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

被引:53
作者
Chitwood, Daniel H. [1 ]
Headland, Lauren R. [1 ]
Ranjan, Aashish [1 ]
Martinez, Ciera C. [1 ]
Braybrook, Siobhan A. [2 ]
Koenig, Daniel P. [3 ]
Kuhlemeier, Cris [2 ]
Smith, Richard S. [2 ]
Sinha, Neelima R. [1 ]
机构
[1] Univ Calif Davis, Dept Plant Biol, Davis, CA 95616 USA
[2] Univ Bern, Inst Plant Sci, CH-3013 Bern, Switzerland
[3] Max Planck Inst Dev Biol, Dept Mol Biol, D-72076 Tubingen, Germany
基金
美国国家科学基金会;
关键词
TRANSPORT; MODEL; GROWTH; SHAPE;
D O I
10.1105/tpc.112.098798
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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.
引用
收藏
页码:2318 / 2327
页数:10
相关论文
共 26 条
[1]   A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta [J].
Barkoulas, Michalis ;
Hay, Angela ;
Kougioumoutzi, Evagelia ;
Tsiantis, Miltos .
NATURE GENETICS, 2008, 40 (09) :1136-1141
[2]   Model for the regulation of Arabidopsis thaliana leaf margin development [J].
Bilsborough, Gemma D. ;
Runions, Adam ;
Barkoulas, Michalis ;
Jenkins, Huw W. ;
Hasson, Alice ;
Galinha, Carla ;
Laufs, Patrick ;
Hay, Angela ;
Prusinkiewicz, Przemyslaw ;
Tsiantis, Miltos .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2011, 108 (08) :3424-3429
[3]  
Dormer K.J. Others., 1972, Shoot organization in vascular plants
[4]   Analysis of expansin-induced morphogenesis on the apical meristem of tomato [J].
Fleming, AJ ;
Caderas, D ;
Wehrli, E ;
McQueen-Mason, S ;
Kuhlemeier, C .
PLANTA, 1999, 208 (02) :166-174
[5]   Evaluation of variation of root shape of Japanese radish (Raphanus sativus L.) based on image analysis using elliptic Fourier descriptors [J].
Iwata, H ;
Niikura, S ;
Matsuura, S ;
Takano, Y ;
Ukai, Y .
EUPHYTICA, 1998, 102 (02) :143-149
[6]   SHAPE: A computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors [J].
Iwata, H ;
Ukai, Y .
JOURNAL OF HEREDITY, 2002, 93 (05) :384-385
[7]   An auxin-driven polarized transport model for phyllotaxis [J].
Jönsson, H ;
Heisler, MG ;
Shapiro, BE ;
Meyerowitz, EM ;
Mjolsness, E .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (05) :1633-1638
[8]   Auxin patterns Solanum lycopersicum leaf morphogenesis [J].
Koenig, Daniel ;
Bayer, Emmanuelle ;
Kang, Julie ;
Kuhlemeier, Cris ;
Sinha, Neelima .
DEVELOPMENT, 2009, 136 (17) :2997-3006
[9]   Anodic asymmetry of leaves and flowers and its relationship to phyllotaxis [J].
Korn, Robert W. .
ANNALS OF BOTANY, 2006, 97 (06) :1011-1015
[10]   Phyllotaxis [J].
Kuhlemeier, Cris .
TRENDS IN PLANT SCIENCE, 2007, 12 (04) :143-150