Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
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DOI：
10.1371/journal.pbio.1001028
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发表时间：
2011-03
期刊：
影响因子：
9.8
通讯作者：
Headon DJ
中科院分区：
文献类型：
--
作者：
Mou C;Pitel F;Gourichon D;Vignoles F;Tzika A;Tato P;Yu L;Burt DW;Bed'hom B;Tixier-Boichard M;Painter KJ;Headon DJ
脊椎动物皮肤的特点是它的图案阵列的附属物，无论是羽毛，毛发，或鳞片。在鸟类皮肤中，羽毛的分布发生在两个不同的空间水平上。在离散的区域内的羽毛的排列，以及位于区域之间的裸露皮肤，被称为宏观图案，而个体羽毛之间的较小尺度的周期性间隔被称为微观图案。在发育过程中，在这两个尺度上运作的图案化机制之间的整合程度以及皮肤宏观图案的显著进化性的机制尚不清楚。宏观模式变异的一个突出例子是多个物种颈部羽毛的趋同损失，这是一种与野生和家养鸟类耐热性相关的特征。在鸡中，一种称为裸颈的突变的特征是身体羽毛减少和完全裸露的脖子。在这里，我们进行遗传精细定位的致病区域，并确定一个大的插入与裸颈性状。一个强有力的候选基因在关键的时间间隔，BMP 12/GDF 7，显示显着升高的表达在裸颈胚胎皮肤由于顺式调节作用的致病突变。BMP家族成员通过反应扩散机制抑制胚胎羽毛的形成，我们发现颈部皮肤选择性地产生视黄酸增强了BMP信号传导，使颈部皮肤比身体皮肤对羽毛发育的抑制更敏感。这种由颈部皮肤选择性产生的视黄酸构成了一种隐蔽的模式，因为它对羽化的影响直到总的BMP水平改变才被揭示出来。颈部和身体皮肤的这种发育模块性允许BMP水平的简单定量变化，以产生稀疏的羽毛或裸露的颈部，同时保持身体上强健的羽毛图案。毛发或羽毛在身体上的分布并不均匀，许多动物的皮肤上都有特征性的区域，要么覆盖丰富，要么覆盖减少。这些特征，如鬃毛、冠或秃斑，在不同的物种中都可以看到，这表明它们可以是选择性的优势，而且皮肤发育的机制以某种方式使这些特征在进化过程中反复出现。在这项研究中，我们探讨了颈部羽毛脱落的基础，这是一个与耐热性相关的特征，在鸟类进化过程中独立出现过几次。我们发现，鸡的裸颈是由BMP的产生增加引起的，BMP是以前与确定相邻羽毛之间间隙大小有关的因素。胚胎颈部皮肤选择性产生视黄酸增强BMP信号传导，从而使该皮肤区域接近完全抑制羽毛发育所需的BMP作用阈值。颈部和身体皮肤之间的这种通常无害的区别使突变能够增加BMP的作用，使颈部完全裸露，同时允许身体上正常的羽毛。因此，皮肤内的底层地图提供了一个通向裸露颈部的一步路线。
Vertebrate skin is characterized by its patterned array of appendages, whether feathers, hairs, or scales. In avian skin the distribution of feathers occurs on two distinct spatial levels. Grouping of feathers within discrete tracts, with bare skin lying between the tracts, is termed the macropattern, while the smaller scale periodic spacing between individual feathers is referred to as the micropattern. The degree of integration between the patterning mechanisms that operate on these two scales during development and the mechanisms underlying the remarkable evolvability of skin macropatterns are unknown. A striking example of macropattern variation is the convergent loss of neck feathering in multiple species, a trait associated with heat tolerance in both wild and domestic birds. In chicken, a mutation called Naked neck is characterized by a reduction of body feathering and completely bare neck. Here we perform genetic fine mapping of the causative region and identify a large insertion associated with the Naked neck trait. A strong candidate gene in the critical interval, BMP12/GDF7, displays markedly elevated expression in Naked neck embryonic skin due to a cis-regulatory effect of the causative mutation. BMP family members inhibit embryonic feather formation by acting in a reaction-diffusion mechanism, and we find that selective production of retinoic acid by neck skin potentiates BMP signaling, making neck skin more sensitive than body skin to suppression of feather development. This selective production of retinoic acid by neck skin constitutes a cryptic pattern as its effects on feathering are not revealed until gross BMP levels are altered. This developmental modularity of neck and body skin allows simple quantitative changes in BMP levels to produce a sparsely feathered or bare neck while maintaining robust feather patterning on the body. The distribution of hairs or feathers across the body is not homogeneous, and many animals have characteristic regions of their skin with either profuse or reduced coverage. These features, such as manes, crests, or bald patches, are seen in diverse species, suggesting that they can be selectively advantageous and also that the mechanisms by which the skin develops somehow enables such features to appear repeatedly in the course of evolution. In this study we explore the basis of loss of neck feathering, a feature associated with heat tolerance that has arisen independently several times during bird evolution. We find that in chickens a bare neck is caused by increased production of BMPs, factors previously implicated in defining the size of the gaps between neighboring feathers. Selective production of retinoic acid by embryonic neck skin enhances BMP signaling, thereby bringing this skin region close to the threshold of BMP action required to completely suppress feather development. This usually innocuous distinction between neck and body skin enables mutations that increase BMP action to render the neck completely bare while permitting normal feathering on the body. Thus an underlying map within the skin provides a one-step route to a bare neck.
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