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A large family of Dscam genes with tandemly arrayed 5' cassettes in Chelicerata.

Yue Y, Meng Y, Ma H, Hou S, Cao G, Hong W, Shi Y, Guo P, Liu B, Shi F, Yang Y, Jin Y - Nat Commun (2016)

Bottom Line: Furthermore, extraordinary isoform diversity has been generated through a combination of alternating promoter and alternative splicing.These sDscams have a high sequence similarity with Drosophila Dscam1, and share striking organizational resemblance to the 5' variable regions of vertebrate clustered Pcdhs.Hence, our findings have important implications for understanding the functional similarities between Drosophila Dscam1 and vertebrate Pcdhs, and may provide further mechanistic insights into the regulation of isoform diversity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biochemistry, Innovation Center for Signaling Network, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang ZJ310058, China.

ABSTRACT
Drosophila Dscam1 (Down Syndrome Cell Adhesion Molecules) and vertebrate clustered protocadherins (Pcdhs) are two classic examples of the extraordinary isoform diversity from a single genomic locus. Dscam1 encodes 38,016 distinct isoforms via mutually exclusive splicing in D. melanogaster, while the vertebrate clustered Pcdhs utilize alternative promoters to generate isoform diversity. Here we reveal a shortened Dscam gene family with tandemly arrayed 5' cassettes in Chelicerata. These cassette repeats generally comprise two or four exons, corresponding to variable Immunoglobulin 7 (Ig7) or Ig7-8 domains of Drosophila Dscam1. Furthermore, extraordinary isoform diversity has been generated through a combination of alternating promoter and alternative splicing. These sDscams have a high sequence similarity with Drosophila Dscam1, and share striking organizational resemblance to the 5' variable regions of vertebrate clustered Pcdhs. Hence, our findings have important implications for understanding the functional similarities between Drosophila Dscam1 and vertebrate Pcdhs, and may provide further mechanistic insights into the regulation of isoform diversity.

No MeSH data available.


Related in: MedlinePlus

Arthropoda diversify two systems to generate Dscam isoforms.Exons that are arranged in a tandem array or their orthologues are shown in coloured boxes, while the constitutive exons (CE) flanking the duplicated exons or their orthologues are shown in the black box. The introns are represented by the lines and are not drawn to scale. The emergence of internal tandem exon duplication is indicated by the filled squares. The emergence of 5′ cassette duplication is indicated by black line squares. The filled circle represents gene duplication. Extant organization of Dscam pre-mRNA and proposed ancestor molecules shown are associated with a cladogram of the phylogenetic relationships in this study26. Dscam1 in D. melanogaster, D. pulex and S. maritima are shown according to previous studies32536. The analysed species and detailed sDscam data are shown in Fig. 1 and Supplementary Fig. 2. The number of copies is shown in parentheses.
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f7: Arthropoda diversify two systems to generate Dscam isoforms.Exons that are arranged in a tandem array or their orthologues are shown in coloured boxes, while the constitutive exons (CE) flanking the duplicated exons or their orthologues are shown in the black box. The introns are represented by the lines and are not drawn to scale. The emergence of internal tandem exon duplication is indicated by the filled squares. The emergence of 5′ cassette duplication is indicated by black line squares. The filled circle represents gene duplication. Extant organization of Dscam pre-mRNA and proposed ancestor molecules shown are associated with a cladogram of the phylogenetic relationships in this study26. Dscam1 in D. melanogaster, D. pulex and S. maritima are shown according to previous studies32536. The analysed species and detailed sDscam data are shown in Fig. 1 and Supplementary Fig. 2. The number of copies is shown in parentheses.

Mentions: Phylogenetic analysis of Arthropoda Dscam genes revealed that Chelicerata sDscam and Drosophila Dscam1 were classified into different clades (Supplementary Fig. 3), suggesting that they may have converged on the common protein domain diversity from independent origins. Notably, duplication of the Ig7-encoding exon 9 or its orthologues occurred internally or 5′ terminally in all Arthropoda species investigated. This suggests that the diversity of Dscam1 Ig7 or its orthologues conferred intrinsic structural and regulatory benefits during Arthropoda evolution. Recent studies indicated that Ig7 domain diversity was crucial for the proper function of Dscam1 (refs 6, 8, 10, 12, 13, 14). Dscam1 generates functionally distinct isoforms through mutually exclusive splicing of internal exons in Drosophila (Fig. 7). However, no Chelicerata Dscam genes appeared to have a similar arrangement, although a random array of only two alternatives for the Dscam1 exon 9 orthologue are often observed in Chelicerata (that is, sDscamβ1 V7). In contrast, sDscam genes have evolved other mechanisms that serve this function in Chelicerata, through a combination of alternative promoter use and alternative splicing (Fig. 7). In this scenario, Drosophila Dscam1 and Chelicerata sDscam represent examples of convergent evolution for isoform diversity.


