Transcriptional Analysis of the Endostyle Reveals Pharyngeal Organ Functions in Ascidian

Abstract

The endostyle is a pharyngeal organ with an opening groove and cilia in invertebrate chordates (amphioxus and ascidian) and cyclostomate (lamprey), serving as a filter-feeding tract and thyroid-secreting location. Emerging evidence implies its complex cellular composition and potentially versatile functions. Multiple cell types in the endostyle have been thought to be progenitors of complex organs in advanced vertebrates. To describe the expression profile and the potential functions, bulk RNA sequencing on the endostyle in ascidian Styela clava was conducted and distinct markers were selected by multileveled comparative analysis. Transcriptional data assay and qRT-PCR-verified results showed the regional expression patterns of Hox genes in the longitudinal axis. Organ-specific markers of the endostyle was proposed by comparing expression with the main organs of the ascidian. A cross-species transcriptional profile projection between the endostyle and organs from Danio rerio and Homo sapiens indicates a robust homogenous relationship to the thyroid and digestive system of the endostyle. The high similarity between the endostyle and the head kidney in zebrafish/the bone marrow in human implies uniquely profound functions of the pharyngeal organ in proto-vertebrates. Our result revealed that the transcriptional profile of the human parathyroid gland was similar to the ascidian endostyle, indicating the evolutionary origin of vertebrate hormone secretion organs.

Spatially resolved single-cell atlas of ascidian endostyle provides insight into the origin of vertebrate pharyngeal organs

“…1B). Although the gene expression pattern along the endostyle longitudinal axis showed a considerable homogeneity, several Hox genes were exceptions ( 35 ). To identify the cell components and potential vertebrate homologs in the endostyle, we established a spatially resolved atlas at single-cell resolution (Fig.…”

“…The updated version of the gene structural annotation was released on EDomics, a multi-omics database for animal evo-devo ( 66 ). scRNA-seq and Stereo-seq identified 18,685 and 11,912 genes, respectively, compared with the bulk RNA-sequencing results (11,083 genes from bulk RNA-sequencing) ( 35 ) (fig. S3, G and H, and data S5), which, to some extent, exhibited differences among the techniques.…”

“…Adults S. clava were purchased from the Xunshan Company in Weihai, China, and temporarily preserved in a circulating aquarium system within the laboratory at 18°C, equipped with air pumps. The endostyle of healthy individuals was gently dissected using disinfected instruments as the previous description ( 35 ). All guidelines for animal experiments were approved by the Institutional Animal Care and Use Committee of Ocean University of China (OUC-IACUC), with approval numbers 2020-0032-0517 and 2023-0032-0039.…”

Single-cell transcriptomic profiling of the whole colony ofBotrylloides diegensis: Insights into tissue specialization and blastogenesis

“…5A). In Styela, Itnl1/Fcn1 mRNAs were enriched in clusters 8 and 3 and zones 6 and 7 of the endostyle (Jiang et al, 2023). Muc5a and VWF transcripts were found in Clusters 3 and 10 (Sasaki et al, 2003;Yamagishi et al, 2022).…”

“…5D). This region of the endostyle functions with zone 7 in immune activities, with high iodine and peroxidase activities (Jiang et al, 2023;Sasaki et al, 2003) (Alesci et al, 2022). Iodine metabolism has been linked to thyroid gland evolution (Fujita and Nanba, 1971).…”