Identification and developmental expression of two Tbx1/10-related genes in the agnathan Lethenteron japonicum

Abstract

We have identified two Tbx1/10-related genes, LjTbx1/10A and LjTbx1/10B, from the Japanese river lamprey Lethenteron japonicum. We used in situ hybridization to characterize their expression pattern during embryonic development. LjTbx1/10A and LjTbx1/10B shared common expression in the pharyngeal arches and otic vesicle, although their levels and timing of expression differed markedly. LjTbx1/10A was highly expressed in the mesodermal core of pharyngeal arches and the adjacent endoderm throughout pharyngeal arch development, whereas LjTbx1/10B expression was only transiently upregulated in forming pharyngeal pouches. LjTbx1/10A transcripts first appeared at stage 25 in otic vesicles, whereas LjTbx1/10B transcripts could already be detected in the developing otic placode at stage 20. These results suggest that lamprey LjTbx1/10A and LjTbx1/10B may play distinct roles in the patterning and development of the pharyngeal apparatus. It appears that lamprey Tbx1/10 genes have undergone subfunctionalization independent from gnathostomes, with regard to both regulation and function.

Evolution and development of the fish jaw skeleton

“…Although modern lampreys and hagfishes have very derived pharyngeal structures associated with their rasping feeding strategies, they provide a useful model out‐group to explore the origins of pharyngeal patterning in gnathostomes. Lampreys express factors associated with pharyngeal arch patterning including Pax1/9 and Tbx1/10 consistent with other ancestral chordates (Ogasawara et al, ; Tiecke et al, ), but as vertebrates, also have true cranial neural crest migrating into arches (Horigome et al, ). Studies of lamprey larvae indicate that some differences in neural crest‐cell migration compared to gnathostomes.…”

A new heart for a new head in vertebrate cardiopharyngeal evolution

“…3). Moreover, lamprey embryos express homologues of Isl1 , Nkx2-5 and Tbx1 in seemingly overlapping anterior and ventral mesodermal domains 58–61 , comparable with the patterns of their homo-logues in the amniote CPF. Interestingly, the emergence of heterogeneous head-muscle groups at the base of vertebrates coincided with the emergence of chambered hearts 62,63 (Fig.…”

An eye on the head: the development and evolution of craniofacial muscles

“…Taken together, these findings suggest that the cell population and the genetic machinery that distinguish head muscles from those of somitic mesoderm origin might have existed, in part, long before the evolution of the vertebrate head. Concordantly, in the basal jawless vertebrate lamprey, Tbx1/10 is expressed in the mesodermal core of the PAs (Sauka-Spengler et al, 2002;Tiecke et al, 2007), as well as in the labial and velar (mandibular arch-derived muscles) muscle progenitors. Furthermore, although Caenorhabditis elegans tbx-2 is not closely related to murine Tbx1 (Larroux et al, 2008), it was shown that tbx-2 is required for the development of the C. elegans pharyngeal muscles, but only those located anteriorly (Smith and Mango, 2007).…”