Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Front Genet
2020 Apr 30;11:831. doi: 10.3389/fgene.2020.00831.
Show Gene links
Show Anatomy links
Transcriptome of the Southern Muriqui Brachyteles arachnoides (Primates:Platyrrhini), a Critically Endangered New World Monkey: Evidence of Adaptive Evolution.
Moreira DA
,
Lamarca AP
,
Soares RF
,
Coelho AMA
,
Furtado C
,
Scherer NM
,
Moreira MAM
,
Seuánez HN
,
Boroni M
.
???displayArticle.abstract???
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.
FIGURE 1. Expression profiles of the Brachyteles arachnoides transcriptome from blood cells and fibroblasts. (A) Venn diagram comparing all CDS with BLAST hit expressed (TPM ≥ 1) by blood cells and fibroblasts. (B) Venn diagram comparing the number of CDS homologous to proteins of the innate immune system. (C) HSP coverage plotted against TPM values with marginal density plots considering all CDS. (D) HSP coverage plotted against TPM values with marginal density plots considering CDS homologous to proteins of the innate immune system.
FIGURE 2. Orthogroups intersections among 11 primate species. The top bar plot represents the number of orthogroups intersections. The bottom-left bar plot represents the number of orthogroups per species. The dots indicate the intersections among the species with at least 50 shared orthogroups.
FIGURE 3. Maximum likelihood phylogeny of primate APOBEC3Gs. A PhyML tree of aligned amino acid sequences. Human and NWM APOBEC3As were used to root the tree. A cluster with NWM APOBEC3Gs and retrocopies are shown in pink. The sister clade of OWM, Great Apes and Human APOBEC3Gs are shown in light pink. The scale bar represents the amino acid substitution rate, using the Blosum62 + GAMMA model. NWM APOBEC3Gs sequences associated with RefSeq accessions are marked with hash sign (#).
FIGURE 4. Alignment of CEACAM1 proteins from nine primate species. Human and B. arachnoides sequences are displayed in the first lines to allow a direct comparison of the altered amino acids. Nine primate sequences were compared to the predicted peptide sequence of B. arachnoides. Numbering corresponds to amino acid (aa) positions considered in the FEL analysis for positively selected sites. Boxes correspond to protein domains and lines point to positively selected aa substitutions.
FIGURE 5. 3D Model of APOBEC3G homodimer. Electrostatic profile of B. arachnoides
(A) and H. sapiens
(B) APOBEC3G: the bluest zones on protein surface represent values +74.419 KT/ec; the reddest zones represent values −74.419 KT/ec of the electrostatic properties; white regions mean zero values of the electrostatic potential. (C) The structural alignment between APOBEC3G Homo sapiens models (gold cartoon) and B. arachnoides (gray cartoon). (D) Template used for structural modeling, showing the homodimeric interaction between two APOBEC3Gs. Insets show residues (in sticks) under positive selection in muriqui sequence, border color of insets corresponds to each specific highlighted region in C.
Akkaya,
How do pathogens drive the evolution of paired receptors?
2013, Pubmed
Akkaya,
How do pathogens drive the evolution of paired receptors?
2013,
Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Angulo,
C-type lectin 17A and macrophage-expressed receptor genes are magnified by fungal β-glucan after Vibrio parahaemolyticus infection in Totoaba macdonaldi cells.
2019,
Pubmed
Baker,
Electrostatics of nanosystems: application to microtubules and the ribosome.
2001,
Pubmed
Barkhash,
Variability in the 2'-5'-oligoadenylate synthetase gene cluster is associated with human predisposition to tick-borne encephalitis virus-induced disease.
2010,
Pubmed
Barreiro,
From evolutionary genetics to human immunology: how selection shapes host defence genes.
2010,
Pubmed
Bentz,
Tissue-specific expression profiles and positive selection analysis in the tree swallow (Tachycineta bicolor) using a de novo transcriptome assembly.
2019,
Pubmed
Boddy,
Evidence of a Conserved Molecular Response to Selection for Increased Brain Size in Primates.
2017,
Pubmed
Boehm,
Structural models for carcinoembryonic antigen and its complex with the single-chain Fv antibody molecule MFE23.
2000,
Pubmed
Bolger,
Trimmomatic: a flexible trimmer for Illumina sequence data.
2014,
Pubmed
Bulliard,
Functional analysis and structural modeling of human APOBEC3G reveal the role of evolutionarily conserved elements in the inhibition of human immunodeficiency virus type 1 infection and Alu transposition.
2009,
Pubmed
Chaves,
Phylogeographic evidence for two species of muriqui (genus Brachyteles).
