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

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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.
Keywords
statistical shape analysis, Arabidopsis thaliana, biomechanical regulation, plant morphogenesis, lateral root development, ARABIDOPSIS-THALIANA, PLANT-GROWTH, CELL, INITIATION, RESOLUTION, EMERGENCE, SUBERIN, MODULE

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MLA
Lucas, Mikaël, Kim Kenobi, Daniel von Wangenheim, et al. “Lateral Root Morphogenesis Is Dependent on the Mechanical Properties of the Overlaying Tissues.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 110.13 (2013): 5229–5234. Print.
APA
Lucas, Mikaël, Kenobi, K., von Wangenheim, D., Voss, U., Swarup, K., De Smet, I., Van Damme, D., et al. (2013). Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 110(13), 5229–5234.
Chicago author-date
Lucas, Mikaël, Kim Kenobi, Daniel von Wangenheim, Ute Voss, Kamal Swarup, Ive De Smet, Daniël Van Damme, et al. 2013. “Lateral Root Morphogenesis Is Dependent on the Mechanical Properties of the Overlaying Tissues.” Proceedings of the National Academy of Sciences of the United States of America 110 (13): 5229–5234.
Chicago author-date (all authors)
Lucas, Mikaël, Kim Kenobi, Daniel von Wangenheim, Ute Voss, Kamal Swarup, Ive De Smet, Daniël Van Damme, Tara Lawrence, Benjamin Péret, Eric Moscardi, Daniel Barbeau, Christophe Godin, David Salt, Soazig Guyomarc’h, Ernst HK Stelzer, Alexis Maizel, Laurent Laplaze, and Malcolm J Bennett. 2013. “Lateral Root Morphogenesis Is Dependent on the Mechanical Properties of the Overlaying Tissues.” Proceedings of the National Academy of Sciences of the United States of America 110 (13): 5229–5234.
Vancouver
1.
Lucas M, Kenobi K, von Wangenheim D, Voss U, Swarup K, De Smet I, et al. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2013;110(13):5229–34.
IEEE
[1]
M. Lucas et al., “Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 110, no. 13, pp. 5229–5234, 2013.
@article{3233116,
  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.},
  author       = {Lucas, Mikaël and Kenobi, Kim and von Wangenheim, Daniel and Voss, Ute and Swarup, Kamal and De Smet, Ive and Van Damme, Daniël and Lawrence, Tara and Péret, Benjamin and Moscardi, Eric and Barbeau, Daniel and Godin, Christophe and Salt, David and Guyomarc'h, Soazig and Stelzer, Ernst HK and Maizel, Alexis and Laplaze, Laurent and Bennett, Malcolm J},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keywords     = {statistical shape analysis,Arabidopsis thaliana,biomechanical regulation,plant morphogenesis,lateral root development,ARABIDOPSIS-THALIANA,PLANT-GROWTH,CELL,INITIATION,RESOLUTION,EMERGENCE,SUBERIN,MODULE},
  language     = {eng},
  number       = {13},
  pages        = {5229--5234},
  title        = {Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues},
  url          = {http://dx.doi.org/10.1073/pnas.1210807110},
  volume       = {110},
  year         = {2013},
}

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