The genus Acipenser as a model system for vertebrate urogenital development: nephrostomial tubules and their significance for the origin of the gonad

Abstract 

Early gonadal development was studied in the sterlet, Acipenser ruthenus, by means of histological and semithin serial sections and scanning electron microscopy. Special attention was given to the role of opisthonephric nephrostomial tubules and their coelomic funnels (nephrostomes, coelomostomes) in the origin of the gonad. Specimens of about 1 mm in length (about 7 days post hatching) have a continuous kidney complex (holonephros) that extends from the branchial region to the level of the cloaca and may be divided into a cranial pronephros and a caudally following opisthonephros, with no overlapping of either portion. In specimens of 10 to 25 mm in length the regression of pronephros and cranial opisthonephros can already been seen; as a consequence, these parts of the kidney complex are not involved in gonadogenesis. The initial gonadal anlage is seen in specimens of 30–40 mm in length. The somatic cells of the gonadal primordium develop from the medial lips of segmentally arranged opisthonephric nephrostomes situated in a line that extends from the level of the stomach through that of the spiral valve. The nephrostomes involved in this process belong to the first-order set of nephrons, since nephrons of higher order that arise continuously from blastema cells during further growth of the animals never send nephrostomial tubules to the coelomic surface. The cells of the medial nephrostomial lips proliferate by many mitoses. They grow over and surround the large germ cells that have accumulated on the medial side of the nephrostomes. The proliferating nephrostomial cells are elongated in shape, and their long axes are oriented in the cranio-caudal direction. By their size, shape and arrangement they replace not only the flat, polygonal, mesothelial cells of lateral plate origin on the medial side of the nephrostomes, but also those in the interstices in between. The result is the formation of a continuous gonadal crest situated medially from the nephrostomial line. At 100–130 mm in length, the gonadal crest has reached the stage of a gonadal fold that is attached to the dorsal body wall by a thin mesogonadium. Stroma cells and blood vessels start to invade the gonadal fold. At 240–290 mm in length, parts of the gonadal fold are converted into a fat body, a structure that is typically present in adult sturgeons of either sex. Nephrostomial tubules and their nephrostomes are visible only for a short period in Acipenser ruthenus. They are completely developed in specimens of 25–40 mm in length and start continuous retrogression immediately afterwards. Therefore, they cannot play an important role in excretion. Their only purpose apparently is to function as precursor tissue for other organs, such as the gonad, in establishing a route by which cells of the intermediate mesoderm can gain access to and spread out over the coelomic surface. In conclusion, the observations made in Acipenser prove that this species is a most suitable model to explain the origin of the gonad from opistho/mesonephric nephrostomial tubules in vertebrates with a less-developed or early regressing pronephros. Most mammals, including man, belong to this category.