Geometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens

Han Tang, Kilian Duijts, Magdalena Bezanilla, Ben Scheres, Joop E.M. Vermeer, Viola Willemsen*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

During land colonization, plants acquired a range of body plan adaptations, of which the innovation of three-dimensional (3D) tissues increased organismal complexity and reproductivity. In the moss, Physcomitrella patens, a 3D leafy gametophore originates from filamentous cells that grow in a two-dimensional (2D) plane through a series of asymmetric cell divisions. Asymmetric cell divisions that coincide with different cell division planes and growth directions enable the developmental switch from 2D to 3D, but insights into the underlying mechanisms coordinating this switch are still incomplete. Using 2D and 3D imaging and image segmentation, we characterized two geometric cues, the width of the initial cell and the angle of the transition division plane, which sufficiently distinguished a gametophore initial cell from a branch initial cell. These identified cues were further confirmed in gametophore formation mutants. The identification of a fluorescent marker allowed us to successfully predict the gametophore initial cell with > 90% accuracy before morphological changes, supporting our hypothesis that, before the transition division, parental cells of the gametophore initials possess different properties from those of the branch initials. Our results suggest that the cell fate decision of the initial cell is determined in the parental cell, before the transition division.

Original languageEnglish
Pages (from-to)1945-1955
JournalNew Phytologist
Volume225
Issue number5
Early online date22 Oct 2019
DOIs
Publication statusE-pub ahead of print - 22 Oct 2019

Fingerprint

Bryopsida
Physcomitrella patens
Cues
gametophores
Growth
Asymmetric Cell Division
cells
cell division
Cell Division
Bryophyta
mosses and liverworts
image analysis

Keywords

  • 2D-to-3D development
  • asymmetric cell division
  • cell fate switch
  • geometric cues
  • Physcomitrella patens

Cite this

Tang, Han ; Duijts, Kilian ; Bezanilla, Magdalena ; Scheres, Ben ; Vermeer, Joop E.M. ; Willemsen, Viola. / Geometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens. In: New Phytologist. 2020 ; Vol. 225, No. 5. pp. 1945-1955.
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abstract = "During land colonization, plants acquired a range of body plan adaptations, of which the innovation of three-dimensional (3D) tissues increased organismal complexity and reproductivity. In the moss, Physcomitrella patens, a 3D leafy gametophore originates from filamentous cells that grow in a two-dimensional (2D) plane through a series of asymmetric cell divisions. Asymmetric cell divisions that coincide with different cell division planes and growth directions enable the developmental switch from 2D to 3D, but insights into the underlying mechanisms coordinating this switch are still incomplete. Using 2D and 3D imaging and image segmentation, we characterized two geometric cues, the width of the initial cell and the angle of the transition division plane, which sufficiently distinguished a gametophore initial cell from a branch initial cell. These identified cues were further confirmed in gametophore formation mutants. The identification of a fluorescent marker allowed us to successfully predict the gametophore initial cell with > 90{\%} accuracy before morphological changes, supporting our hypothesis that, before the transition division, parental cells of the gametophore initials possess different properties from those of the branch initials. Our results suggest that the cell fate decision of the initial cell is determined in the parental cell, before the transition division.",
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Geometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens. / Tang, Han; Duijts, Kilian; Bezanilla, Magdalena; Scheres, Ben; Vermeer, Joop E.M.; Willemsen, Viola.

In: New Phytologist, Vol. 225, No. 5, 03.2020, p. 1945-1955.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Geometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens

AU - Tang, Han

AU - Duijts, Kilian

AU - Bezanilla, Magdalena

AU - Scheres, Ben

AU - Vermeer, Joop E.M.

AU - Willemsen, Viola

PY - 2019/10/22

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