Gene Conversion and the Evolution of Protocadherin Gene Cluster Diversity

Noonan, James P.; Grimwood, Jane; Schmutz, Jeremy; Dickson, Mark; Myers, R

doi:10.1101/gr.2133704

Cited by 102 publications

(138 citation statements)

References 55 publications

Supporting

Mentioning

125

Contrasting

Unclassified

Order By: Relevance

“…The overall gene content of the elephant shark protocadherin cluster (47 variable exons arrayed in four subclusters) is comparable to that in coelacanth (49 variable exons in three subclusters) (4) and human (53 variable exons in three subclusters) (3,15). However, its gene content is considerably lower than that in fugu (Ͼ77 variable exons) (6) and zebrafish (Ͼ107 variable exons) (2,4,5,7).…”

Section: Elephant Shark Protocadherin Cluster Genes Organized Into Fourmentioning

confidence: 94%

“…Because of the ''fish-specific'' whole-genome duplication, teleost fishes such as fugu and zebrafish contain two unlinked protocadherin clusters, designated Pcdh1 and Pcdh2. Although fugu Pcdh1 cluster is highly degenerate, Pcdh2 clusters in both fishes have undergone lineage-specific repeated tandem duplications, and gene losses giving rise to Ͼ107 genes in zebrafish (2,5,7) and Ͼ77 genes in fugu (6). However, these teleost protocadherin genes are orthologous to only Pcdh␣ and -␥ subcluster genes in mammals and coelacanth.…”

mentioning

confidence: 99%

“…It is composed of tandem arrays of paralogous genes that are highly susceptible to lineage-specific gene losses, tandem duplications, and gene conversion (2)(3)(4)(5)(6)(7). These clustered genes are distinct from nonclustered protocadherin genes by possessing a large coding exon that codes for the entire extracellular domain, the transmembrane domain, and a small portion of the cytoplasmic domain, whereas the extracellular domain of the nonclustered protocadherins is usually encoded by multiple exons (8).…”

mentioning

confidence: 99%

“…However, these teleost protocadherin genes are orthologous to only Pcdh␣ and -␥ subcluster genes in mammals and coelacanth. Another interesting feature of teleost protocadherin cluster genes is that they have experienced extensive regional gene conversion events resulting in nucleotide identity of Ͼ99% in the 3Ј region of variable exons among paralogs (5,6). Based on the organization, gene content, and phylogenetic relationships of protocadherin clusters in bony vertebrates, the ancestral vertebrate protocadherin cluster is predicted to contain either two (Pcdh␣ and -␥) or three subclusters (Pcdh␣, -␤, and -␥) that have subsequently undergone lineage-specific gene losses and gene duplications, including the whole-locus duplication in the teleost fish lineage (6).…”

mentioning

confidence: 99%

See 3 more Smart Citations

Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster

Rajasegaran

Yew

et al. 2008

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

View full text Add to dashboard Cite

Cartilaginous fishes are the oldest living phylogenetic group of jawed vertebrates. Here, we demonstrate the value of cartilaginous fish sequences in reconstructing the evolutionary history of vertebrate genomes by sequencing the protocadherin cluster in the relatively small genome (910 Mb) of the elephant shark (Callorhinchus milii). Human and coelacanth contain a single protocadherin cluster with 53 and 49 genes, respectively, that are organized in three subclusters, Pcdh␣, Pcdh␤, and Pcdh␥, whereas the duplicated protocadherin clusters in fugu and zebrafish contain >77 and 107 genes, respectively, that are organized in Pcdh␣ and Pcdh␥ subclusters. By contrast, the elephant shark contains a single protocadherin cluster with 47 genes organized in four subclusters (Pcdh␦, Pcdh, Pcdh, and Pcdh). By comparison with elephant shark sequences, we discovered a Pcdh␦ subcluster in teleost fishes, coelacanth, Xenopus, and chicken. Our results suggest that the protocadherin cluster in the ancestral jawed vertebrate contained more subclusters than modern vertebrates, and the evolution of the protocadherin cluster is characterized by lineagespecific differential loss of entire subclusters of genes. In contrast to teleost fish and mammalian protocadherin genes that have undergone gene conversion events, elephant shark protocadherin genes have experienced very little gene conversion. The syntenic block of genes in the elephant shark protocadherin locus is well conserved in human but disrupted in fugu. Thus, the elephant shark genome appears to be less prone to rearrangements compared with teleost fish genomes. The small and ''stable'' genome of the elephant shark is a valuable reference for understanding the evolution of vertebrate genomes.ancestral jawed vertebrate ͉ clustered protocadherins ͉ cartilaginous fish ͉ Callorhinchus milii ͉ gene conversion R econstructing the evolutionary history of vertebrate genomes, and in particular the human genome, is a major goal of vertebrate comparative genomics. Efforts are underway to reconstruct the evolutionary history of the human genome at the nucleotide level and at the level of large-scale chromosomal rearrangements (1) with the objective of predicting ancestral genomes with high accuracy. The accuracy of the reconstruction of ancestral genomes is greatly influenced by the choice and number of genomes compared. Although a comparison of genomes from all major vertebrate groups is desirable, it is also important to compare genomes from the most distant branches of the phylogenetic tree. Here, we show how the genome sequence from the oldest living phylogenetic group of jawed vertebrates, the cartilaginous fishes, can dramatically change our inferences of the state of the ancestral vertebrate genome.The protocadherin gene cluster is one of the most evolutionarily dynamic loci in vertebrates. It is composed of tandem arrays of paralogous genes that are highly susceptible to lineage-specific gene losses, tandem duplications, and gene conversion (2-7). These clustered genes are distinc...

