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Composition and genomic organization of arthropod Hox clusters.

Pace RM, Grbić M, Nagy LM - Evodevo (2016)

Bottom Line: The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods.The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain.Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721 USA ; Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030 USA.

ABSTRACT

Background: The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. Within arthropods, Hox gene mutations result in transformation of segment identities. Despite the fact that variation in segment number/character was common in the diversification of arthropods, few examples of Hox gene gains/losses have been correlated with morphological evolution. Furthermore, a full appreciation of the variation in the genomic arrangement of Hox genes in extant arthropods has not been recognized, as genome sequences from each major arthropod clade have not been reported until recently. Initial genomic analysis of the chelicerate Tetranychus urticae suggested that loss of Hox genes and Hox gene clustering might be more common than previously assumed. To further characterize the genomic evolution of arthropod Hox genes, we compared the genomic arrangement and general characteristics of Hox genes from representative taxa from each arthropod subphylum.

Results: In agreement with others, we find arthropods generally contain ten Hox genes arranged in a common orientation in the genome, with an increasing number of sampled species missing either Hox3 or abdominal-A orthologs. The genomic clustering of Hox genes in species we surveyed varies significantly, ranging from 0.3 to 13.6 Mb. In all species sampled, arthropod Hox genes are dispersed in the genome relative to the vertebrate Mus musculus. Differences in Hox cluster size arise from variation in the number of intervening genes, intergenic spacing, and the size of introns and UTRs. In the arthropods surveyed, Hox gene duplications are rare and four microRNAs are, in general, conserved in similar genomic positions relative to the Hox genes.

Conclusions: The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods. The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain. Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.

No MeSH data available.


Related in: MedlinePlus

Comparison of the relative sizes of the coding, intronic, and untranslated regions of arthropod and vertebrate Hox genes. The relative sizes of amino acid coding sequence (CDS), introns, and total and 5′ and 3′ untranslated regions (UTRs) are shown for twelve arthropods surveyed and the vertebrate Mus musculus. Individual Hox genes are represented as a stack, in their respective genomic location of the Hox cluster, and labeled by color. The overall coding sequence length among arthropods ranges from 7.1 kb in Ixodes to 18.1 kb in Daphnia. The overall intron length among arthropods ranges from 14.5 kb in Ixodes to 624.6 kb in Bombyx. The overall UTR length among arthropods ranges from 2.3 kb in Anopheles to 30.5 kb in Drosophila. Asterisks indicate missing or incomplete data
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Fig2: Comparison of the relative sizes of the coding, intronic, and untranslated regions of arthropod and vertebrate Hox genes. The relative sizes of amino acid coding sequence (CDS), introns, and total and 5′ and 3′ untranslated regions (UTRs) are shown for twelve arthropods surveyed and the vertebrate Mus musculus. Individual Hox genes are represented as a stack, in their respective genomic location of the Hox cluster, and labeled by color. The overall coding sequence length among arthropods ranges from 7.1 kb in Ixodes to 18.1 kb in Daphnia. The overall intron length among arthropods ranges from 14.5 kb in Ixodes to 624.6 kb in Bombyx. The overall UTR length among arthropods ranges from 2.3 kb in Anopheles to 30.5 kb in Drosophila. Asterisks indicate missing or incomplete data

Mentions: In contrast to the uncommon association of a loss of a Hox gene with morphological variation, there are numerous examples where morphological diversification along the A/P body axis is achieved through changes in the regulation of the Hox genes, leading to variation in the A/P expression boundaries of the Hox genes [37, 38] (see [12] for review), as well as to changes in their downstream targets [39, 40] (see [41] for review). The intergenic regions between Hox genes are thus important sites of regulation [42] and also include microRNAs (miRNAs), small non-coding RNAs, known to play essential roles in Hox gene regulation [43]. While there is no consensus on the number of conserved arthropod Hox gene-associated miRNAs, more than twenty are functionally annotated in Drosophila melanogaster between the Hox genes labial and Abdominal-B [44], with four of these miRNAs—miR-993, miR-10, miR-iab-4, and miR-iab-8—found in conserved positions within arthropod genomes [45–51] (Fig. 2). The last two, miR-iab-4 and miR-iab-8, reside at the same locus and produces sense (miR-iab-4) and antisense (miR-iab-8) transcripts [52, 53]. However, these views of arthropod Hox gene regulation are mainly derived from insects, leaving relatively little known about the extent of miRNA conservation and divergence throughout the Arthropoda.Fig. 2


Composition and genomic organization of arthropod Hox clusters.

