Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution
The southern muriqui (Brachyteles arachnoides) is the largest neotropical primate. This species is endemic to Brazil and is currently critically endangered due to its habitat destruction. The genetic basis underlying adaptive traits of New World monkeys has been a subject of interest to several inve...
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Frontiers Media S.A.
2020-07-01
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author | Daniel A. Moreira Alessandra P. Lamarca Rafael Ferreira Soares Ana M. A. Coelho Carolina Furtado Nicole M. Scherer Miguel A. M. Moreira Hector N. Seuánez Mariana Boroni |
author_facet | Daniel A. Moreira Alessandra P. Lamarca Rafael Ferreira Soares Ana M. A. Coelho Carolina Furtado Nicole M. Scherer Miguel A. M. Moreira Hector N. Seuánez Mariana Boroni |
author_sort | Daniel A. Moreira |
collection | DOAJ |
description | The southern muriqui (Brachyteles arachnoides) is the largest neotropical primate. This species is endemic to Brazil and is currently critically endangered due to its habitat destruction. The genetic basis underlying adaptive traits of New World monkeys has been a subject of interest to several investigators, with significant concern about genes related to the immune system. In the absence of a reference genome, RNA-seq and de novo transcriptome assembly have proved to be valuable genetic procedures for accessing gene sequences and testing evolutionary hypotheses. We present here a first report on the sequencing, assembly, annotation and adaptive selection analysis for thousands of transcripts of B. arachnoides from two different samples, corresponding to 13 different blood cells and fibroblasts. We assembled 284,283 transcripts with N50 of 2,940 bp, with a high rate of complete transcripts, with a median high scoring pair coverage of 88.2%, including low expressed transcripts, accounting for 72.3% of complete BUSCOs. We could predict and extract 81,400 coding sequences with 79.8% of significant BLAST hit against the Euarchontoglires SwissProt dataset. Of these 64,929 sequences, 34,084 were considered homologous to Supraprimate proteins, and of the remaining sequences (30,845), 94% were associated with a protein domain or a KEGG Orthology group, indicating potentially novel or specific protein-coding genes of B. arachnoides. We use the predicted protein sequences to perform a comparative analysis with 10 other primates. This analysis revealed, for the first time in an Atelid species, an expansion of APOBEC3G, extending this knowledge to all NWM families. Using a branch-site model, we searched for evidence of positive selection in 4,533 orthologous sets. This evolutionary analysis revealed 132 amino acid sites in 30 genes potentially evolving under positive selection, shedding light on primate genome evolution. These genes belonged to a wide variety of categories, including those encoding the innate immune system proteins (APOBEC3G, OAS2, and CEACAM1) among others related to the immune response. This work generated a set of thousands of complete sequences that can be used in other studies on molecular evolution and may help to unveil the evolution of primate genes. Still, further functional studies are required to provide an understanding of the underlying evolutionary forces modeling the primate genome. |
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spelling | doaj.art-1e5fd8d121f34aada6743f9e1c35e9672022-12-21T18:59:19ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-07-011110.3389/fgene.2020.00831551290Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive EvolutionDaniel A. Moreira0Alessandra P. Lamarca1Rafael Ferreira Soares2Ana M. A. Coelho3Carolina Furtado4Nicole M. Scherer5Miguel A. M. Moreira6Hector N. Seuánez7Mariana Boroni8Laboratory of Bioinformatics and Computational Biology, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilLaboratory of Bioinformatics and Molecular Evolution, Department of Genetics, Institute of Biology, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilLaboratory for Functional Genomics and Bioinformatics, Oswaldo Cruz Institute, Fiocruz, Rio de Janeiro, BrazilDepartment of Genetics, Institute of Biology, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, BrazilGenetics Program, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilLaboratory of Bioinformatics and Computational Biology, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilGenetics Program, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilGenetics Program, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilLaboratory of Bioinformatics and Computational Biology, Division of Experimental and Translational Research, Brazilian National Cancer Institute (INCA), Rio de Janeiro, BrazilThe southern muriqui (Brachyteles arachnoides) is the largest neotropical primate. This species is endemic to Brazil and is currently critically endangered due to its habitat destruction. The genetic basis underlying adaptive traits of New World monkeys has been a subject of interest to several investigators, with significant concern about genes related to the immune system. In the absence of a reference genome, RNA-seq and de novo transcriptome assembly have proved to be valuable genetic procedures for accessing gene sequences and testing evolutionary hypotheses. We present here a first report on the sequencing, assembly, annotation and adaptive selection analysis for thousands of transcripts of B. arachnoides from two different samples, corresponding to 13 different blood cells and fibroblasts. We assembled 284,283 transcripts with N50 of 2,940 bp, with a high rate of complete transcripts, with a median high scoring pair coverage of 88.2%, including low expressed transcripts, accounting for 72.3% of complete BUSCOs. We could predict and extract 81,400 coding sequences with 79.8% of significant BLAST hit against the Euarchontoglires SwissProt dataset. Of these 64,929 sequences, 34,084 were considered homologous to Supraprimate proteins, and of the remaining sequences (30,845), 94% were associated with a protein domain or a KEGG Orthology group, indicating potentially novel or specific protein-coding genes of B. arachnoides. We use the predicted protein sequences to perform a comparative analysis with 10 other primates. This analysis revealed, for the first time in an Atelid species, an expansion of APOBEC3G, extending this knowledge to all NWM families. Using a branch-site model, we searched for evidence of positive selection in 4,533 orthologous sets. This evolutionary analysis revealed 132 amino acid sites in 30 genes potentially evolving under positive selection, shedding light on primate genome evolution. These genes belonged to a wide variety of categories, including those encoding the innate immune system proteins (APOBEC3G, OAS2, and CEACAM1) among others related to the immune response. This work generated a set of thousands of complete sequences that can be used in other studies on molecular evolution and may help to unveil the evolution of primate genes. Still, further functional studies are required to provide an understanding of the underlying evolutionary forces modeling the primate genome.https://www.frontiersin.org/article/10.3389/fgene.2020.00831/fullRNA-seqde novo transcriptome assemblyprimatepositive selectionimmune system |
spellingShingle | Daniel A. Moreira Alessandra P. Lamarca Rafael Ferreira Soares Ana M. A. Coelho Carolina Furtado Nicole M. Scherer Miguel A. M. Moreira Hector N. Seuánez Mariana Boroni Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution Frontiers in Genetics RNA-seq de novo transcriptome assembly primate positive selection immune system |
title | Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution |
title_full | Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution |
title_fullStr | Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution |
title_full_unstemmed | Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution |
title_short | Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution |
title_sort | transcriptome of the southern muriqui brachyteles arachnoides primates platyrrhini a critically endangered new world monkey evidence of adaptive evolution |
topic | RNA-seq de novo transcriptome assembly primate positive selection immune system |
url | https://www.frontiersin.org/article/10.3389/fgene.2020.00831/full |
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