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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Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Genetics
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Online Access:https://www.frontiersin.org/article/10.3389/fgene.2020.00831/full
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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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