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Multi-omics analysis identifies genes mediating the extension of cell walls in the Arabidopsis thaliana root elongation zone

Wilson, Michael H.; Holman, Tara J.; S�rensen, Iben; Cancho-Sanchez, Ester; Wells, Darren M.; Swarup, Ranjan; Knox, J. Paul; Willats, William G.T.; Ubeda-Tom�s, 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 Thumbnail


Authors

Tara J. Holman

Iben S�rensen

Ester Cancho-Sanchez

J. Paul Knox

William G.T. Willats

Susana Ubeda-Tom�s

Kris Vissenberg

T. Charlie Hodgman



Abstract

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.

Citation

Wilson, M. H., Holman, T. J., Sørensen, I., Cancho-Sanchez, E., Wells, D. M., Swarup, R., Knox, J. P., Willats, W. G., Ubeda-Tomás, S., Holdsworth, M. J., Bennett, M. J., Vissenberg, K., & Hodgman, T. C. (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(FEB), Article 10. https://doi.org/10.3389/fcell.2015.00010

Journal Article Type Article
Acceptance Date Feb 1, 2015
Online Publication Date Feb 20, 2015
Publication Date Feb 20, 2015
Deposit Date Mar 30, 2017
Publicly Available Date Mar 30, 2017
Journal Frontiers in Cell and Developmental Biology
Electronic ISSN 2296-634X
Publisher Frontiers Media
Peer Reviewed Peer Reviewed
Volume 3
Issue FEB
Article Number 10
DOI https://doi.org/10.3389/fcell.2015.00010
Keywords Root growth, Plant cell walls, Multiomics, Transcriptomics, Localisomics, Epitomics, Cell-wall polysaccharides, Cell elongation
Public URL https://nottingham-repository.worktribe.com/output/744719
Publisher URL https://doi.org/10.3389/fcell.2015.00010
Contract Date Mar 30, 2017

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