Literature DB >> 34112988

Real-time conversion of tissue-scale mechanical forces into an interdigitated growth pattern.

Samuel A Belteton1, Wenlong Li2, Makoto Yanagisawa3, Faezeh A Hatam2, Madeline I Quinn1, Margaret K Szymanski4, Matthew W Marley1, Joseph A Turner2, Daniel B Szymanski5,6.   

Abstract

The leaf epidermis is a dynamic biomechanical shell that integrates growth across spatial scales to influence organ morphology. Pavement cells, the fundamental unit of this tissue, morph irreversibly into highly lobed cells that drive planar leaf expansion. Here, we define how tissue-scale cell wall tensile forces and the microtubule-cellulose synthase systems dictate the patterns of interdigitated growth in real time. A morphologically potent subset of cortical microtubules span the periclinal and anticlinal cell faces to pattern cellulose fibres that generate a patch of anisotropic wall. The subsequent local polarized growth is mechanically coupled to the adjacent cell via a pectin-rich middle lamella, and this drives lobe formation. Finite element pavement cell models revealed cell wall tensile stress as an upstream patterning element that links cell- and tissue-scale biomechanical parameters to interdigitated growth. Cell lobing in leaves is evolutionarily conserved, occurs in multiple cell types and is associated with important agronomic traits. Our general mechanistic models of lobe formation provide a foundation to analyse the cellular basis of leaf morphology and function.

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Year:  2021        PMID: 34112988     DOI: 10.1038/s41477-021-00931-z

Source DB:  PubMed          Journal:  Nat Plants        ISSN: 2055-0278            Impact factor:   15.793


  62 in total

1.  Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process.

Authors:  Megan Andriankaja; Stijn Dhondt; Stefanie De Bodt; Hannes Vanhaeren; Frederik Coppens; Liesbeth De Milde; Per Mühlenbock; Aleksandra Skirycz; Nathalie Gonzalez; Gerrit T S Beemster; Dirk Inzé
Journal:  Dev Cell       Date:  2012-01-05       Impact factor: 12.270

2.  Divergence in Patterns of Leaf Growth Polarity Is Associated with the Expression Divergence of miR396.

Authors:  Mainak Das Gupta; Utpal Nath
Journal:  Plant Cell       Date:  2015-09-26       Impact factor: 11.277

3.  Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex.

Authors:  R Swarup; J Friml; A Marchant; K Ljung; G Sandberg; K Palme; M Bennett
Journal:  Genes Dev       Date:  2001-10-15       Impact factor: 11.361

4.  Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis.

Authors:  Ying Fu; Ying Gu; Zhiliang Zheng; Geoffrey Wasteneys; Zhenbiao Yang
Journal:  Cell       Date:  2005-03-11       Impact factor: 41.582

Review 5.  The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments.

Authors:  Emmanuel Panteris; Basil Galatis
Journal:  New Phytol       Date:  2005-09       Impact factor: 10.151

6.  Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development.

Authors:  Yangbin Gao; Yi Zhang; Da Zhang; Xinhua Dai; Mark Estelle; Yunde Zhao
Journal:  Proc Natl Acad Sci U S A       Date:  2015-02-02       Impact factor: 11.205

Review 7.  Evolutionary and Environmental Forces Sculpting Leaf Development.

Authors:  Daniel H Chitwood; Neelima R Sinha
Journal:  Curr Biol       Date:  2016-04-04       Impact factor: 10.834

8.  The epidermis both drives and restricts plant shoot growth.

Authors:  Sigal Savaldi-Goldstein; Charles Peto; Joanne Chory
Journal:  Nature       Date:  2007-03-08       Impact factor: 49.962

9.  The plant hormone ethylene restricts Arabidopsis growth via the epidermis.

Authors:  Irina Ivanova Vaseva; Enas Qudeimat; Thomas Potuschak; Yunlong Du; Pascal Genschik; Filip Vandenbussche; Dominique Van Der Straeten
Journal:  Proc Natl Acad Sci U S A       Date:  2018-04-11       Impact factor: 11.205

10.  Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape.

Authors:  Róza V Vőfély; Joseph Gallagher; Grace D Pisano; Madelaine Bartlett; Siobhan A Braybrook
Journal:  New Phytol       Date:  2018-10-03       Impact factor: 10.151

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  6 in total

1.  Cell twisting during desiccation reveals axial asymmetry in wall organization.

Authors:  Sedighe Keynia; Thomas C Davis; Daniel B Szymanski; Joseph A Turner
Journal:  Biophys J       Date:  2022-02-11       Impact factor: 4.033

2.  Protocol for mapping the variability in cell wall mechanical bending behavior in living leaf pavement cells.

Authors:  Wenlong Li; Sedighe Keynia; Samuel A Belteton; Faezeh Afshar-Hatam; Daniel B Szymanski; Joseph A Turner
Journal:  Plant Physiol       Date:  2022-03-04       Impact factor: 8.340

3.  CLASP balances two competing cell division plane cues during leaf development.

Authors:  Liyong Zhang; Chris Ambrose
Journal:  Nat Plants       Date:  2022-06-06       Impact factor: 17.352

Review 4.  Materials science and mechanosensitivity of living matter.

Authors:  Alison E Patteson; Merrill E Asp; Paul A Janmey
Journal:  Appl Phys Rev       Date:  2022-03       Impact factor: 19.527

5.  Building an extensible cell wall.

Authors:  Daniel J Cosgrove
Journal:  Plant Physiol       Date:  2022-06-27       Impact factor: 8.005

6.  Tethering of cellulose synthase to microtubules dampens mechano-induced cytoskeletal organization in Arabidopsis pavement cells.

Authors:  René Schneider; David W Ehrhardt; Elliot M Meyerowitz; Arun Sampathkumar
Journal:  Nat Plants       Date:  2022-08-18       Impact factor: 17.352

  6 in total

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