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The evolution and expression of the snaR family of small non-coding RNAs.

Parrott AM, Tsai M, Batchu P, Ryan K, Ozer HL, Tian B, Mathews MB - Nucleic Acids Res. (2010)

Bottom Line: We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein.The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse.We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, New Jersey Medical School, UMDNJ, Newark, New Jersey, USA.

ABSTRACT
We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein. The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse. We report their expression in human tissues and their evolution in primates. snaR genes are exclusively in African Great Apes and some are unique to humans. Two novel families of snaR-related genetic elements were found in primates: CAS (catarrhine ancestor of snaR), limited to Old World Monkeys and apes; and ASR (Alu/snaR-related), present in all monkeys and apes. ASR and CAS appear to have spread by retrotransposition, whereas most snaR genes have spread by segmental duplication. snaR-A and snaR-G2 are differentially expressed in discrete regions of the human brain and other tissues, notably including testis. snaR-A is up-regulated in transformed and immortalized human cells, and is stably bound to ribosomes in HeLa cells. We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

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Stages of snaR molecular evolution correlate with major primate speciation events. (A) Unrooted phylogram displaying sequences of all known snaR genes (in red) together with 12 hamadryas baboon (Ph), 6 grivet (Ca), 17 mantled guereza (Cg), 23 rhesus macaque (Mm), 11 white-cheeked crested gibbon (Nl), 24 common chimpanzee (Pt), 24 human (Hs), 26 sumatran orangutan (Pa) and 3 western gorilla (Gg) CAS elements (in black) and ASR elements (in blue). Human Alu relatives (in gold) and squirrel monkey (Sb) and common marmoset (Cj) ASR elements are included. CAS elements located within the orthologous segment of chromosome 19 (in green) and in HERV (branch is shaded orange) are denoted. The scale bar represents 0.1 nt substitutions per site. Numbers in parentheses indicate snaR gene multiplicity. (B) Primate dendrogram illustrating the species range and longevity of snaR (red box) and CAS (black box) genes, and the possible extent of ASR genes (blue box). HERV-W integration into the primate lineage is indicated. Tree is modified from (75).
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Figure 8: Stages of snaR molecular evolution correlate with major primate speciation events. (A) Unrooted phylogram displaying sequences of all known snaR genes (in red) together with 12 hamadryas baboon (Ph), 6 grivet (Ca), 17 mantled guereza (Cg), 23 rhesus macaque (Mm), 11 white-cheeked crested gibbon (Nl), 24 common chimpanzee (Pt), 24 human (Hs), 26 sumatran orangutan (Pa) and 3 western gorilla (Gg) CAS elements (in black) and ASR elements (in blue). Human Alu relatives (in gold) and squirrel monkey (Sb) and common marmoset (Cj) ASR elements are included. CAS elements located within the orthologous segment of chromosome 19 (in green) and in HERV (branch is shaded orange) are denoted. The scale bar represents 0.1 nt substitutions per site. Numbers in parentheses indicate snaR gene multiplicity. (B) Primate dendrogram illustrating the species range and longevity of snaR (red box) and CAS (black box) genes, and the possible extent of ASR genes (blue box). HERV-W integration into the primate lineage is indicated. Tree is modified from (75).

Mentions: The major stages of snaR molecular evolution are clearly segregated in the unrooted phylogram shown in Figure 8A. Although the transitions between the stages are accompanied by insertion and deletion events (indels; Figure 3D), they are also characterized by sequence changes (Supplementary Figure S6). A similar phylogram results using an alignment from which the indels were omitted (Supplementary Figure S7). Hence, the stages of snaR evolution are segregated by substitutions between the different molecular species as well as by indels. Strikingly, the evolution of each phylogram cluster in this molecular lineage coincides with major primate speciation events (Figure 8B). Thus, ASR elements are likely to have evolved in Simiiformes with the internal deletion of 17–19 nt from a FLAM C-like ancestor (δ1, Figure 3D). CAS elements probably evolved from ASR via a 3′-deletion (δ2, Figure 3D) in Catarrhines, after their geographical separation from New World Monkeys (Platyrrhines) in the late Eocene (30–45 MYA). The snaR genes appear to have evolved from CAS through two separate internal expansion events (ε1 and ε2, Figure 3D), in the common ancestor of African Great Apes in the Miocene Epoch (9–17 MYA). We conclude that the pathway of snaR gene evolution is characterized by a series of deletions followed by internal duplications, and its principal steps correlate with pivotal events in primate evolution: first, the divergence of simians from prosimians; second, the separation of Old World from New World monkeys; and third, the divergence of the African Great Apes from other apes.Figure 8.


The evolution and expression of the snaR family of small non-coding RNAs.

