Evolution of OTP-independent larval skeleton patterning in the direct-developing sea urchin, Heliocidaris erythrogramma.
Heliocidaris erythrogramma is a direct-developing sea urchin that has evolved a modified ontogeny, a reduced larval skeleton, and accelerated development of the adult skeleton. The Orthopedia gene (Otp) encodes a homeodomain transcription factor crucial in patterning the larval skeleton of indirect-developing sea urchins. We compare the role of Otp in larvae of the indirect-developing sea urchin Heliocidaris tuberculata and its direct-developing congener H. erythrogramma. Otp is a single-copy gene with an identical protein sequence in these species. Expression of Otp is initiated by the late gastrula, initially in two cells of the oral ectoderm in H. tuberculata. These cells are restricted to oral ectoderm and exhibit left-right symmetry. There are about 266 copies of Otp mRNA per Otp- expressing cell in H. tuberculata. We tested OTP function in H. tuberculata and H. erythrogramma embryos by microinjection of Otp mRNA. Mis-expression of Otp mRNA in H. tuberculata radialized the embryos and caused defects during larval skeletogenesis. Mis-expression of Otp mRNA in H. erythrogramma embryos did not affect skeleton formation. This is consistent with the observation by in situ hybridization of no concentration of Otp transcript in any particular cells or region of the H. erythrogramma larva, and measurement of a level of less than one copy of endogenous Otp mRNA per cell in H. erythrogramma. OTP plays an important role in patterning the larval skeleton of H. tuberculata, but this role apparently has been lost in the evolution of the H. erythrogramma larva, and replaced by a new patterning mechanism.
Zhou
Na
N
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
Wilson
Keen A
KA
Andrews
Mary E
ME
Kauffman
Jeffery S
JS
Raff
Rudolf A
RA
D000818:Animals; D015139:Blotting, Southern; D019521:Body Patterning / Q000235:genetics*; D017931:DNA Primers; D004625:Embryo, Nonmammalian / Q000033:anatomy & histology; D018507:Gene Expression Regulation, Developmental; D006652:Histological Techniques; D018398:Homeodomain Proteins / Q000235:genetics; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008845:Microinjections; D009419:Nerve Tissue Proteins / Q000235:genetics*; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012617:Sea Urchins / Q000196:embryology* / Q000235:genetics*
D017931:DNA Primers; D018398:Homeodomain Proteins; D009419:Nerve Tissue Proteins; D012333:RNA, Messenger