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Research ArticleResearch Article
Open Access

Leaf Asymmetry as a Developmental Constraint Imposed by Auxin-Dependent Phyllotactic Patterning

Daniel H. Chitwood, Lauren R. Headland, Aashish Ranjan, Ciera C. Martinez, Siobhan A. Braybrook, Daniel P. Koenig, Cris Kuhlemeier, Richard S. Smith, Neelima R. Sinha
Daniel H. Chitwood
aDepartment of Plant Biology, University of California, Davis, California 95616
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Lauren R. Headland
aDepartment of Plant Biology, University of California, Davis, California 95616
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Aashish Ranjan
aDepartment of Plant Biology, University of California, Davis, California 95616
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Ciera C. Martinez
aDepartment of Plant Biology, University of California, Davis, California 95616
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Siobhan A. Braybrook
bInstitute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland
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Daniel P. Koenig
cDepartment of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tuebingen, Germany
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Cris Kuhlemeier
bInstitute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland
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Richard S. Smith
bInstitute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland
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Neelima R. Sinha
aDepartment of Plant Biology, University of California, Davis, California 95616
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  • For correspondence: nrsinha@ucdavis.edu

Published June 2012. DOI: https://doi.org/10.1105/tpc.112.098798

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  • © 2012 American Society of Plant Biologists. All rights reserved.

Abstract

In a majority of species, leaf development is thought to proceed in a bilaterally symmetric fashion without systematic asymmetries. This is despite the left and right sides of an initiating primordium occupying niches that differ in their distance from sinks and sources of auxin. Here, we revisit an existing model of auxin transport sufficient to recreate spiral phyllotactic patterns and find previously overlooked asymmetries between auxin distribution and the centers of leaf primordia. We show that it is the direction of the phyllotactic spiral that determines the side of the leaf these asymmetries fall on. We empirically confirm the presence of an asymmetric auxin response using a DR5 reporter and observe morphological asymmetries in young leaf primordia. Notably, these morphological asymmetries persist in mature leaves, and we observe left-right asymmetries in the superficially bilaterally symmetric leaves of tomato (Solanum lycopersicum) and Arabidopsis thaliana that are consistent with modeled predictions. We further demonstrate that auxin application to a single side of a leaf primordium is sufficient to recapitulate the asymmetries we observe. Our results provide a framework to study a previously overlooked developmental axis and provide insights into the developmental constraints imposed upon leaf morphology by auxin-dependent phyllotactic patterning.

  • Glossary

    SAM
    shoot apical meristem
    IAA
    indole-3-acetic acid
    C
    clockwise
    CC
    counterclockwise
    EFDs
    elliptical Fourier descriptors
    PC
    principal component
    • Received March 27, 2012.
    • Revised May 18, 2012.
    • Accepted June 4, 2012.
    • Published June 21, 2012.

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    Leaf Asymmetry as a Developmental Constraint Imposed by Auxin-Dependent Phyllotactic Patterning
    Daniel H. Chitwood, Lauren R. Headland, Aashish Ranjan, Ciera C. Martinez, Siobhan A. Braybrook, Daniel P. Koenig, Cris Kuhlemeier, Richard S. Smith, Neelima R. Sinha
    The Plant Cell Jun 2012, 24 (6) 2318-2327; DOI: 10.1105/tpc.112.098798

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    Leaf Asymmetry as a Developmental Constraint Imposed by Auxin-Dependent Phyllotactic Patterning
    Daniel H. Chitwood, Lauren R. Headland, Aashish Ranjan, Ciera C. Martinez, Siobhan A. Braybrook, Daniel P. Koenig, Cris Kuhlemeier, Richard S. Smith, Neelima R. Sinha
    The Plant Cell Jun 2012, 24 (6) 2318-2327; DOI: 10.1105/tpc.112.098798
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