Parrott AM, Tsai M, Batchu P, Ryan K, Ozer HL, Tian B, Mathews MB - Nucleic Acids Res. (2010)

Stages of snaR molecular evolution correlate with major primate speciation events. (A) Unrooted phylogram displaying sequences of all known snaR genes (in red) together with 12 hamadryas baboon (Ph), 6 grivet (Ca), 17 mantled guereza (Cg), 23 rhesus macaque (Mm), 11 white-cheeked crested gibbon (Nl), 24 common chimpanzee (Pt), 24 human (Hs), 26 sumatran orangutan (Pa) and 3 western gorilla (Gg) CAS elements (in black) and ASR elements (in blue). Human Alu relatives (in gold) and squirrel monkey (Sb) and common marmoset (Cj) ASR elements are included. CAS elements located within the orthologous segment of chromosome 19 (in green) and in HERV (branch is shaded orange) are denoted. The scale bar represents 0.1 nt substitutions per site. Numbers in parentheses indicate snaR gene multiplicity. (B) Primate dendrogram illustrating the species range and longevity of snaR (red box) and CAS (black box) genes, and the possible extent of ASR genes (blue box). HERV-W integration into the primate lineage is indicated. Tree is modified from (75).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3045588&req=5

Figure 8: Stages of snaR molecular evolution correlate with major primate speciation events. (A) Unrooted phylogram displaying sequences of all known snaR genes (in red) together with 12 hamadryas baboon (Ph), 6 grivet (Ca), 17 mantled guereza (Cg), 23 rhesus macaque (Mm), 11 white-cheeked crested gibbon (Nl), 24 common chimpanzee (Pt), 24 human (Hs), 26 sumatran orangutan (Pa) and 3 western gorilla (Gg) CAS elements (in black) and ASR elements (in blue). Human Alu relatives (in gold) and squirrel monkey (Sb) and common marmoset (Cj) ASR elements are included. CAS elements located within the orthologous segment of chromosome 19 (in green) and in HERV (branch is shaded orange) are denoted. The scale bar represents 0.1 nt substitutions per site. Numbers in parentheses indicate snaR gene multiplicity. (B) Primate dendrogram illustrating the species range and longevity of snaR (red box) and CAS (black box) genes, and the possible extent of ASR genes (blue box). HERV-W integration into the primate lineage is indicated. Tree is modified from (75).
Mentions: The major stages of snaR molecular evolution are clearly segregated in the unrooted phylogram shown in Figure 8A. Although the transitions between the stages are accompanied by insertion and deletion events (indels; Figure 3D), they are also characterized by sequence changes (Supplementary Figure S6). A similar phylogram results using an alignment from which the indels were omitted (Supplementary Figure S7). Hence, the stages of snaR evolution are segregated by substitutions between the different molecular species as well as by indels. Strikingly, the evolution of each phylogram cluster in this molecular lineage coincides with major primate speciation events (Figure 8B). Thus, ASR elements are likely to have evolved in Simiiformes with the internal deletion of 17–19 nt from a FLAM C-like ancestor (δ1, Figure 3D). CAS elements probably evolved from ASR via a 3′-deletion (δ2, Figure 3D) in Catarrhines, after their geographical separation from New World Monkeys (Platyrrhines) in the late Eocene (30–45 MYA). The snaR genes appear to have evolved from CAS through two separate internal expansion events (ε1 and ε2, Figure 3D), in the common ancestor of African Great Apes in the Miocene Epoch (9–17 MYA). We conclude that the pathway of snaR gene evolution is characterized by a series of deletions followed by internal duplications, and its principal steps correlate with pivotal events in primate evolution: first, the divergence of simians from prosimians; second, the separation of Old World from New World monkeys; and third, the divergence of the African Great Apes from other apes.Figure 8.

Bottom Line: We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein.The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse.We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, New Jersey Medical School, UMDNJ, Newark, New Jersey, USA.

ABSTRACT
We recently identified the snaR family of small non-coding RNAs that associate in vivo with the nuclear factor 90 (NF90/ILF3) protein. The major human species, snaR-A, is an RNA polymerase III transcript with restricted tissue distribution and orthologs in chimpanzee but not rhesus macaque or mouse. We report their expression in human tissues and their evolution in primates. snaR genes are exclusively in African Great Apes and some are unique to humans. Two novel families of snaR-related genetic elements were found in primates: CAS (catarrhine ancestor of snaR), limited to Old World Monkeys and apes; and ASR (Alu/snaR-related), present in all monkeys and apes. ASR and CAS appear to have spread by retrotransposition, whereas most snaR genes have spread by segmental duplication. snaR-A and snaR-G2 are differentially expressed in discrete regions of the human brain and other tissues, notably including testis. snaR-A is up-regulated in transformed and immortalized human cells, and is stably bound to ribosomes in HeLa cells. We infer that snaR evolved from the left monomer of the primate-specific Alu SINE family via ASR and CAS in conjunction with major primate speciation events, and suggest that snaRs participate in tissue- and species-specific regulation of cell growth and translation.

Show MeSH
Related in: MedlinePlus