Shaping of a three-dimensional carnivorous trap through modulation of a planar growth mechanism

Autor: Jacob L. Newman, Richard Kennaway, John A. Fozard, Chunlan Piao, Chris D Whitewoods, Karen Lee, Yohei Koide, Man Yu, Minlong Cui, Athanasius F. M. Marée, Claire Bushell, Jerome Avondo, Enrico Coen
Jazyk: angličtina
Rok vydání: 2019
Předmět:
0301 basic medicine
Leaves
Research Facilities
Plant Science
Information Centers
0302 clinical medicine
Planar
Cell polarity
Cell Cycle and Cell Division
Biology (General)
Anisotropy
Utricularia
Plant Growth and Development
Carnivorous plant
Archives
General Neuroscience
Physics
Plant Anatomy
Eukaryota
Cell Polarity
Plants
Condensed Matter Physics
Carnivory
Lamiales
Experimental Organism Systems
Cell Processes
Physical Sciences
General Agricultural and Biological Sciences
Biological system
Research Article
Cell Physiology
QH301-705.5
Polarity (physics)
Arabidopsis Thaliana
Materials Science
Material Properties
Morphogenesis
Plant Development
Brassica
Biology
Research and Analysis Methods
General Biochemistry
Genetics and Molecular Biology
03 medical and health sciences
Model Organisms
Plant and Algal Models
Plant Cells
Molecular Biology Techniques
Molecular Biology
Cell Shape
Utricularia gibba
Cell Proliferation
Cell Size
General Immunology and Microbiology
Organisms
Biology and Life Sciences
Leaf Development
Cell Biology
biology.organism_classification
Plant Leaves
030104 developmental biology
Animal Studies
030217 neurology & neurosurgery
Cloning
Developmental Biology
Zdroj: PLoS Biology
PLoS Biology, Vol 17, Iss 10, p e3000427 (2019)
ISSN: 1544-9173
Popis: Leaves display a remarkable range of forms, from flat sheets with simple outlines to cup-shaped traps. Although much progress has been made in understanding the mechanisms of planar leaf development, it is unclear whether similar or distinctive mechanisms underlie shape transformations during development of more complex curved forms. Here, we use 3D imaging and cellular and clonal analysis, combined with computational modelling, to analyse the development of cup-shaped traps of the carnivorous plant Utricularia gibba. We show that the transformation from a near-spherical form at early developmental stages to an oblate spheroid with a straightened ventral midline in the mature form can be accounted for by spatial variations in rates and orientations of growth. Different hypotheses regarding spatiotemporal control predict distinct patterns of cell shape and size, which were tested experimentally by quantifying cellular and clonal anisotropy. We propose that orientations of growth are specified by a proximodistal polarity field, similar to that hypothesised to account for Arabidopsis leaf development, except that in Utricularia, the field propagates through a highly curved tissue sheet. Independent evidence for the polarity field is provided by the orientation of glandular hairs on the inner surface of the trap. Taken together, our results show that morphogenesis of complex 3D leaf shapes can be accounted for by similar mechanisms to those for planar leaves, suggesting that simple modulations of a common growth framework underlie the shaping of a diverse range of morphologies.
Many plant and animal organs derive from tissue sheets, but how are they shaped to create the diversity of forms observed in nature? This study uses a combination of imaging and mathematical modelling to show how carnivorous plant traps shape themselves in 3D by a growth framework oriented by tissue polarity, similar to that found in planar leaves.
Databáze: OpenAIRE
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