Department of Biological Sciences, Carnegie Mellon University, 4400 5th Avenue, Pittsburgh, PA, 15213, USA.
Evodevo. 2012 Aug 9;3(1):17. doi: 10.1186/2041-9139-3-17.
The mechanisms by which the conserved genetic "toolkit" for development generates phenotypic disparity across metazoans is poorly understood. Echinoderm larvae provide a great resource for understanding how developmental novelty arises. The sea urchin pluteus larva is dramatically different from basal echinoderm larval types, which include the auricularia-type larva of its sister taxon, the sea cucumbers, and the sea star bipinnaria larva. In particular, the pluteus has a mesodermally-derived larval skeleton that is not present in sea star larvae or any outgroup taxa. To understand the evolutionary origin of this structure, we examined the molecular development of mesoderm in the sea cucumber, Parastichopus parvimensis.
By comparing gene expression in sea urchins, sea cucumbers and sea stars, we partially reconstructed the mesodermal regulatory state of the echinoderm ancestor. Surprisingly, we also identified expression of the transcription factor alx1 in a cryptic skeletogenic mesenchyme lineage in P. parvimensis. Orthologs of alx1 are expressed exclusively within the sea urchin skeletogenic mesenchyme, but are not expressed in the mesenchyme of the sea star, which suggests that alx1+ mesenchyme is a synapomorphy of at least sea urchins and sea cucumbers. Perturbation of Alx1 demonstrates that this protein is necessary for the formation of the sea cucumber spicule. Overexpression of the sea star alx1 ortholog in sea urchins is sufficient to induce additional skeleton, indicating that the Alx1 protein has not evolved a new function during the evolution of the larval skeleton.
The proposed echinoderm ancestral mesoderm state is highly conserved between the morphologically similar, but evolutionarily distant, auricularia and bipinnaria larvae. However, the auricularia, but not bipinnaria, also develops a simple skelotogenic cell lineage. Our data indicate that the first step in acquiring these novel cell fates was to re-specify the ancestral mesoderm into molecularly distinct territories. These new territories likely consisted of only a few cells with few regulatory differences from the ancestral state, thereby leaving the remaining mesoderm to retain its original function. The new territories were then free to take on a new fate. Partitioning of existing gene networks was a necessary pre-requisite to establish novelty in this system.
后生动物中保守的发育“工具包”是如何产生表型差异的，这一机制还不太清楚。棘皮动物幼虫为理解发育新颖性的产生提供了很好的资源。海胆幼体与基础棘皮动物幼虫类型（包括其姐妹类群海参的耳状幼虫和海星的双腕幼虫）有很大的不同。特别是，幼体具有中胚层衍生的幼虫骨骼，而海星幼虫或任何外群类群都没有这种骨骼。为了了解这种结构的进化起源，我们研究了海参 Parastichopus parvimensis 中中胚层的分子发育。
通过比较海胆、海参和海星中的基因表达，我们部分重建了棘皮动物祖先的中胚层调控状态。令人惊讶的是，我们还在 P. parvimensis 的一个隐式骨骼发生间质谱系中鉴定到了转录因子 alx1 的表达。alx1 的同源物仅在海胆的骨骼发生间质中表达，但在海星的间质中不表达，这表明 alx1+间质是至少海胆和海参的一个共衍征。Alx1 的扰动表明该蛋白对于海参刺的形成是必需的。海星 alx1 同源物在海胆中的过表达足以诱导额外的骨骼，表明在幼虫骨骼的进化过程中，Alx1 蛋白没有进化出新的功能。
在形态相似但进化距离较远的耳状幼虫和双腕幼虫之间，所提出的棘皮动物祖先中胚层状态高度保守。然而，耳状幼虫但不是双腕幼虫也发育出一个简单的骨骼发生细胞谱系。我们的数据表明，获得这些新细胞命运的第一步是将祖先中胚层重新指定为分子上不同的区域。这些新区域可能只包含少数几个细胞，与祖先状态的差异很小，从而使剩余的中胚层保留其原始功能。然后，这些新区域可以自由地承担新的命运。现有基因网络的分区是该系统建立新颖性的必要前提。
