Literature DB >> 27380805

A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis.

Yassin Refahi1,2, Géraldine Brunoud1, Etienne Farcot3,4, Alain Jean-Marie5, Minna Pulkkinen6, Teva Vernoux1, Christophe Godin7.   

Abstract

Exploration of developmental mechanisms classically relies on analysis of pattern regularities. Whether disorders induced by biological noise may carry information on building principles of developmental systems is an important debated question. Here, we addressed theoretically this question using phyllotaxis, the geometric arrangement of plant aerial organs, as a model system. Phyllotaxis arises from reiterative organogenesis driven by lateral inhibitions at the shoot apex. Motivated by recurrent observations of disorders in phyllotaxis patterns, we revisited in depth the classical deterministic view of phyllotaxis. We developed a stochastic model of primordia initiation at the shoot apex, integrating locality and stochasticity in the patterning system. This stochastic model recapitulates phyllotactic patterns, both regular and irregular, and makes quantitative predictions on the nature of disorders arising from noise. We further show that disorders in phyllotaxis instruct us on the parameters governing phyllotaxis dynamics, thus that disorders can reveal biological watermarks of developmental systems.

Entities:  

Keywords:  A. thaliana; developmental biology; emergence; inhibitory fields; multi-scale modeling; noise; permutations; phyllotaxis; plant biology; stem cells

Mesh:

Year:  2016        PMID: 27380805      PMCID: PMC4947393          DOI: 10.7554/eLife.14093

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  39 in total

Review 1.  Complex pattern formation by a self-destabilization of established patterns: chemotactic orientation and phyllotaxis as examples.

Authors:  Hans Meinhardt
Journal:  C R Biol       Date:  2003-02       Impact factor: 1.583

2.  Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.

Authors:  Alexis Peaucelle; Siobhan A Braybrook; Laurent Le Guillou; Emeric Bron; Cris Kuhlemeier; Herman Höfte
Journal:  Curr Biol       Date:  2011-10-06       Impact factor: 10.834

3.  An auxin-driven polarized transport model for phyllotaxis.

Authors:  Henrik Jönsson; Marcus G Heisler; Bruce E Shapiro; Elliot M Meyerowitz; Eric Mjolsness
Journal:  Proc Natl Acad Sci U S A       Date:  2006-01-13       Impact factor: 11.205

4.  A plausible model of phyllotaxis.

Authors:  Richard S Smith; Soazig Guyomarc'h; Therese Mandel; Didier Reinhardt; Cris Kuhlemeier; Przemyslaw Prusinkiewicz
Journal:  Proc Natl Acad Sci U S A       Date:  2006-01-23       Impact factor: 11.205

Review 5.  Phyllotaxis.

Authors:  Cris Kuhlemeier
Journal:  Trends Plant Sci       Date:  2007-03-26       Impact factor: 18.313

Review 6.  Temporal dynamics of patterning by morphogen gradients.

Authors:  Eva Kutejova; James Briscoe; Anna Kicheva
Journal:  Curr Opin Genet Dev       Date:  2009-07-10       Impact factor: 5.578

Review 7.  Phenotyping and beyond: modelling the relationships between traits.

Authors:  Christine Granier; Denis Vile
Journal:  Curr Opin Plant Biol       Date:  2014-03-15       Impact factor: 7.834

8.  The auxin signalling network translates dynamic input into robust patterning at the shoot apex.

Authors:  Teva Vernoux; Géraldine Brunoud; Etienne Farcot; Valérie Morin; Hilde Van den Daele; Jonathan Legrand; Marina Oliva; Pradeep Das; Antoine Larrieu; Darren Wells; Yann Guédon; Lynne Armitage; Franck Picard; Soazig Guyomarc'h; Coralie Cellier; Geraint Parry; Rachil Koumproglou; John H Doonan; Mark Estelle; Christophe Godin; Stefan Kepinski; Malcolm Bennett; Lieven De Veylder; Jan Traas
Journal:  Mol Syst Biol       Date:  2011-07-05       Impact factor: 11.429

9.  Noise and robustness in phyllotaxis.

Authors:  Vincent Mirabet; Fabrice Besnard; Teva Vernoux; Arezki Boudaoud
Journal:  PLoS Comput Biol       Date:  2012-02-16       Impact factor: 4.475

10.  Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development.

Authors:  Szymon Stoma; Mikael Lucas; Jérôme Chopard; Marianne Schaedel; Jan Traas; Christophe Godin
Journal:  PLoS Comput Biol       Date:  2008-10-31       Impact factor: 4.475

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  9 in total

1.  Symmetry and its transition in phyllotaxis.

Authors:  Takaaki Yonekura; Munetaka Sugiyama
Journal:  J Plant Res       Date:  2021-04-28       Impact factor: 2.629

2.  Golden ratio and phyllotaxis, a clear mathematical link.

Authors:  François Bergeron; Christophe Reutenauer
Journal:  J Math Biol       Date:  2018-07-23       Impact factor: 2.259

3.  Temporal integration of auxin information for the regulation of patterning.

Authors:  Carlos S Galvan-Ampudia; Guillaume Cerutti; Jonathan Legrand; Géraldine Brunoud; Raquel Martin-Arevalillo; Romain Azais; Vincent Bayle; Steven Moussu; Christian Wenzl; Yvon Jaillais; Jan U Lohmann; Christophe Godin; Teva Vernoux
Journal:  Elife       Date:  2020-05-07       Impact factor: 8.140

Review 4.  Developmental stochasticity and variation in floral phyllotaxis.

Authors:  Miho S Kitazawa
Journal:  J Plant Res       Date:  2021-04-05       Impact factor: 2.629

Review 5.  What shoots can teach about theories of plant form.

Authors:  Teva Vernoux; Fabrice Besnard; Christophe Godin
Journal:  Nat Plants       Date:  2021-06-07       Impact factor: 15.793

Review 6.  Light Regulation of Axillary Bud Outgrowth Along Plant Axes: An Overview of the Roles of Sugars and Hormones.

Authors:  Anne Schneider; Christophe Godin; Frédéric Boudon; Sabine Demotes-Mainard; Soulaiman Sakr; Jessica Bertheloot
Journal:  Front Plant Sci       Date:  2019-10-18       Impact factor: 5.753

7.  Phyllotactic regularity requires the Paf1 complex in Arabidopsis.

Authors:  Kateryna Fal; Mengying Liu; Assem Duisembekova; Yassin Refahi; Elizabeth S Haswell; Olivier Hamant
Journal:  Development       Date:  2017-10-05       Impact factor: 6.868

8.  Synthetic hormone-responsive transcription factors can monitor and re-program plant development.

Authors:  Arjun Khakhar; Alexander R Leydon; Andrew C Lemmex; Eric Klavins; Jennifer L Nemhauser
Journal:  Elife       Date:  2018-05-01       Impact factor: 8.140

9.  Spiral phyllotaxis underlies constrained variation in Anemone (Ranunculaceae) tepal arrangement.

Authors:  Miho S Kitazawa; Koichi Fujimoto
Journal:  J Plant Res       Date:  2018-03-27       Impact factor: 2.629

  9 in total

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