期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：51
DOI：10.1073/pnas.2114563118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
The tetrapod vertebral skeleton is subdivided into distinct regions that are determined by spatial expression of
Hox genes in the early embryo. Fishes are thought to lack comparable regionalization, but the relationship between anatomy and
hox expression has not been tested beyond tetrapods. By comparing vertebral morphology with embryonic
hox expression in a cartilaginous fish, the skate (
Leucoraja erinacea), we found that the skate vertebral column is regionalized, with regional transitions predicted by embryonic
hox gene expression patterns. This discovery points to an origin of nested
hox gene expression and
hox-based vertebral regionalization at the common ancestor of jawed vertebrates.
The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of
Hox5/6,
-9,
-10, and
-11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of
Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of
hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (
Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of
hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of
hox5/6,
hox9,
hox10, and
hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that
hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.