2019,
Pubmed
,
Echinobase
Chiu,
The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements.
2008,
Pubmed
Darc,
Molecular evolution of α4 integrin binding site to lentiviral envelope proteins in new world primates.
2012,
Pubmed
Daugherty,
Rules of engagement: molecular insights from host-virus arms races.
2012,
Pubmed
Di Fiore,
The rise and fall of a genus: Complete mtDNA genomes shed light on the phylogenetic position of yellow-tailed woolly monkeys, Lagothrix flavicauda, and on the evolutionary history of the family Atelidae (Primates: Platyrrhini).
2015,
Pubmed
Dolinsky,
PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations.
2007,
Pubmed
Emms,
OrthoFinder: phylogenetic orthology inference for comparative genomics.
2019,
Pubmed
Fam,
AVPR1b variation and the emergence of adaptive phenotypes in Platyrrhini primates.
2019,
Pubmed
Fletcher,
The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection.
2010,
Pubmed
Fu,
CD-HIT: accelerated for clustering the next-generation sequencing data.
2012,
Pubmed
George,
Trans genomic capture and sequencing of primate exomes reveals new targets of positive selection.
2011,
Pubmed
Grabherr,
Full-length transcriptome assembly from RNA-Seq data without a reference genome.
2011,
Pubmed
Graham,
Prolectin, a glycan-binding receptor on dividing B cells in germinal centers.
2009,
Pubmed
Guindon,
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.
2010,
Pubmed
Haas,
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis.
2013,
Pubmed
Hancks,
Overlapping Patterns of Rapid Evolution in the Nucleic Acid Sensors cGAS and OAS1 Suggest a Common Mechanism of Pathogen Antagonism and Escape.
2015,
Pubmed
Hauck,
Cellular adhesion molecules as targets for bacterial infection.
2006,
Pubmed
He,
Extracellular matrix protein 1 promotes follicular helper T cell differentiation and antibody production.
2018,
Pubmed
Hu,
SLC15A2 and SLC15A4 Mediate the Transport of Bacterially Derived Di/Tripeptides To Enhance the Nucleotide-Binding Oligomerization Domain-Dependent Immune Response in Mouse Bone Marrow-Derived Macrophages.
2018,
Pubmed
Huerta-Cepas,
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper.
2017,
Pubmed
Huerta-Cepas,
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses.
2019,
Pubmed
Hulme,
Selective inhibition of Alu retrotransposition by APOBEC3G.
2007,
Pubmed
Hultquist,
Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1.
2011,
Pubmed
International Human Genome Sequencing Consortium,
Finishing the euchromatic sequence of the human genome.
2004,
Pubmed
Kaján,
Virus-Host Coevolution with a Focus on Animal and Human DNA Viruses.
2020,
Pubmed
Kammerer,
Species-specific evolution of immune receptor tyrosine based activation motif-containing CEACAM1-related immune receptors in the dog.
2007,
Pubmed
Kammerer,
Identification of allelic variants of the bovine immune regulatory molecule CEACAM1 implies a pathogen-driven evolution.
2004,
Pubmed
Kammerer,
Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families.
2010,
Pubmed
Katoh,
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.
2013,
Pubmed
Kosakovsky Pond,
Not so different after all: a comparison of methods for detecting amino acid sites under selection.
2005,
Pubmed
Kosiol,
Patterns of positive selection in six Mammalian genomes.
2008,
Pubmed
Krupp,
APOBEC3G polymorphism as a selective barrier to cross-species transmission and emergence of pathogenic SIV and AIDS in a primate host.
2013,
Pubmed
Kuespert,
CEACAMs: their role in physiology and pathophysiology.
2006,
Pubmed
Lan,
De novo transcriptome assembly and positive selection analysis of an individual deep-sea fish.
2018,
Pubmed
Langmead,
Fast gapped-read alignment with Bowtie 2.
2012,
Pubmed
Li,
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.
2011,
Pubmed
Li,
Evaluation of de novo transcriptome assemblies from RNA-Seq data.
2014,
Pubmed
Lim,
Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man.
2009,
Pubmed
Losse,
Factor H and factor H-related protein 1 bind to human neutrophils via complement receptor 3, mediate attachment to Candida albicans, and enhance neutrophil antimicrobial activity.
2010,
Pubmed
Madeira,
The EMBL-EBI search and sequence analysis tools APIs in 2019.
2019,
Pubmed
Maudhoo,
De novo assembly of the common marmoset transcriptome from NextGen mRNA sequences.
2014,
Pubmed
Mbisa,
APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms.
2010,
Pubmed
Monath,
Review of the risks and benefits of yellow fever vaccination including some new analyses.
