Compartmentalized expression patterns of pancreatic- and gastric-related genes in the alimentary canal of the ascidian Ciona intestinalis: evolutionary insights into the functional regionality of the gastrointestinal tract in Olfactores.

Abstract

Many heterotrophic animals have a one-way alimentary canal that is essential for their nutrition and sequential steps of the digestive system, namely ingestion, digestion, absorption and elimination, are widely shared among bilaterians. Morphological, functional and molecular knowledge of the alimentary canal has been obtained in particular from mammalian research but the shared features and evolution of these aspects of the highly diverged alimentary canal in the animal kingdom are still unclear. We therefore investigate spatial gene expression patterns of pancreatic- and gastric-related molecules of ascidians (a sister group of vertebrates) with special reference to the functional regionality of the gastrointestinal tract. Genome-wide surveys of ascidian homologs to mammalian exocrine digestive enzyme genes revealed that pancreatic enzymes, namely alpha-amylase, lipase, phospholipase A2, trypsin, chymotrypsin and carboxypeptidase, exist in the ascidian genome. However, an ascidian homolog of the mammalian gastric enzyme pepsin has not been identified, although molecules resembling cathepsin D, a pepsin relative, are indeed present. Spatial expression analyses in the ascidian Ciona intestinalis, by means of whole-mount in situ hybridization, have elucidated that the expression of Ciona homologs of pancreatic- and gastric-related exocrine enzyme genes and of their transcriptional regulator genes is restricted to the Ciona stomach. Furthermore, the expression of these genes is localized to specific regions of the stomach epithelium according to their regionality in the vertebrate digestive system. The compartmentalized expression patterns of Ciona homologs imply primitive and/or ancestral aspects of molecular, functional and morphological bases among Olfactores.