TY - JOUR
T1 - Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues
AU - Lucas, Mikaël
AU - Kenobi, Kim
AU - Von Wangenheim, Daniel
AU - Voß, Ute
AU - Swarup, Kamal
AU - De Smet, Ive
AU - Van Damme, Daniël
AU - Lawrence, Tara
AU - Péret, Benjamin
AU - Moscardi, Eric
AU - Barbeau, Daniel
AU - Godin, Christophe
AU - Salt, David
AU - Guyomarc'h, Soazig
AU - Stelzer, Ernst H.K.
AU - Maizel, Alexis
AU - Laplaze, Laurent
AU - Bennett, Malcolm J.
N1 - Copyright:
Copyright 2013 Elsevier B.V., All rights reserved.
PY - 2013/3/26
Y1 - 2013/3/26
N2 - 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.
AB - 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.
KW - Arabidopsis thaliana
KW - Biomechanical regulation
KW - Lateral root development
KW - Plant morphogenesis
KW - Statistical shape analysis
UR - http://www.scopus.com/inward/record.url?scp=84875511938&partnerID=8YFLogxK
U2 - 10.1073/pnas.1210807110
DO - 10.1073/pnas.1210807110
M3 - Article
C2 - 23479644
AN - SCOPUS:84875511938
SN - 0027-8424
VL - 110
SP - 5229
EP - 5234
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 13
ER -