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Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues

Lucas, Mika�l; Kenobi, Kim; Von Wangenheim, Daniel; Vo�, Ute; Swarup, Kamal; De Smet, Ive; Van Damme, Dani�l; Lawrence, Tara; P�ret, Benjamin; Moscardi, Eric; Barbeau, Daniel; Godin, Christophe; Salt, David; Guyomarc'h, Soazig; Stelzer, Ernst H.K.; Maizel, Alexis; Laplaze, Laurent; Bennett, Malcolm J.

Authors

Mika�l Lucas

Kim Kenobi

Daniel Von Wangenheim

UTE VOSS ute.voss@nottingham.ac.uk
Assistant Professor

Kamal Swarup

Ive De Smet

Dani�l Van Damme

Tara Lawrence

Benjamin P�ret

Eric Moscardi

Daniel Barbeau

Christophe Godin

David Salt

Soazig Guyomarc'h

Ernst H.K. Stelzer

Alexis Maizel

Laurent Laplaze



Abstract

In Arabidopsis, lateral root primordia (LRPs) originate from pericycle cells located deep within the parental root and have to emerge through endodermal, cortical, and epidermal tissues. These overlaying tissues place biomechanical constraints on the LRPs that are likely to impact their morphogenesis. This study probes the interplay between the patterns of cell division, organ shape, and overlaying tissues on LRP morphogenesis by exploiting recent advances in live plant cell imaging and image analysis. Our 3D/4D image analysis revealed that early stage LRPs exhibit tangential divisions that create a ring of cells corralling a population of rapidly dividing cells at its center. The patterns of division in the latter population of cells during LRP morphogenesis are not stereotypical. In contrast, statistical analysis demonstrated that the shape of new LRPs is highly conserved. We tested the relative importance of cell division pattern versus overlaying tissues on LRP morphogenesis using mutant and transgenic approaches. The double mutant aurora1 (aur1) aur2 disrupts the pattern of LRP cell divisions and impacts its growth dynamics, yet the new organ's dome shape remains normal. In contrast, manipulating the properties of overlaying tissues disrupted LRP morphogenesis. We conclude that the interaction with overlaying tissues, rather than the precise pattern of divisions, is most important for LRP morphogenesis and optimizes the process of lateral root emergence. © PNAS 2013.

Citation

Lucas, M., Kenobi, K., Von Wangenheim, D., Voß, U., Swarup, K., De Smet, I., …Bennett, M. J. (2013). Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proceedings of the National Academy of Sciences, 110(13), 5229-5234. https://doi.org/10.1073/pnas.1210807110

Journal Article Type Article
Online Publication Date Mar 11, 2013
Publication Date Mar 26, 2013
Deposit Date May 15, 2020
Journal Proceedings of the National Academy of Sciences of the United States of America
Print ISSN 0027-8424
Electronic ISSN 1091-6490
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 110
Issue 13
Pages 5229-5234
DOI https://doi.org/10.1073/pnas.1210807110
Public URL https://nottingham-repository.worktribe.com/output/3092741
Publisher URL https://www.pnas.org/content/110/13/5229