show abstract

Section: Elephant Shark Protocadherin Cluster Genes Organized Into Fourmentioning

confidence: 94%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster

Rajasegaran

Yew

et al. 2008

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

View full text Add to dashboard Cite

show abstract

“…Almost all gene conversion events discovered in teleosts have affected paralogues that do not stem from TS-WGD but rather from more recent duplications (mostly tandem duplications) in teleost sublineages (Bargelloni et al, 1999;McGuigan et al, 2004;Noonan et al, 2004;Gerrard and Meyer, 2007;Yu et al, 2007;Windsor and Owens, 2009;Weadick and Chang, 2012). Only one instance of gene conversion between paralogues generated by TS-WGD, namely rainbow trout sox9α2 and sox9 (Alfaqih et al, 2009) has so far been documented.…”

mentioning

confidence: 99%

Whole-genome duplication in teleost fishes and its evolutionary consequences

2014

View full text Add to dashboard Cite

Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change. AbstractWhole genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, the by far most species-rich vertebrate clade. After initial controversy, evidence is now solid that such an event took place in the common ancestor of all extant teleosts, the so-called teleostspecific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both copies of the gene. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosageselection (preserving genes to maintain dosage-balance between interconnected components).Since the frequency of these mechanisms is influenced by the gene's properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massi...

show abstract

Protocadherin‐17 function in Zebrafish retinal development

Chen

Londraville

Brickner

et al. 2013

Developmental Neurobiology

View full text Add to dashboard Cite

Cadherin cell adhesion molecules play crucial roles in vertebrate development including the development of the retina. Most studies have focused on examining functions of classic cadherins (e.g. N-cadherin) in retinal development. There is little information on the function of protocadherins in the development of the vertebrate visual system. We previously showed that protocadherin-17 mRNA was expressed in developing zebrafish retina during critical stages of the retinal development. To gain insight into protocadherin-17 function in the formation of the retina, we analyzed eye development and differentiation of retinal cells in zebrafish embryos injected with protocadherin-17 specific antisense morpholino oligonucleotides (MOs). Protocadherin-17 knockdown embryos (pcdh17 morphants) had significantly reduced eyes due mainly to decreased cell proliferation. Differentiation of several retinal cell types (e.g. retinal ganglion cells) was also disrupted in the pcdh17 morphants. Phenotypic rescue was achieved by injection of protocadherin-17 mRNA. Injection of a vivo-protocadherin-17 MO into one eye of embryonic zebrafish resulted in similar eye defects. Our results suggest that protocadherin-17 plays an important role in the normal formation of the zebrafish retina.

show abstract

Gene Conversion and the Evolution of Protocadherin Gene Cluster Diversity

Cited by 102 publications

References 55 publications

Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster

Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: A comparative analysis of the protocadherin cluster

Whole-genome duplication in teleost fishes and its evolutionary consequences

Protocadherin‐17 function in Zebrafish retinal development

Contact Info

Product

Resources

About