Two-stage patterning dynamics in conifer cotyledon whorl morphogenesis. (4th January 2018)

• Record Type: Journal Article
• Authors: Holloway, David M; Rozada, Ignacio; Bray, Joshua J H
• Is Part Of: Annals of botany. Volume 121:Number 3(2018)
• Page Start: 525
• Page End: 534
• Publication Date: 2018-01-04
• Subjects: Conifer -- Pinaceae -- embryogenesis -- whorl -- cotyledon -- pattern formation -- morphogenesis -- finite element model -- plant growth regulator -- reaction–diffusion -- auxin -- NPA; Botany -- Periodicals; 580
• DOI: 10.1093/aob/mcx185
• Languages: English
• ISSNs: 0305-7364

Abstract

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.