A large family of Dscam genes with tandemly arrayed 5' cassettes in Chelicerata.

Yue Y, Meng Y, Ma H, Hou S, Cao G, Hong W, Shi Y, Guo P, Liu B, Shi F, Yang Y, Jin Y - Nat Commun (2016)

Arthropoda diversify two systems to generate Dscam isoforms.Exons that are arranged in a tandem array or their orthologues are shown in coloured boxes, while the constitutive exons (CE) flanking the duplicated exons or their orthologues are shown in the black box. The introns are represented by the lines and are not drawn to scale. The emergence of internal tandem exon duplication is indicated by the filled squares. The emergence of 5′ cassette duplication is indicated by black line squares. The filled circle represents gene duplication. Extant organization of Dscam pre-mRNA and proposed ancestor molecules shown are associated with a cladogram of the phylogenetic relationships in this study26. Dscam1 in D. melanogaster, D. pulex and S. maritima are shown according to previous studies32536. The analysed species and detailed sDscam data are shown in Fig. 1 and Supplementary Fig. 2. The number of copies is shown in parentheses.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835542&req=5

f7: Arthropoda diversify two systems to generate Dscam isoforms.Exons that are arranged in a tandem array or their orthologues are shown in coloured boxes, while the constitutive exons (CE) flanking the duplicated exons or their orthologues are shown in the black box. The introns are represented by the lines and are not drawn to scale. The emergence of internal tandem exon duplication is indicated by the filled squares. The emergence of 5′ cassette duplication is indicated by black line squares. The filled circle represents gene duplication. Extant organization of Dscam pre-mRNA and proposed ancestor molecules shown are associated with a cladogram of the phylogenetic relationships in this study26. Dscam1 in D. melanogaster, D. pulex and S. maritima are shown according to previous studies32536. The analysed species and detailed sDscam data are shown in Fig. 1 and Supplementary Fig. 2. The number of copies is shown in parentheses.
Mentions: Phylogenetic analysis of Arthropoda Dscam genes revealed that Chelicerata sDscam and Drosophila Dscam1 were classified into different clades (Supplementary Fig. 3), suggesting that they may have converged on the common protein domain diversity from independent origins. Notably, duplication of the Ig7-encoding exon 9 or its orthologues occurred internally or 5′ terminally in all Arthropoda species investigated. This suggests that the diversity of Dscam1 Ig7 or its orthologues conferred intrinsic structural and regulatory benefits during Arthropoda evolution. Recent studies indicated that Ig7 domain diversity was crucial for the proper function of Dscam1 (refs 6, 8, 10, 12, 13, 14). Dscam1 generates functionally distinct isoforms through mutually exclusive splicing of internal exons in Drosophila (Fig. 7). However, no Chelicerata Dscam genes appeared to have a similar arrangement, although a random array of only two alternatives for the Dscam1 exon 9 orthologue are often observed in Chelicerata (that is, sDscamβ1 V7). In contrast, sDscam genes have evolved other mechanisms that serve this function in Chelicerata, through a combination of alternative promoter use and alternative splicing (Fig. 7). In this scenario, Drosophila Dscam1 and Chelicerata sDscam represent examples of convergent evolution for isoform diversity.

Bottom Line: Furthermore, extraordinary isoform diversity has been generated through a combination of alternating promoter and alternative splicing.These sDscams have a high sequence similarity with Drosophila Dscam1, and share striking organizational resemblance to the 5' variable regions of vertebrate clustered Pcdhs.Hence, our findings have important implications for understanding the functional similarities between Drosophila Dscam1 and vertebrate Pcdhs, and may provide further mechanistic insights into the regulation of isoform diversity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biochemistry, Innovation Center for Signaling Network, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang ZJ310058, China.

ABSTRACT
Drosophila Dscam1 (Down Syndrome Cell Adhesion Molecules) and vertebrate clustered protocadherins (Pcdhs) are two classic examples of the extraordinary isoform diversity from a single genomic locus. Dscam1 encodes 38,016 distinct isoforms via mutually exclusive splicing in D. melanogaster, while the vertebrate clustered Pcdhs utilize alternative promoters to generate isoform diversity. Here we reveal a shortened Dscam gene family with tandemly arrayed 5' cassettes in Chelicerata. These cassette repeats generally comprise two or four exons, corresponding to variable Immunoglobulin 7 (Ig7) or Ig7-8 domains of Drosophila Dscam1. Furthermore, extraordinary isoform diversity has been generated through a combination of alternating promoter and alternative splicing. These sDscams have a high sequence similarity with Drosophila Dscam1, and share striking organizational resemblance to the 5' variable regions of vertebrate clustered Pcdhs. Hence, our findings have important implications for understanding the functional similarities between Drosophila Dscam1 and vertebrate Pcdhs, and may provide further mechanistic insights into the regulation of isoform diversity.

No MeSH data available.


Related in: MedlinePlus