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The ubiquilin gene family: evolutionary patterns and functional insights.

Marín I - BMC Evol. Biol. (2014)

Bottom Line: This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis.The ubiquilin gene family is highly conserved in eukaryotes.The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), Valencia, Spain. imarin@ibv.csic.es.

ABSTRACT

Background: Ubiquilins are proteins that function as ubiquitin receptors in eukaryotes. Mutations in two ubiquilin-encoding genes have been linked to the genesis of neurodegenerative diseases. However, ubiquilin functions are still poorly understood.

Results: In this study, evolutionary and functional data are combined to determine the origin and diversification of the ubiquilin gene family and to characterize novel potential roles of ubiquilins in mammalian species, including humans. The analysis of more than six hundred sequences allowed characterizing ubiquilin diversity in all the main eukaryotic groups. Many organisms (e. g. fungi, many animals) have single ubiquilin genes, but duplications in animal, plant, alveolate and excavate species are described. Seven different ubiquilins have been detected in vertebrates. Two of them, here called UBQLN5 and UBQLN6, had not been hitherto described. Significantly, marsupial and eutherian mammals have the most complex ubiquilin gene families, composed of up to 6 genes. This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis. A gene with related features has independently arisen in species of the Drosophila genus. Positive selection acting on some mammalian ubiquilins has been detected.

Conclusions: The ubiquilin gene family is highly conserved in eukaryotes. The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

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Related in: MedlinePlus

Plant ubiquilins. Two ancient duplications are indicated as Dicot I/II and Poaceae I/II (see text). Colors are applied to some main angiosperm classes (pink: rosid dicots; green: saxifragal dicots; yellow: asterid dicots; blue: monocots).
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Figure 5: Plant ubiquilins. Two ancient duplications are indicated as Dicot I/II and Poaceae I/II (see text). Colors are applied to some main angiosperm classes (pink: rosid dicots; green: saxifragal dicots; yellow: asterid dicots; blue: monocots).

Mentions: The number of ubiquilin sequences available in green plants is limited, just 73, but the broad phylogenetic range of species from which they derive allow for a precise characterization of their patterns of diversification. A first result is that all the species for which there is complete or almost complete genomic data have a very limited number of ubiquilins. The maximum number observed is four, in the dicots Glycine max and Brassica rapa and the monocot Zea mays. Most species have however just two ubiquilin genes. Figure 5 shows the phylogenetic tree obtained when those 73 sequences are compared, which serves to determine the origin of all those genes. Contrary to the trees in Figures 1, 2 and 3, which, as indicated, derive solely from the UBL and UBA domain information, this tree was obtained with the full sequences. The reason is that all plants have structurally very similar ubiquilins, all of them with four Sti1 domains. Given that they can be quite easily aligned along their whole lengths, it makes sense using here all the information to generate the trees. Notice also that this structural similarity also supports the monophyletic origin of all plant ubiquilins. This putative monophyly is again reinforced by the phylogenetic trees (Figure 5), which perfectly recapitulate the known evolutionary relationships of the plant species, with early-branching species (such as the charophyte alga Klebsormidium, the spikemoss Selaginella and the moss Physcomytrella) separated from both the two gymnosperms for which ubiquilin genes have been detected (Picea glauca and Pseudotsuga menziessi) and all the angiosperms. Within angiosperms, the divergence of monocot and dicot species is also recapitulated in the tree.


The ubiquilin gene family: evolutionary patterns and functional insights.

Marín I - BMC Evol. Biol. (2014)

Plant ubiquilins. Two ancient duplications are indicated as Dicot I/II and Poaceae I/II (see text). Colors are applied to some main angiosperm classes (pink: rosid dicots; green: saxifragal dicots; yellow: asterid dicots; blue: monocots).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4230246&req=5

Figure 5: Plant ubiquilins. Two ancient duplications are indicated as Dicot I/II and Poaceae I/II (see text). Colors are applied to some main angiosperm classes (pink: rosid dicots; green: saxifragal dicots; yellow: asterid dicots; blue: monocots).
Mentions: The number of ubiquilin sequences available in green plants is limited, just 73, but the broad phylogenetic range of species from which they derive allow for a precise characterization of their patterns of diversification. A first result is that all the species for which there is complete or almost complete genomic data have a very limited number of ubiquilins. The maximum number observed is four, in the dicots Glycine max and Brassica rapa and the monocot Zea mays. Most species have however just two ubiquilin genes. Figure 5 shows the phylogenetic tree obtained when those 73 sequences are compared, which serves to determine the origin of all those genes. Contrary to the trees in Figures 1, 2 and 3, which, as indicated, derive solely from the UBL and UBA domain information, this tree was obtained with the full sequences. The reason is that all plants have structurally very similar ubiquilins, all of them with four Sti1 domains. Given that they can be quite easily aligned along their whole lengths, it makes sense using here all the information to generate the trees. Notice also that this structural similarity also supports the monophyletic origin of all plant ubiquilins. This putative monophyly is again reinforced by the phylogenetic trees (Figure 5), which perfectly recapitulate the known evolutionary relationships of the plant species, with early-branching species (such as the charophyte alga Klebsormidium, the spikemoss Selaginella and the moss Physcomytrella) separated from both the two gymnosperms for which ubiquilin genes have been detected (Picea glauca and Pseudotsuga menziessi) and all the angiosperms. Within angiosperms, the divergence of monocot and dicot species is also recapitulated in the tree.

Bottom Line: This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis.The ubiquilin gene family is highly conserved in eukaryotes.The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), Valencia, Spain. imarin@ibv.csic.es.

ABSTRACT

Background: Ubiquilins are proteins that function as ubiquitin receptors in eukaryotes. Mutations in two ubiquilin-encoding genes have been linked to the genesis of neurodegenerative diseases. However, ubiquilin functions are still poorly understood.

Results: In this study, evolutionary and functional data are combined to determine the origin and diversification of the ubiquilin gene family and to characterize novel potential roles of ubiquilins in mammalian species, including humans. The analysis of more than six hundred sequences allowed characterizing ubiquilin diversity in all the main eukaryotic groups. Many organisms (e. g. fungi, many animals) have single ubiquilin genes, but duplications in animal, plant, alveolate and excavate species are described. Seven different ubiquilins have been detected in vertebrates. Two of them, here called UBQLN5 and UBQLN6, had not been hitherto described. Significantly, marsupial and eutherian mammals have the most complex ubiquilin gene families, composed of up to 6 genes. This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis. A gene with related features has independently arisen in species of the Drosophila genus. Positive selection acting on some mammalian ubiquilins has been detected.

Conclusions: The ubiquilin gene family is highly conserved in eukaryotes. The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

Show MeSH
Related in: MedlinePlus