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Human and Chimpanzee Chorionic Gonadotropin Beta Genes Pille Hallast1, Janna Saarela2, Aarno Palotie3,4,5 and Maris Laan*1

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Human and Chimpanzee Chorionic Gonadotropin Beta Genes Pille Hallast1, Janna Saarela2, Aarno Palotie3,4,5 and Maris Laan*1 BMC Evolutionary Biology BioMed Central Research article Open Access High divergence in primate-specific duplicated regions: Human and chimpanzee Chorionic Gonadotropin Beta genes Pille Hallast1, Janna Saarela2, Aarno Palotie3,4,5 and Maris Laan*1 Address: 1Department of Biotechnology, Institute of Molecular and Cell Biology, University of Tartu, Riia 23, 51010 Tartu, Estonia, 2Department of Molecular Medicine, National Public Health Institute, Haartmaninkatu 8, 00290 Helsinki, Finland, 3Finnish Genome Center, Biomedicum Helsinki, University of Helsinki, Haartmaninkatu 8, 00290 Helsinki, Finland, 4The Broad Institute of Harvard and MIT, Cambridge Center, Cambridge, MA 02142, USA and 5Wellcome Trust Sanger Institute, Hinxton, Cambridge, CB10 1SA, UK Email: Pille Hallast - [email protected]; Janna Saarela - [email protected]; Aarno Palotie - [email protected]; Maris Laan* - [email protected] * Corresponding author Published: 7 July 2008 Received: 29 August 2007 Accepted: 7 July 2008 BMC Evolutionary Biology 2008, 8:195 doi:10.1186/1471-2148-8-195 This article is available from: http://www.biomedcentral.com/1471-2148/8/195 © 2008 Hallast et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Low nucleotide divergence between human and chimpanzee does not sufficiently explain the species-specific morphological, physiological and behavioral traits. As gene duplication is a major prerequisite for the emergence of new genes and novel biological processes, comparative studies of human and chimpanzee duplicated genes may assist in understanding the mechanisms behind primate evolution. We addressed the divergence between human and chimpanzee duplicated genomic regions by using Luteinizing Hormone Beta (LHB)/Chorionic Gonadotropin Beta (CGB) gene cluster as a model. The placental CGB genes that are essential for implantation have evolved from an ancestral pituitary LHB gene by duplications in the primate lineage. Results: We shotgun sequenced and compared the human (45,165 bp) and chimpanzee (39,876 bp) LHB/CGB regions and hereby present evidence for structural variation resulting in discordant number of CGB genes (6 in human, 5 in chimpanzee). The scenario of species-specific parallel duplications was supported (i) as the most parsimonious solution requiring the least rearrangement events to explain the interspecies structural differences; (ii) by the phylogenetic trees constructed with fragments of intergenic regions; (iii) by the sequence similarity calculations. Across the orthologous regions of LHB/CGB cluster, substitutions and indels contributed approximately equally to the interspecies divergence and the distribution of nucleotide identity was correlated with the regional repeat content. Intraspecies gene conversion may have shaped the LHB/CGB gene cluster. The substitution divergence (1.8–2.59%) exceeded two-three fold the estimates for single-copy loci and the fraction of transversional mutations was increased compared to the unique sequences (43% versus ~30%). Despite the high sequence identity among LHB/CGB genes, there are signs of functional differentiation among the gene copies. Estimates for dn/ds rate ratio suggested a purifying selection on LHB and CGB8, and a positive evolution of CGB1. Conclusion: If generalized, our data suggests that in addition to species-specific deletions and duplications, parallel duplication events may have contributed to genetic differences separating humans from their closest relatives. Compared to unique genomic segments, duplicated regions are characterized by high divergence promoted by intraspecies gene conversion and species-specific chromosomal rearrangements, including the alterations in gene copy number. Page 1 of 14 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:195 http://www.biomedcentral.com/1471-2148/8/195 Background gested that CGB gene first arose in the common ancestor Gene duplication has long been considered as one of the of the anthropoid primates after diverging from tarsiers main mechanisms of the adaptive evolution and as an [16]. important source of the genetic novelty [1]. Differential duplications and deletions of chromosomal regions We have chosen LHB/CGB genomic region as a model to including coding genes provide a powerful source for the study the evolution of recent primate duplications. evolution of species-specific biological differences [2]. Although the chimpanzee genome has been sequenced, Compared to other mammals, the genomes of primates there are