Functional & Integrative Genomics

, Volume 11, Issue 3, pp 507–517 | Cite as

Major chimpanzee-specific structural changes in sperm development-associated genes

  • Ryong Nam Kim
  • Dae-Won Kim
  • Sang-Haeng Choi
  • Sung-Hwa Chae
  • Seong-Hyeuk Nam
  • Dong-Wook Kim
  • Aeri Kim
  • Aram Kang
  • Kun-Hyang Park
  • Yong Seok Lee
  • Momoki Hirai
  • Yutaka Suzuki
  • Sumio Sugano
  • Katsuyuki Hashimoto
  • Dae-Soo Kim
  • Hong-Seog Park
Short Communication

Abstract

A comprehensive analysis of transcriptional structures of chimpanzee sperm development-associated genes is of significant interest for deeply understanding sperm development and male reproductive process. In this study, we sequenced 7,680 clones from a chimpanzee testis full-length cDNA library and obtained 1,933 nonredundant high-quality full-length cDNA sequences. Comparative analysis between human and chimpanzee showed that 78 sperm development-associated genes, most of which were yet uncharacterized, had undergone severe structural changes (mutations at the start/stop codons, INDELs, alternative splicing variations and fusion forms) on genomic and transcript levels throughout chimpanzee evolution. Specifically, among the 78 sperm development-associated genes, 39 including ODF2, UBC, and CD59 showed markedly chimpanzee-specific structural changes. Through dN/dS analysis, we found that 56 transcripts (including seven sperm development-associated genes) had values of greater than one when comparing human and chimpanzee DNA sequences, whereas the values were less than one when comparing humans and orangutans. Gene ontology annotation and expression profiling showed that the chimpanzee testis transcriptome was enriched with genes that are associated with chimpanzee male germ cell development. Taken together, our study provides the first comprehensive molecular evidence that many chimpanzee sperm development-associated genes had experienced severe structural changes over the course of evolution on genomic and transcript levels.

Keywords

Structural changes Chimpanzee Testis Sperm development Gene ontology 

Supplementary material

10142_2011_220_MOESM1_ESM.pdf (51 kb)
Supplementary Fig. 1Pipeline for identification and analysis of chimpanzee full-length cDNAs. The procedure of computational semiauto annotation is illustrated step-by-step (PDF 50 kb)
10142_2011_220_MOESM2_ESM.pdf (192 kb)
Supplementary Fig. 2Graphical description of the different patterns observed when comparing with annotated representative human genes corresponding to chimpanzee testis transcripts. a It has 5′-end variation of transcripts. b It has 3′-end variation of transcripts. c It has a specific protein domain due to alternative splicing of specific exon regions of 5′ and 3′ ends. d It is bridging two annotated neighboring genes. e It is a bidirectional transcript overlapping exons of annotated genes. Arrow indicates orientation (PDF 191 kb)
10142_2011_220_MOESM3_ESM.pdf (36 kb)
Supplementary Fig. 3Statistics of alternative splicing patterns in the protein-coding region. Alternative splicing events are divided into seven patterns. Schematic representatives of the exon–intron structure and a total number of alternative splice events in protein-coding regions are given. Alternative exons are depicted in blue. Daggers when we count 5′-end and/or 3′-end alternative splicing events, truncated patterns were not considered (PDF 36 kb)
10142_2011_220_MOESM4_ESM.pdf (241 kb)
Supplementary Fig. 4Gene ontology (GO) assignments (the detailed strategy is shown in “Materials and methods” section). a Biological process. b Molecular function (PDF 240 kb)
10142_2011_220_MOESM5_ESM.pdf (14 kb)
Supplementary Fig. 5a The genome regions of the UBC gene are as follows: human (chr12:123,959,671-123,967,092, March 2006) and chimp (chr12:126,825,938-126,827,500, March 2006). Regions of internal CDSs and UTRs are represented using sky and black boxes, respectively. Red, orange, green, and violet colors indicate the regions of four human repeat sequences deleted from the chimpanzee UBC gene. b Multiple sequence alignment between the four human repeat sequences deleted from the chimpanzee UBC gene (PDF 13 kb)
10142_2011_220_MOESM6_ESM.pdf (8 kb)
Supplementary Table 1List of transcripts with mutations at start or stop codons (PDF 8 kb)
10142_2011_220_MOESM7_ESM.pdf (31 kb)
Supplementary Table 2Summary of chimpanzee testis transcripts showing inserted/deleted sequences with respect to those of human and out-groups (PDF 31 kb)
10142_2011_220_MOESM8_ESM.pdf (75 kb)
Supplementary Table 3Characterization of tandem repeat polymorphisms of UBC in cross-species (PDF 75 kb)
10142_2011_220_MOESM9_ESM.pdf (525 kb)
Supplementary Table 4Alternative splicing patterns in the protein-coding regions (PDF 524 kb)
10142_2011_220_MOESM10_ESM.pdf (11 kb)
Supplementary Table 5Cojoined transcripts (PDF 11 kb)
10142_2011_220_MOESM11_ESM.pdf (29 kb)
Supplementary Table 6dN/dS (PDF 28 kb)
10142_2011_220_MOESM12_ESM.pdf (36 kb)
Supplementary Table 7GO classification of chimpanzee testis transcripts (PDF 35 kb)
10142_2011_220_MOESM13_ESM.pdf (14 kb)
Supplementary Table 8Biological processes and molecular functions of overexpressed genes (PDF 13 kb)
10142_2011_220_MOESM14_ESM.pdf (868 kb)
Supplementary Table 91,933 nonredundant chimpanzee testis transcripts (PDF 868 kb)
10142_2011_220_MOESM15_ESM.pdf (82 kb)
Supplementary Table 10Highly matched transcripts at the nucleotide and/or amino acid level (PDF 82 kb)
10142_2011_220_MOESM16_ESM.pdf (12 kb)
Supplementary Table 11The most highly expressed transcripts revealed from gene expression profiling of chimpanzee testis transcriptome (PDF 12 kb)

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ryong Nam Kim
    • 1
  • Dae-Won Kim
    • 1
    • 8
  • Sang-Haeng Choi
    • 1
  • Sung-Hwa Chae
    • 3
  • Seong-Hyeuk Nam
    • 1
  • Dong-Wook Kim
    • 1
  • Aeri Kim
    • 1
    • 2
  • Aram Kang
    • 1
    • 2
  • Kun-Hyang Park
    • 1
  • Yong Seok Lee
    • 4
  • Momoki Hirai
    • 5
  • Yutaka Suzuki
    • 6
  • Sumio Sugano
    • 6
  • Katsuyuki Hashimoto
    • 7
  • Dae-Soo Kim
    • 1
  • Hong-Seog Park
    • 1
    • 2
  1. 1.Genome Resource CenterKorea Research Institute of Bioscience and Biotechnology (KRIBB)DaejeonSouth Korea
  2. 2.University of Science and Technology (UST)DaejeonSouth Korea
  3. 3.Research Institute of GnC Bio Co. LtdDaejeonSouth Korea
  4. 4.Department of ParasitologyCollege of Medicine and Frontier Inje Research for Science and Technology, Inje UniversityBusanSouth Korea
  5. 5.International Research and Educational Institute for Integrated Medical SciencesTokyo Women’s Medical UniversityTokyoJapan
  6. 6.Department of Medical Genome Sciences, Graduate School of Frontier SciencesThe University of TokyoTokyoJapan
  7. 7.Division of Biomedical Research ResourcesNational Institute of Biomedical InnovationOsakaJapan
  8. 8.Division of Malaria and Parasitic DiseasesNational Institute of HealthSeoulSouth Korea

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