Literature DB >> 29309524

Two-stage patterning dynamics in conifer cotyledon whorl morphogenesis.

David M Holloway1,2, Ignacio Rozada1, Joshua J H Bray3.   

Abstract

Background and Aims: Conifer embryos, unlike those of monocots or dicots, have variable numbers of cotyledons, even within the same species. Cotyledons form in a single whorl on a dome-shaped embryo. The closely spaced cotyledons are not found outside this ring, indicating a radial control on where they can form. Polar transport of the hormone auxin affects outgrowth of distinct cotyledons, but not the radial aspect of the whorl or the within-whorl spacing between cotyledons. A quantitative model of plant growth regulator patterning is needed to understand the dynamics of this complex morphogenetic process.
Methods: A two-stage reaction-diffusion model is developed for the spatial patterning of growth regulators on the embryo surface, with a radial pattern (P1) constraining the shorter-wavelength cotyledon pattern (P2) to a whorl. These patterns drive three-dimensional (3-D) morphogenesis by catalysing local surface growth. Key
Results: Growth driven by P2 generates single whorls across the experimentally observed range of two to 11 cotyledons, as well as the circularly symmetric response to auxin transport interference. These computations are the first corroboration of earlier theoretical proposals for hierarchical control of whorl formation. The model generates the linear relationship between cotyledon number and embryo diameter observed experimentally. This accounts for normal integer cotyledon number selection, as well as the less common cotyledon fusings and splittings observed experimentally. Flattening of the embryo during development may affect the upward outgrowth angle of the cotyledons. Conclusions: Cotyledon morphogenesis is more complex geometrically in conifers than in angiosperms, involving 2-D patterning which deforms a surface in three dimensions. This work develops a quantitative framework for understanding the growth and patterning dynamics involved in conifer cotyledon development, and applies more generally to the morphogenesis of whorls with many primordia.
© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Year:  2018        PMID: 29309524      PMCID: PMC5838814          DOI: 10.1093/aob/mcx185

Source DB:  PubMed          Journal:  Ann Bot        ISSN: 0305-7364            Impact factor:   4.357


  34 in total

Review 1.  Auxin transport - shaping the plant.

Authors:  Jirí Friml
Journal:  Curr Opin Plant Biol       Date:  2003-02       Impact factor: 7.834

2.  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

3.  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

4.  WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism.

Authors:  Stefanie Sick; Stefan Reinker; Jens Timmer; Thomas Schlake
Journal:  Science       Date:  2006-11-02       Impact factor: 47.728

5.  Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism.

Authors:  Rushikesh Sheth; Luciano Marcon; M Félix Bastida; Marisa Junco; Laura Quintana; Randall Dahn; Marie Kmita; James Sharpe; Maria A Ros
Journal:  Science       Date:  2012-12-14       Impact factor: 47.728

6.  Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients.

Authors:  J Raspopovic; L Marcon; L Russo; J Sharpe
Journal:  Science       Date:  2014-08-01       Impact factor: 47.728

7.  MAB4-induced auxin sink generates local auxin gradients in Arabidopsis organ formation.

Authors:  Masahiko Furutani; Yasukazu Nakano; Masao Tasaka
Journal:  Proc Natl Acad Sci U S A       Date:  2014-01-06       Impact factor: 11.205

8.  Spatially quantitative control of the number of cotyledons in a clonal population of somatic embryos of hybrid larch Larix x leptoeuropaea.

Authors:  Lionel G Harrison; Patrick Von Aderkas
Journal:  Ann Bot       Date:  2004-04       Impact factor: 4.357

9.  Inhibited polar auxin transport results in aberrant embryo development in Norway spruce.

Authors:  Emma Larsson; Folke Sitbon; Karin Ljung; Sara Von Arnold
Journal:  New Phytol       Date:  2007-11-27       Impact factor: 10.151

10.  A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves.

Authors:  Simona Digiuni; Swen Schellmann; Florian Geier; Bettina Greese; Martina Pesch; Katja Wester; Burcu Dartan; Valerie Mach; Bhylahalli Purushottam Srinivas; Jens Timmer; Christian Fleck; Martin Hulskamp
Journal:  Mol Syst Biol       Date:  2008-09-02       Impact factor: 11.429

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  1 in total

Review 1.  Patterning, From Conifers to Consciousness: Turing's Theory and Order From Fluctuations.

Authors:  Thurston C Lacalli
Journal:  Front Cell Dev Biol       Date:  2022-05-03
  1 in total

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