still large gaps and uncertainties concerning the show an enrichment of large segmental duplications with segmental duplications regions, including the LHB/CGB high levels (>90%) of sequence identity [3]. In the human region. To obtain a high-quality DNA sequence, we con- genome particularly pronounced expansions of the copy structed and sequenced a shot-gun library, and hereby number have been reported for genes involved in the report the complete sequence of the entire LHB/CGB clus- structure and function of the brain [4]. In comparison of ter in the common chimpanzee. We are addressing the fol- human and its closest relative chimpanzee, large duplica- lowing aspects regarding to the evolution of duplicated tions contribute considerably (2.7%; [5]) to the overall genes in closely related species: (i) in-depth comparison divergence compared to single base pair substitutions of the human and chimpanzee LHB/CGB genome clusters; (1.2–1.5%; [2,6-12]). In addition to providing the sub- (ii) variation in substitution rates; (iii) genic and inter- strate for non-allelic homologous recombination mediat- genic divergences; (iv) impact of intraspecies gene conver- ing genomic disorders (reviewed by [13]), the duplication sion in phylogeny, divergence and transversion/transition architecture of a genome may also influence normal phe- ratios; (v) evidence of natural selection. To our knowl- notypic variation. It has been estimated that ~20% of seg- edge, this is the first detailed report of parallel independ- mental duplications are polymorphic within human and ent duplication events initiated within a duplicated chimpanzee populations contributing to intraspecies genome cluster and leading to structural divergence in the diversity [5,14]. Despite the fact that segmental duplica- two sister-species, human and common chimpanzee. tions cover a substantial fraction of the great apes genomes, the experimental data on the divergence and Results and Discussion detailed evolutionary dynamics of duplicated gene Human and chimpanzee LHB/CGB genome clusters differ regions is still limited. Sequence comparison of dupli- considerably in size cated genes in sister-species would assist in understanding The total length of the sequenced chimpanzee (Ch) LHB/ the mechanisms behind primate evolution and in associ- CGB genomic region obtained from two overlapping BAC ating the genetic divergence with phenotypic diversifica- clones was 43,945 bp. It encompasses 1,029 bp of the tion. flanking (centromeric side) RUVBL2 gene, 39,876 bp of the entire LHB/CGB cluster and 2,986 bp of the flanking One of the genomic regions that has evolved through sev- (telomeric side) NTF5 gene (Figure 1B; Genbank submis- eral gene duplication events in primate lineage is the sion: EU000308). Compared to the human (Hu) LHB/ Luteinizing Hormone Beta (LHB)/Chorionic Gonadotro- CGB region (Genbank: NG_000019), the sequence of the pin Beta (CGB) gene cluster locating in human at ChLHB/CGB cluster is 5,289 bp shorter. The sequence 19q13.32. The LHB/CGB genes have an essential role in characteristics of the LHB/CGB genomic regions are simi- reproduction: placentally expressed HCG hormone con- lar in these two species: extremely high GC-nucleotide tributes to the implantation process of the embryo during content (57% compared to average 41% for Hu and Ch the early stages of pregnancy, pituitary expressed luteiniz- [10]), high fraction of CpG islands (Hu 6.6%, Ch 6.1% ing hormone promotes the ovulation and luteinization of compared to estimated 1–3.5% for Hu and Ch [6,8]) and follicles and stimulates the steroidogenesis. In human, the repetitive sequences (Hu 26.9%, Ch 25.15%), especially cluster consists of seven highly homologous genes: an SINEs (Hu 23.23%, Ch 21.81%) (Additional file 1). High ancestral LHB and six duplicated CGB genes [15]. The data repeat content is also characteristic to several other dupli- from other primates supports the hypothesis of several cated regions, such as MHC class I region [7] and Apolipo- sequential duplication events increasing gradually the protein CI genomic segment [17]. number of CGB genes among primates from one (New World monkeys: the owl monkey, Aotus trivirgatus and the As expected, there is a considerable similarity between the dusky titi monkey, Callicebus moloch) to six in human (Fig- genomic organization of human and chimpanzee LHB/ ure 1A). The mapped copy number of the CGB gene CGB clusters (Figure 1B). We identified two highly identi- among Old World monkeys varies: three in rhesus cal, apparently orthologous segments within the cluster: macaque (Macaca mulatta), five in guereza monkey (Colo- RUVBL2/LHB/intergenic region A (Ch 8,084 bp, Hu 7,973 bus guereza) and dusky leaf monkey (Presbytis obscura), bp; 96% sequence identity)
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