Pace RM, Grbić M, Nagy LM - Evodevo (2016)

Comparison of the relative sizes of the coding, intronic, and untranslated regions of arthropod and vertebrate Hox genes. The relative sizes of amino acid coding sequence (CDS), introns, and total and 5′ and 3′ untranslated regions (UTRs) are shown for twelve arthropods surveyed and the vertebrate Mus musculus. Individual Hox genes are represented as a stack, in their respective genomic location of the Hox cluster, and labeled by color. The overall coding sequence length among arthropods ranges from 7.1 kb in Ixodes to 18.1 kb in Daphnia. The overall intron length among arthropods ranges from 14.5 kb in Ixodes to 624.6 kb in Bombyx. The overall UTR length among arthropods ranges from 2.3 kb in Anopheles to 30.5 kb in Drosophila. Asterisks indicate missing or incomplete data
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4862073&req=5

Fig2: Comparison of the relative sizes of the coding, intronic, and untranslated regions of arthropod and vertebrate Hox genes. The relative sizes of amino acid coding sequence (CDS), introns, and total and 5′ and 3′ untranslated regions (UTRs) are shown for twelve arthropods surveyed and the vertebrate Mus musculus. Individual Hox genes are represented as a stack, in their respective genomic location of the Hox cluster, and labeled by color. The overall coding sequence length among arthropods ranges from 7.1 kb in Ixodes to 18.1 kb in Daphnia. The overall intron length among arthropods ranges from 14.5 kb in Ixodes to 624.6 kb in Bombyx. The overall UTR length among arthropods ranges from 2.3 kb in Anopheles to 30.5 kb in Drosophila. Asterisks indicate missing or incomplete data
Mentions: In contrast to the uncommon association of a loss of a Hox gene with morphological variation, there are numerous examples where morphological diversification along the A/P body axis is achieved through changes in the regulation of the Hox genes, leading to variation in the A/P expression boundaries of the Hox genes [37, 38] (see [12] for review), as well as to changes in their downstream targets [39, 40] (see [41] for review). The intergenic regions between Hox genes are thus important sites of regulation [42] and also include microRNAs (miRNAs), small non-coding RNAs, known to play essential roles in Hox gene regulation [43]. While there is no consensus on the number of conserved arthropod Hox gene-associated miRNAs, more than twenty are functionally annotated in Drosophila melanogaster between the Hox genes labial and Abdominal-B [44], with four of these miRNAs—miR-993, miR-10, miR-iab-4, and miR-iab-8—found in conserved positions within arthropod genomes [45–51] (Fig. 2). The last two, miR-iab-4 and miR-iab-8, reside at the same locus and produces sense (miR-iab-4) and antisense (miR-iab-8) transcripts [52, 53]. However, these views of arthropod Hox gene regulation are mainly derived from insects, leaving relatively little known about the extent of miRNA conservation and divergence throughout the Arthropoda.Fig. 2

Bottom Line: The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods.The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain.Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721 USA ; Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030 USA.

ABSTRACT

Background: The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. Within arthropods, Hox gene mutations result in transformation of segment identities. Despite the fact that variation in segment number/character was common in the diversification of arthropods, few examples of Hox gene gains/losses have been correlated with morphological evolution. Furthermore, a full appreciation of the variation in the genomic arrangement of Hox genes in extant arthropods has not been recognized, as genome sequences from each major arthropod clade have not been reported until recently. Initial genomic analysis of the chelicerate Tetranychus urticae suggested that loss of Hox genes and Hox gene clustering might be more common than previously assumed. To further characterize the genomic evolution of arthropod Hox genes, we compared the genomic arrangement and general characteristics of Hox genes from representative taxa from each arthropod subphylum.

Results: In agreement with others, we find arthropods generally contain ten Hox genes arranged in a common orientation in the genome, with an increasing number of sampled species missing either Hox3 or abdominal-A orthologs. The genomic clustering of Hox genes in species we surveyed varies significantly, ranging from 0.3 to 13.6 Mb. In all species sampled, arthropod Hox genes are dispersed in the genome relative to the vertebrate Mus musculus. Differences in Hox cluster size arise from variation in the number of intervening genes, intergenic spacing, and the size of introns and UTRs. In the arthropods surveyed, Hox gene duplications are rare and four microRNAs are, in general, conserved in similar genomic positions relative to the Hox genes.

Conclusions: The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods. The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain. Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.

No MeSH data available.


Related in: MedlinePlus