Unusual gene order and organization of the sea urchin hox cluster

Cameron, R. Andrew; Rowen, Lee; Nesbitt, Ryan; Bloom, Scott; Rast, Jonathan P.; Berney, Kevin; Arenas-Mena, César; Martinez, Pedro; Lucas, Susan; Richardson, Paul M.; Davidson, Eric H.; Peterson, Kevin J.; Hood, Leroy

doi:10.1002/jez.b.21070

Cited by 157 publications

(133 citation statements)

References 65 publications

Supporting

Mentioning

129

Contrasting

Order By: Relevance

“…It has been proposed that Hox genes were organized into a cluster in the ancestor of deuterostomes and that the Hox gene cluster became disorganized in echinoderm and urochordate lineages (Cameron et al, 2006;Ikuta and Saiga, 2005;Lemons and McGinnis, 2006;Seo et al, 2004). It is an indisputable fact that ascidian Hox genes are no longer all clustered and that the colinearity is residual.…”

Section: Discussionmentioning

confidence: 99%

Limited functions of Hox genes in the larval development of the ascidian Ciona intestinalis

2010

View full text Add to dashboard Cite

SUMMARYIn animals, region specific morphological characters along the anteroposterior axis are controlled by a number of developmental genes, including Hox genes encoding homeodomain transcription factors. Although Hox genes have been regarded to play a key role in the evolution of morphological diversity, as well as in the establishment of the body plan, little is known about the function of Hox genes in invertebrates, except for in insects and nematodes. The present study addresses the role of Hox genes in body patterning during the larval development of the ascidian Ciona intestinalis conducting knockdown experiments of the seven Hox genes expressed during embryogenesis. Experimental results have demonstrated that Ci-Hox12 plays an important role in tail development through the maintenance of expression of Ci-Fgf8/17/18 and Ci-Wnt5 in the tail tip epidermis. Additionally, it has been shown that Ci-Hox10 is involved in the development of GABAergic neurons in the dorsal visceral ganglion. Surprisingly, knockdown of Ci-Hox1, Ci-Hox2, Ci-Hox3, Ci-Hox4 and Ci-Hox5 did not give rise to any consistent morphological defects in the larvae. Furthermore, expression of neuronal marker genes was not affected in larvae injected with MOs against Ci-Hox1, Ci-Hox3 or Ci-Hox5. In conclusion, we suggest that the contribution of Hox genes to the larval development of the ascidian C. intestinalis might be limited, despite the fact that Ci-Hox10 and Ci-Hox12 play important roles in neuronal and tail development.

show abstract

Section: Discussionmentioning

confidence: 99%

Limited functions of Hox genes in the larval development of the ascidian Ciona intestinalis

2010

View full text Add to dashboard Cite

show abstract

“…Our results raise the possibility that Col1␣1 and Col2␣1 arose from the same duplication event, and thus the major matrix components of bone and cartilage may have evolved at the same time in vertebrates. Finally, it is noteworthy that clade A fibrillar collagens are physically linked with Hox gene clusters in vertebrates and in echinoderms (31). Duplication of the clade A fibrillar collagen genes therefore may have coincided with the Hox cluster duplications (32,33).…”