2012,
Pubmed
Mozzi,
OASes and STING: adaptive evolution in concert.
2015,
Pubmed
Murrell,
Gene-wide identification of episodic selection.
2015,
Pubmed
Navaratnam,
An overview of cytidine deaminases.
2006,
Pubmed
Navarro,
Complementary function of the two catalytic domains of APOBEC3G.
2005,
Pubmed
Newman,
Robust enumeration of cell subsets from tissue expression profiles.
2015,
Pubmed
Newman,
Determining cell type abundance and expression from bulk tissues with digital cytometry.
2019,
Pubmed
Nguyen,
IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.
2015,
Pubmed
Nielsen,
A scan for positively selected genes in the genomes of humans and chimpanzees.
2005,
Pubmed
Olival,
Host and viral traits predict zoonotic spillover from mammals.
2017,
Pubmed
Perelman,
A molecular phylogeny of living primates.
2011,
Pubmed
Perlman,
Another Decade, Another Coronavirus.
2020,
Pubmed
Perry,
Comparative RNA sequencing reveals substantial genetic variation in endangered primates.
2012,
Pubmed
Possas,
Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation.
2018,
Pubmed
Rausell,
Genomics of host-pathogen interactions.
2014,
Pubmed
Ribeiro,
Evolution of cyclophilin A and TRIMCyp retrotransposition in New World primates.
2005,
Pubmed
Ribeiro,
CCR5 chemokine receptor gene evolution in New World monkeys (Platyrrhini, Primates): implication on resistance to lentiviruses.
2005,
Pubmed
Sarkar,
The nature of the catalytic domain of 2'-5'-oligoadenylate synthetases.
1999,
Pubmed
Sawyer,
Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G.
2004,
Pubmed
Schmieder,
Quality control and preprocessing of metagenomic datasets.
2011,
Pubmed
Schneider,
Can molecular data place each neotropical monkey in its own branch?
2001,
Pubmed
Schneider,
Molecular phylogeny of the New World monkeys (Platyrrhini, primates).
1993,
Pubmed
Schrago,
Chronology of deep nodes in the neotropical primate phylogeny: insights from mitochondrial genomes.
2012,
Pubmed
,
Echinobase
Silva,
Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease.
2020,
Pubmed
Simão,
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs.
2015,
Pubmed
Smith,
Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection.
2015,
Pubmed
Soares,
Evolution of TRIM5alpha B30.2 (SPRY) domain in New World primates.
2010,
Pubmed
Stapley,
Adaptation genomics: the next generation.
2010,
Pubmed
Strier,
Demographic monitoring of wild muriqui populations: Criteria for defining priority areas and monitoring intensity.
2017,
Pubmed
,
Echinobase
Strier,
Status of the northern muriqui (Brachyteles hypoxanthus) in the time of yellow fever.
2019,
Pubmed
Thamizhmani,
Association of dengue virus infection susceptibility with polymorphisms of 2'-5'-oligoadenylate synthetase genes: a case-control study.
2014,
Pubmed
Thompson,
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
1994,
Pubmed
Unni,
Web servers and services for electrostatics calculations with APBS and PDB2PQR.
2011,
Pubmed
Vargas-Pinilla,
Evolutionary pattern in the OXT-OXTR system in primates: coevolution and positive selection footprints.
2015,
Pubmed
Voges,
CEACAM1 recognition by bacterial pathogens is species-specific.
2010,
Pubmed
Wang,
WebGestalt 2017: a more comprehensive, powerful, flexible and interactive gene set enrichment analysis toolkit.
2017,
Pubmed
Webb,
Comparative Protein Structure Modeling Using MODELLER.
2016,
Pubmed
Williams,
Inhibition of protein synthesis by 2'-5' linked adenine oligonucleotides in intact cells.
1978,
Pubmed
Yang,
Understanding the structural basis of HIV-1 restriction by the full length double-domain APOBEC3G.
2020,
Pubmed
Yang,
Retrocopying expands the functional repertoire of APOBEC3 antiviral proteins in primates.
2020,
Pubmed
Yang,
Comprehensive transcriptome analysis reveals accelerated genic evolution in a Tibet fish, Gymnodiptychus pachycheilus.
2014,
Pubmed
Yang,
PAML 4: phylogenetic analysis by maximum likelihood.
2007,
Pubmed
Zimmermann,
Coevolution of paired receptors in Xenopus carcinoembryonic antigen-related cell adhesion molecule families suggests appropriation as pathogen receptors.
2016,
Pubmed
de Oliveira,
Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus.
2005,
Pubmed
,
Echinobase