Quantitative control of organ shape by combinatorial gene activity.
Quantitative control of organ shape by combinatorial gene activity.
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DOI：
10.1371/journal.pbio.1000538
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发表时间：
2010-11-09
期刊：
影响因子：
9.8
通讯作者：
Coen E
中科院分区：
文献类型：
--
作者：
Cui ML;Copsey L;Green AA;Bangham JA;Coen E
分子遗传学，形状分析和计算建模的新组合显示了Snapdragon花的复杂三维形状如何通过局部基因活动产生。具有特定形状的器官的发育，如翅膀或花朵，取决于转录因子和信号分子的区域活动。然而，将这些分子活动与形状相关的形态发生事件联系起来的机制却知之甚少。在这里，我们描述了一个实验和计算的方法来解决这个问题的组合，将它们应用到一组基因控制花的形状在金鱼草（金鱼草）。已知四种转录因子在控制金鱼草花的形状和不对称性中起关键作用。我们使用这些因素的突变体的定量形状分析，以确定基本的花形变化的主成分。我们发现，每个转录因子对花内区域的形状和大小有特定的影响，改变花在形状空间中的位置。通过产生异位表达某些基因的双突变体和品系进一步分析这些转变。通过将这些观察结果与已知的基因表达模式和相互作用相结合，我们得出了一个组合方案，说明区域对形状的影响是如何遗传控制的。我们评估我们的计划，将建议的相互作用到生成模型，在那里发育中的花被视为一个材料片，根据基因如何修改本地极性和增长率的增长。该模型产生的花瓣形状显示出良好的定量匹配与实验观察到的每个花瓣在许多基因型，从而验证了假设的计划。因此，本文展示了如何复杂的形状可以占区域生长特性的转录因子的组合效应。这一发现不仅对形状如何发展有意义，而且对它们如何通过修补转录因子及其靶点而进化也有意义。发育生物学的一个主要挑战是了解基因活动模式如何转化为复杂的三维形式，如心脏，翅膀或花朵。解决这个问题并不容易，部分原因是难以量化基因对形状的影响，也因为我们缺乏框架，可以评估潜在机制的假设。在这里，我们解决这个问题，通过实验和计算方法相结合，使用Snapdragon花作为模型系统。通过量化这些花的形状在一系列的突变体与特定基因的活性降低或增加，我们展示了复杂的花的形状取决于基因的方式在每个花瓣区域的组合。建议的相互作用进行了测试，将它们纳入一个计算模型的成长花。定量比较表明，模型产生的形状和实验观察到的形状之间有很好的一致性，证实了我们的基本假设。Snapdragon花，其紧密贴合的上下花瓣，已经进化成为一种专门针对传粉者的机制。我们的文章展示了这些形式的发展和进化可能是通过自然修补基因对生长的局部影响而产生的。
A novel combination of molecular genetics, shape analysis, and computational modelling shows how the complex three-dimensional shape of the Snapdragon flower can arise through local gene activity. 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. A major challenge in developmental biology is to understand how patterns of gene activity are translated into complex three-dimensional forms, like hearts, wings, or flowers. Addressing this problem has not been easy, partly because of the difficulties in quantifying the effects of genes on shape and also because we lack frameworks that allow hypotheses about underlying mechanisms to be evaluated. Here we address this issue through a combination of experimental and computational approaches, using the Snapdragon flower as a model system. By quantifying the shapes of these flowers in a range of mutants with reduced or increased activity of particular genes, we show how the complex floral shape depends on the way genes act in combination in each petal region. The proposed interactions were tested by incorporating them into a computational model of the growing flower. Quantitative comparisons reveal a good agreement between the shapes generated by the model and those observed experimentally, confirming our underlying hypothesis. The Snapdragon flower, with its tightly fitting upper and lower petals, has evolved as a specialised mechanism for targeting pollinators. Our article shows how the development and evolution of such forms may have arisen by natural tinkering with the local effects of genes on growth.
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