Section: Clade a Fibrillar Collagen Duplication Facilitated Evolutionmentioning

confidence: 99%

Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

Zhang

Cohn

2006

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

The origin of vertebrates was defined by evolution of a skeleton; however, little is known about the developmental mechanisms responsible for this landmark evolutionary innovation. In jawed vertebrates, cartilage matrix consists predominantly of type II collagen (Col2␣1), whereas that of jawless fishes has long been thought to be noncollagenous. We recently showed that Col2␣1 is present in lamprey cartilage, indicating that type II collagen-based cartilage evolved earlier than previously recognized. Here, we investigate the origin of vertebrate cartilage, and we report that hagfishes, the sister group to lampreys, also have Col2␣1-based cartilage, suggesting its presence in the common ancestor of crown-group vertebrates. We go on to show that lancelets, a sister group to vertebrates, possess an ancestral clade A fibrillar collagen (ColA) gene that is expressed in the notochord. Together, these results suggest that duplication and diversification of ColA genes at the chordate-vertebrate transition may underlie the evolutionary origin of vertebrate skeletal tissues.development ͉ gene duplication ͉ skeleton evolution ͉ chordate ͉ notochord T he phylogenetic relationships of the vertebrates were established largely based on anatomical characters, particularly those of the skeleton. The skeletons of jawed vertebrates (gnathostomes) are composed of cartilage and bone, which contain high levels of type II and type I collagen (Col2␣1 and Col1␣1͞2 protein, respectively). By contrast, the cartilaginous skeletons of lampreys and hagfishes, the only extant jawless fishes (agnathans), have been reported to be noncollagenous and to contain instead the elastin-like proteins lamprin and myxinin (1). This difference in the extracellular matrices of vertebrate skeletons led to the idea that type II collagen became the major structural component of gnathostome cartilage after the divergence of these two lineages (1). However, this view was challenged by our recent report that lampreys have two Col2␣1 orthologs and that both genes are expressed during chondrogenesis. Adult lamprey cartilage was also shown to be rich in Col2␣1 protein (2). Furthermore, we identified a lamprey ortholog of Sox9, a direct transcriptional regulator of Col2␣1 in gnathostomes, and we showed that it is coexpressed with Col2␣1 (2). This discovery revealed that the genetic pathway for vertebrate chondrogenesis predated the divergence of lampreys and gnathostomes, although precisely how early this character arose is unknown. Here, we investigate the evolutionary origin of Col2␣1-based cartilage by expanding our analysis to the most inclusive clade of vertebrates, which includes the hagfishes, and to a sister group to the vertebrates, the lancelets (3, 4). We report that hagfishes also have Col2␣1-based cartilage, suggesting that this type of cartilage was present in common ancestor of all crown vertebrates. Our analysis of lancelets revealed the presence of an ancestral clade A fibrillar collagen (ColA) gene that is expressed in the notochord. Thus, during th...

show abstract

“…The situation in protostomes is equally heterogeneous. The sea urchin Hox cluster is large and contains genes in opposite transcriptional orientations and at unexpected positions with respect to their paralogous groups, revealing the occurrence of important rearrangements (Cameron et al, 2006) that are typical of type D clusters. By contrast, analyses of Ciona intestinalis and Oikopleura dioica indicate that urochordates have atomized 'clusters' of Hox genes (Ikuta et al, 2004;Seo et al, 2004).…”

Section: There Are Clusters and Clustersmentioning

confidence: 99%

The rise and fall of Hox gene clusters

2007

View full text Add to dashboard Cite

Although all bilaterian animals have a related set of Hox genes, the genomic organization of this gene complement comes in different flavors. In some unrelated species, Hox genes are clustered; in others, they are not. This indicates that the bilaterian ancestor had a clustered Hox gene family and that, subsequently, this genomic organization was either maintained or lost. Remarkably, the tightest organization is found in vertebrates, raising the embarrassingly finalistic possibility that vertebrates have maintained best this ancestral configuration. Alternatively, could they have co-evolved with an increased `organization' of the Hox clusters, possibly linked to their genomic amplification, which would be at odds with our current perception of evolutionary mechanisms? When discussing the why's and how's of Hox gene clustering, we need to account for three points: the mechanisms of cluster evolution; the underlying biological constraints; and the developmental modes of the animals under consideration. By integrating these parameters, general conclusions emerge that can help solve the aforementioned dilemma. “See my son, here time becomes space” Gurnemanz, in Parsifal (R. Wagner)

show abstract

Unusual gene order and organization of the sea urchin hox cluster

Cited by 157 publications

References 65 publications

Limited functions of Hox genes in the larval development of the ascidian Ciona intestinalis

Limited functions of Hox genes in the larval development of the ascidian Ciona intestinalis

Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

The rise and fall of Hox gene clusters

Contact Info

Product

Resources

About