An LTR Retrotransposon-Derived Gene Displays Lineage-Specific Structural and Putative Species-Specific Functional Variations in Eutherians.

Masahito Irie,Tomoko Kaneko-Ishino,Akihiko Koga,Fumitoshi Ishino

doi:10.3389/fchem.2016.00026

Masahito Irie, Tomoko Kaneko-Ishino + Show 2 more

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https://doi.org/10.3389/fchem.2016.00026

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Abstract

Amongst the 11 eutherian-specific genes acquired from a sushi-ichi retrotransposon is the CCHC type zinc-finger protein-encoding gene SIRH11/ZCCHC16. Its contribution to eutherian brain evolution is implied because of its involvement in cognitive function in mice, possibly via the noradrenergic system. Although, the possibility that Sirh11/Zcchc16 functions as a non-coding RNA still remains, dN/dS ratios in pairwise comparisons between its orthologs have provided supportive evidence that it acts as a protein. It became a pseudogene in armadillos (Cingulata) and sloths (Pilosa), the only two extant orders of xenarthra, which prompted us to examine the lineage-specific variations of SIRH11/ZCCHC16 in eutherians. We examined the predicted SIRH11/ZCCHC16 open reading frame (ORF) in 95 eutherian species based on the genomic DNA information in GenBank. A large variation in the SIRH11/ZCCHC16 ORF was detected in several lineages. These include a lack of a CCHC RNA-binding domain in its C-terminus, observed in gibbons (Hylobatidae: Primates) and megabats (Megachiroptera: Chiroptera). A lack of the N-terminal half, on the other hand, was observed in New World monkeys (Platyrrhini: Primates) and species belonging to New World and African Hystricognaths (Caviomorpha and Bathyergidae: Rodents) along with Cetacea and Ruminantia (Cetartiodactyla). Among the hominoids, interestingly, three out of four genera of gibbons have lost normal SIRH11/ZCCHC16 function by deletion or the lack of the CCHC RNA-binding domain. Our extensive dN/dS analysis suggests that such truncated SIRH11/ZCCHC16 ORFs are functionally diversified even within lineages. Combined, our results show that SIRH11/ZCCHC16 may contribute to the diversification of eutherians by lineage-specific structural changes after its domestication in the common eutherian ancestor, followed by putative species-specific functional changes that enhanced fitness and occurred as a consequence of complex natural selection events.

Highlights

Mutation and selection are two principal factors in the Darwinian theory of evolution
It is of interest to determine the roles genes acquired from long terminal repeat (LTR) retrotransposons play in organisms in the current form of the developmental system as well as in the course of biological evolution
We found that SIRH11/ZCCHC16 displays lineage-specific structural variations in eutherians, such as the lack of the CCHC RNA-binding domain or the N-terminal half, as well as species-specific variations in the resulting truncated open reading frame (ORF)

Summary

Introduction

Mutation and selection are two principal factors in the Darwinian theory of evolution. Among all the other eutherianspecific SIRH genes, PEG11/RTL1/SIRH2 (Paternally expressed 11/Retrotransposon-like 1) and SIRH7/LDOC1 (Leucine zipper, downregulated in cancer 1) have been shown to have essential placental functions (Charlier et al, 2001; Edwards et al, 2008; Kagami et al, 2008; Sekita et al, 2008; Naruse et al, 2014), such as maintenance of fetal capillaries and the differentiation/maturation of a variety of placental cells, respectively All of this evidence provides strong support for the contribution of SIRH genes to the evolution of viviparity in mammals via their eutherian-specific functions (Kaneko-Ishino and Ishino, 2012, 2015)

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