . 10/1-10/12. ISSN 2296-634X Root growth Plant cell walls Multiomics Transcriptomics Localisomics Epitomics Cell-wall polysaccharides Cell elongation https://doi.org/10.3389/fcell.2015.00010 doi:10.3389/fcell.2015.00010 doi:10.3389/fcell.2015.00010 |
| spellingShingle | Root growth Plant cell walls Multiomics Transcriptomics Localisomics Epitomics Cell-wall polysaccharides Cell elongation Wilson, Michael H. Holman, Tara J. Sørensen, Iben Cancho-Sanchez, Ester Wells, Darren M. Swarup, Ranjan Knox, J. Paul Willats, William G.T. Ubeda-Tomás, Susana Holdsworth, Michael J. Bennett, Malcolm J. Vissenberg, Kris Hodgman, T. Charlie Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title | Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title_full | Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title_fullStr | Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title_full_unstemmed | Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title_short | Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone |
| title_sort | multi-omics analysis identifies genes mediating the extension of cell walls in the arabidopsis thaliana root elongation zone |
| topic | Root growth Plant cell walls Multiomics Transcriptomics Localisomics Epitomics Cell-wall polysaccharides Cell elongation |
| url | https://eprints.nottingham.ac.uk/41647/ https://eprints.nottingham.ac.uk/41647/ https://eprints.nottingham.ac.uk/41647/ |