Genetic control of organ shape and tissue polarity.

Genetic control of organ shape and tissue polarity.
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DOI:
10.1371/journal.pbio.1000537
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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
Coen E
中科院分区:
生物学1区
文献类型:
--
作者:
Green AA;Kennaway JR;Hanna AI;Bangham JA;Coen E

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实验分析和数学建模相结合,展示了组织极性的遗传控制如何在形态的发展和进化中发挥基础性作用。人们对基因控制器官形状的机制知之甚少。原则上,基因可以通过改变局部变形速率和/或方向来控制形状。由于模式、方向和生长过程中的机械约束之间的相互作用,区分这些可能性一直很困难。在这里,我们展示了如何结合生长分析、分子遗传学和建模来分析影响形状的因素。以金鱼草为例,我们展示了形状发育如何反映组织生长的局部速率和方向,这些速度和方向在空间和时间上变化,形成一个动态的生长场。这一生长区域受几个影响花形的背腹基因的控制。这些基因的作用可以通过假设它们调节与局部取向平行或垂直的特定生长速率来模拟,局部取向是由几个组织极性的关键组织者建立的。背腹基因只影响特定生长速度的模型不能完全解释观察到的生长领域和形状。然而,这些数据可以很容易地用一个模型来解释,在这个模型中,背腹基因也改变了组织极性的组织者。特别是,腹侧花瓣连接处和远端边界的组织极性组织者的遗传控制使得野生型和突变体都可以解释花的形状和生长场。结果表明,组织极性组织者的遗传控制在形状的发展和进化中发挥了关键作用。众所周知,基因可以控制花、心脏和四肢等生物结构的形状,但人们对基因如何做到这一点知之甚少。一个可行的假说是,基因通过调节生长组织变形的局部速率来控制形状。然而,由于生长和变形组织中发生的动态相互作用,评估这一想法一直很困难。为了解决这个问题,我们使用了实验和数学建模相结合的方法来研究基因如何控制骁龙花的形状。这个系统的优点是,拥有定义明确的影响形状的基因,并且可以进行生长分析。我们首先尝试用基因影响局部组织生长速度的模型来解释实验数据。虽然这个模型可以捕捉到花发育的许多方面,但它没有考虑到一些关键特征。如果基因也影响由组织极性组织者建立的指导生长的内部定向场,那么这些就可以最容易地解释。因此,我们的分析揭示了形状基因在组织极性控制中以前未曾被怀疑的作用,强调了这一过程对组织形式发展和进化的重要性。
A combination of experimental analysis and mathematical modelling shows how the genetic control of tissue polarity plays a fundamental role in the development and evolution of form. The mechanisms by which genes control organ shape are poorly understood. In principle, genes may control shape by modifying local rates and/or orientations of deformation. Distinguishing between these possibilities has been difficult because of interactions between patterns, orientations, and mechanical constraints during growth. Here we show how a combination of growth analysis, molecular genetics, and modelling can be used to dissect the factors contributing to shape. Using the Snapdragon (Antirrhinum) flower as an example, we show how shape development reflects local rates and orientations of tissue growth that vary spatially and temporally to form a dynamic growth field. This growth field is under the control of several dorsoventral genes that influence flower shape. The action of these genes can be modelled by assuming they modulate specified growth rates parallel or perpendicular to local orientations, established by a few key organisers of tissue polarity. Models in which dorsoventral genes only influence specified growth rates do not fully account for the observed growth fields and shapes. However, the data can be readily explained by a model in which dorsoventral genes also modify organisers of tissue polarity. In particular, genetic control of tissue polarity organisers at ventral petal junctions and distal boundaries allows both the shape and growth field of the flower to be accounted for in wild type and mutants. The results suggest that genetic control of tissue polarity organisers has played a key role in the development and evolution of shape. Genes are known to control the shape of biological structures, like flowers, hearts, and limbs, yet how they do this is poorly understood. A working hypothesis is that genes control shape by modulating local rates at which growing tissue deforms. Evaluating this idea has been difficult, however, because of the dynamic interactions that occur within growing and deforming tissue. To address this problem, we used a combination of experimental and mathematical modelling approaches to study how genes control shape in the Snapdragon flower. This system has the advantages of having well defined genes that influence shape and being accessible to growth analysis. We first tried to explain the experimental data with a model in which genes influence local rates of tissue growth. While this model could capture many aspects of flower development, it failed to account for some key features. These could be most readily explained if genes also affect an internal field of orientations along which growth is directed, established by organisers of tissue polarity. Our analysis therefore revealed a previously unsuspected role of shape genes in the control of tissue polarity, highlighting the importance of this process for the development and evolution of tissue forms.
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