Sorbonne Université, CNRS, Biologie Intégrative Des Organismes Marins (BIOM), Banyuls/Mer, 66650, France.
Present address: Laboratory of Developmental Neurobiology, Department of Biology, KU Leuven, Louvain, Belgium.
BMC Biol. 2024 Apr 2;22(1):74. doi: 10.1186/s12915-024-01872-7.
The tunicates form a group of filter-feeding marine animals closely related to vertebrates. They share with them a number of features such as a notochord and a dorsal neural tube in the tadpole larvae of ascidians, one of the three groups that make tunicates. However, a number of typical chordate characters have been lost in different branches of tunicates, a diverse and fast-evolving phylum. Consequently, the tunic, a sort of exoskeleton made of extracellular material including cellulose secreted by the epidermis, is the unifying character defining the tunicate phylum. In the larva of ascidians, the tunic differentiates in the tail into a median fin (with dorsal and ventral extended blades) and a caudal fin.
Here we have performed experiments in the ascidian Phallusia mammillata to address the molecular control of tunic 3D morphogenesis. We have demonstrated that the tail epidermis medio-lateral patterning essential for peripheral nervous system specification also controls tunic elongation into fins. More specifically, when tail epidermis midline identity was abolished by BMP signaling inhibition, or CRISPR/Cas9 inactivation of the transcription factor coding genes Msx or Klf1/2/4/17, median fin did not form. We postulated that this genetic program should regulate effectors of tunic secretion. We thus analyzed the expression and regulation in different ascidian species of two genes acquired by horizontal gene transfer (HGT) from bacteria, CesA coding for a cellulose synthase and Gh6 coding for a cellulase. We have uncovered an unexpected dynamic history of these genes in tunicates and high levels of variability in gene expression and regulation among ascidians. Although, in Phallusia, Gh6 has a regionalized expression in the epidermis compatible with an involvement in fin elongation, our functional studies indicate a minor function during caudal fin formation only.
Our study constitutes an important step in the study of the integration of HGT-acquired genes into developmental networks and a cellulose-based morphogenesis of extracellular material in animals.
被囊动物是一组滤食性海洋动物，与脊椎动物关系密切。它们在尾索动物的幼体中有一些共同的特征，如脊索和背侧神经管，尾索动物是被囊动物的三个组成部分之一。然而，在被囊动物的不同分支中，许多典型的脊索动物特征已经丢失，被囊动物是一个多样化和快速进化的门。因此，被囊，一种由细胞外物质组成的外骨骼，包括由表皮分泌的纤维素，是定义被囊动物门的统一特征。在尾索动物的幼虫中，被囊在尾部分化为一个中鳍（有背侧和腹侧延伸的叶片）和一个尾鳍。
在这里，我们在 Phallusia mammillata 海鞘中进行了实验，以解决 3D 被囊形态发生的分子控制问题。我们证明了对周围神经系统特化至关重要的尾部表皮中-侧模式也控制着被囊向鳍的伸长。更具体地说，当 BMP 信号抑制或 CRISPR/Cas9 失活转录因子编码基因 Msx 或 Klf1/2/4/17 时，尾部表皮的中线身份被废除，中鳍就不会形成。我们推测这个遗传程序应该调节被囊分泌的效应物。因此，我们分析了两个通过水平基因转移（HGT）从细菌获得的基因在不同的海鞘物种中的表达和调节，CesA 编码纤维素合酶，Gh6 编码纤维素酶。我们揭示了这些基因在被囊动物中的一个意想不到的动态历史，以及在海鞘中基因表达和调节的高度可变性。尽管在 Phallusia 中，Gh6 在表皮中有一个区域化的表达，与鳍的伸长有关，但我们的功能研究表明，它在尾鳍形成中仅起次要作用。
我们的研究是研究水平基因转移获得的基因如何整合到发育网络中以及动物细胞外物质的纤维素基形态发生的重要一步。
