A core mechanism for specifying root vascular pattern can replicate the anatomical variation seen in diverse plant species

Mellor, Nathan; Vaughan-Hirsch, John; Kümpers, Britta M.C.; Help-Rinta-Rahko, Hanna; Miyashima, Shunsuke; Pekka Mähönen, Ari; Campilho, Ana; King, John R.; Bishopp, Anthony

Abstract

Pattern formation is typically controlled through the interaction between molecular signals within a given tissue. During early embryonic development, roots of the model plant Arabidopsis thaliana have a radially symmetric pattern, but a heterogeneous input of the hormone auxin from the two cotyledons forces the vascular cylinder to develop a diarch pattern with two xylem poles. Molecular analyses and mathematical approaches have uncovered the regulatory circuit that propagates this initial auxin signal into a stable cellular pattern. The diarch pattern seen in Arabidopsis is relatively uncommon among flowering plants, with most species having between three and eight xylem poles. Here, we have used multiscale mathematical modelling to demonstrate that this regulatory module does not require a heterogeneous auxin input to specify the vascular pattern. Instead, the pattern can emerge dynamically, with its final form dependent upon spatial constraints and growth. The predictions of our simulations compare to experimental observations of xylem pole number across a range of species, as well as in transgenic systems in Arabidopsis in which we manipulate the size of the vascular cylinder. By considering the spatial constraints, our model is able to explain much of the diversity seen in different flowering plant species.

Citation

Mellor, N., Vaughan-Hirsch, J., Kümpers, B. M., Help-Rinta-Rahko, H., Miyashima, S., Pekka Mähönen, A., …Bishopp, A. (2019). A core mechanism for specifying root vascular pattern can replicate the anatomical variation seen in diverse plant species. Development, 146(6), Article dev172411. https://doi.org/10.1242/dev.172411

• Journal Article Type: Article
• Acceptance Date: Feb 18, 2019
• Online Publication Date: Mar 15, 2019
• Publication Date: Mar 15, 2019
• Deposit Date: Feb 26, 2019
• Publicly Available Date: Mar 16, 2020
• Journal: Development
• Print ISSN: 0950-1991
• Electronic ISSN: 1477-9129
• Publisher: Company of Biologists
• Peer Reviewed: Peer Reviewed
• Volume: 146
• Issue: 6
• Article Number: dev172411
• DOI: https://doi.org/10.1242/dev.172411
• Keywords: Multiscale modelling, Vascular pattern, Auxin, Cytokinin, Developmental biology, Root biology
• Public URL: https://nottingham-repository.worktribe.com/output/1586569
• Publisher URL: http://dev.biologists.org/content/146/6/dev172411
• Additional Information: Project: Anthony Bishopp New Investigator
• Contract Date: Feb 26, 2019