Quantitative Control of Organ Shape by Combinatorial Gene Activity

被引:42
作者
Cui, Min-Long [1 ]
Copsey, Lucy [1 ]
Green, Amelia A. [1 ]
Bangham, J. Andrew [2 ]
Coen, Enrico [1 ]
机构
[1] John Innes Ctr, Dept Cell & Dev Biol, Norwich, Norfolk, England
[2] Univ E Anglia, Sch Comp Sci, Norwich NR4 7TJ, Norfolk, England
基金
英国生物技术与生命科学研究理事会;
关键词
ANTIRRHINUM-MAJUS; FLORAL ASYMMETRY; DROSOPHILA-MELANOGASTER; CELL-DIFFERENTIATION; WING SHAPE; EVOLUTION; FLOWERS; GROWTH; TRANSFORMATION; PROTEIN;
D O I
10.1371/journal.pbio.1000538
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
The development of organs with particular shapes, like wings or flowers, depends on regional activity of transcription factors and signalling molecules. However, the mechanisms that link these molecular activities to the morphogenetic events underlying shape are poorly understood. Here we describe a combination of experimental and computational approaches that address this problem, applying them to a group of genes controlling flower shape in the Snapdragon (Antirrhinum). Four transcription factors are known to play a key role in the control of floral shape and asymmetry in Snapdragon. We use quantitative shape analysis of mutants for these factors to define principal components underlying flower shape variation. We show that each transcription factor has a specific effect on the shape and size of regions within the flower, shifting the position of the flower in shape space. These shifts are further analysed by generating double mutants and lines that express some of the genes ectopically. By integrating these observations with known gene expression patterns and interactions, we arrive at a combinatorial scheme for how regional effects on shape are genetically controlled. We evaluate our scheme by incorporating the proposed interactions into a generative model, where the developing flower is treated as a material sheet that grows according to how genes modify local polarities and growth rates. The petal shapes generated by the model show a good quantitative match with those observed experimentally for each petal in numerous genotypes, thus validating the hypothesised scheme. This article therefore shows how complex shapes can be accounted for by combinatorial effects of transcription factors on regional growth properties. This finding has implications not only for how shapes develop but also for how they may have evolved through tinkering with transcription factors and their targets.
引用
收藏
页数:12
相关论文
共 33 条
[1]  
Almeida J, 1997, DEVELOPMENT, V124, P1387
[2]   Diversification and co-option of RAD-like genes in the evolution of floral asymmetry [J].
Baxter, Catherine E. L. ;
Costa, Maria Manuela R. ;
Coen, Enrico S. .
PLANT JOURNAL, 2007, 52 (01) :105-113
[3]   BINARY AGROBACTERIUM VECTORS FOR PLANT TRANSFORMATION [J].
BEVAN, M .
NUCLEIC ACIDS RESEARCH, 1984, 12 (22) :8711-8721
[4]   Networks in leaf development [J].
Byrne, ME .
CURRENT OPINION IN PLANT BIOLOGY, 2005, 8 (01) :59-66
[5]   COMPARISON OF GENETIC BEHAVIOR OF THE TRANSPOSABLE ELEMENT TAM3 AT 2 UNLINKED PIGMENT LOCI IN ANTIRRHINUM-MAJUS [J].
CARPENTER, R ;
MARTIN, C ;
COEN, ES .
MOLECULAR & GENERAL GENETICS, 1987, 207 (01) :82-89
[6]   Floral asymmetry involves an interplay between TO and MYB transcription factors in Antirrhinum [J].
Corley, SB ;
Carpenter, R ;
Copsey, L ;
Coen, E .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (14) :5068-5073
[7]   Evolution of regulatory interactions controlling floral asymmetry [J].
Costa, MMR ;
Fox, S ;
Hanna, AI ;
Baxter, C ;
Coen, E .
DEVELOPMENT, 2005, 132 (22) :5093-5101
[8]   CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of antirrhinum [J].
Crawford, BCW ;
Nath, U ;
Carpenter, R ;
Coen, ES .
PLANT PHYSIOLOGY, 2004, 135 (01) :244-253
[9]   An improved protocol for Agrobacterium-mediated transformation of Antirrhinum majus L. [J].
Cui, ML ;
Handa, T ;
Ezura, H .
MOLECULAR GENETICS AND GENOMICS, 2003, 270 (04) :296-302
[10]   The Ultrabithorax Hox gene of Drosophila controls haltere size by regulating the Dpp pathway [J].
de Navas, Luis F. ;
Garaulet, Daniel L. ;
Sanchez-Herrero, Ernesto .
DEVELOPMENT, 2006, 133 (22) :4495-4506