A New Dataset of Spermatogenic vs. Oogenic Transcriptomes in the Nematode Caenorhabditis elegans

Abstract

The nematode Caenorhabditis elegans is an important model for studies of germ cell biology, including the meiotic cell cycle, gamete specification as sperm or oocyte, and gamete development. Fundamental to those studies is a genome-level knowledge of the germline transcriptome. Here, we use RNA-Seq to identify genes expressed in isolated XX gonads, which are approximately 95% germline and 5% somatic gonadal tissue. We generate data from mutants making either sperm [fem-3(q96)] or oocytes [fog-2(q71)], both grown at 22°. Our dataset identifies a total of 10,754 mRNAs in the polyadenylated transcriptome of XX gonads, with 2748 enriched in spermatogenic gonads, 1732 enriched in oogenic gonads, and the remaining 6274 not enriched in either. These spermatogenic, oogenic, and gender-neutral gene datasets compare well with those of previous studies, but double the number of genes identified. A comparison of the additional genes found in our study with in situ hybridization patterns in the Kohara database suggests that most are expressed in the germline. We also query our RNA-Seq data for differential exon usage and find 351 mRNAs with sex-enriched isoforms. We suggest that this new dataset will prove useful for studies focusing on C. elegans germ cell biology.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 48

1. 1.

   Albritton S. E. Kranz A. L. Rao P. Kramer M. Dieterich C., 2014 Sex-biased gene expression and evolution of the X chromosome in nematodes. Genetics 197: 865–883

   Not in our library10.1534/genetics.114.163311

2. 2.
   Differential expression analysis for sequence count data · 2010

   No notice
3. 3.

   Anders S. Reyes A. Huber W., 2012 Detecting differential usage of exons from RNA-seq data. Genome Res. 22: 2008–2017

   Not in our library10.1101/gr.133744.111

4. 4.

   Barton M. K. Schedl T. B. Kimble J., 1987 Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115: 107–119

   Not in our library10.1093/genetics/115.1.107

5. 5.

   Baugh L. R. Hill A. A. Slonim D. K. Brown E. L. Hunter C. P., 2003 Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 130: 889–900

   Not in our library10.1242/dev.00302

6. 6.

   C. elegans Sequencing Consortium, 1998 Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282: 2012–2018.

   Not in our library10.1126/science.282.5396.2012

7. 7.

   Chen P.-J. Singal A. Kimble J. Ellis R. E., 2000 A novel member of the Tob family of proteins controls sexual fate in Caenorhabditis elegans germ cells. Dev. Biol. 217: 77–90

   Not in our library10.1006/dbio.1999.9521

8. 8.

   Chik J. K. Schriemer D. C. Childs S. J. McGhee J. D., 2011 Proteome of the Caenorhabditis elegans oocyte. J. Proteome Res. 10: 2300–2305

   Not in our library10.1021/pr101124f

9. 9.

   Conine C. C. Moresco J. J. Gu W. Shirayama M. Conte D. Jr., 2013 Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans. Cell 155: 1532–1544

   Not in our library10.1016/j.cell.2013.11.032

10. 10.

    Dernburg A. F. McDonald K. Moulder G. Barstead R. Dresser M., 1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387–398

    Not in our library10.1016/s0092-8674(00)81481-6

11. 11.

    Detwiler M. R. Reuben M. Li X. Rogers E. Lin R., 2001 Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev. Cell 1: 187–199

    Not in our library10.1016/s1534-5807(01)00026-0

12. 12.

    Ellis, R., and T. Schedl, 2007 Sex determination in the germ line. WormBook Mar 5: 1–13. 10.1895/wormbook.1.82.2.

    Not in our library10.1895/wormbook.1.82.2

13. 13.
    Ensembl 2014 · 2013

    No notice
14. 14.

    Geles K. G. Adam S. A., 2001 Germline and developmental roles of the nuclear transport factor importin α3 in C. elegans. Development 128: 1817–1830

    Not in our library10.1242/dev.128.10.1817

15. 15.

    Gerstein M. B. Lu Z. J. Van Nostrand E. L. Cheng C. Arshinoff B. I., 2010 Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775–1787

    Not in our library10.1126/science.1196914

16. 16.

    Grant B. Hirsh D., 1999 Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10: 4311–4326

    Not in our library10.1091/mbc.10.12.4311

17. 17.

    Greenstein, D., 2005 Control of oocyte meiotic maturation and fertilization. WormBook Dec 28 1–12. 10.1895/wormbook.1.53.1.

    Not in our library10.1895/wormbook.1.53.1

18. 18.

    Hirsh D. Oppenheim D. Klass M., 1976 Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 49: 200–219

    Not in our library10.1016/0012-1606(76)90267-0

19. 19.

    Jaramillo-Lambert A. Ellefson M. Villeneuve A. M. Engebrecht J., 2007 Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 308: 206–221

    Not in our library10.1016/j.ydbio.2007.05.019

20. 20.

    Jungkamp A. C. Stoeckius M. Mecenas D. Grun D. Mastrobuoni G., 2011 In vivo and transcriptome-wide identification of RNA binding protein target sites. Mol. Cell 44: 828–840

    Not in our library10.1016/j.molcel.2011.11.009

21. 21.

    Kerins J. A. Hanazawa M. Dorsett M. Schedl T., 2010 PRP-17 and the pre-mRNA splicing pathway are preferentially required for the proliferation vs. meiotic development decision and germline sex determination in Caenorhabditis elegans. Dev. Dyn. 239: 1555–1572

    Not in our library10.1002/dvdy.22274

22. 22.

    Kershner A. M. Kimble J., 2010 Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator. Proc. Natl. Acad. Sci. USA 107: 3936–3941

    Not in our library10.1073/pnas.1000495107

23. 23.

    Kim K. W. Nykamp K. Suh N. Bachorik J. L. Wang L., 2009 Antagonism between GLD-2 binding partners controls gamete sex. Dev. Cell 16: 723–733

    Not in our library10.1016/j.devcel.2009.04.002

24. 24.

    Kim K. W. Wilson T. L. Kimble J., 2010 GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc. Natl. Acad. Sci. USA 107: 17445–17450

    Not in our library10.1073/pnas.1012611107

25. 25.

    Kimble J. Crittenden S. L., 2007 Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 23: 405–433

    Not in our library10.1146/annurev.cellbio.23.090506.123326

26. 26.

    Kudron M. Niu W. Lu Z. Wang G. Gerstein M., 2013 Tissue-specific direct targets of Caenorhabditis elegans Rb/E2F dictate distinct somatic and germline programs. Genome Biol. 14: R5

    Not in our library10.1186/gb-2013-14-1-r5

27. 27.

    Kulkarni M. Shakes D. C. Guevel K. Smith H. E., 2012 SPE-44 implements sperm cell fate. PLoS Genet. 8: e1002678

    Not in our library10.1371/journal.pgen.1002678

28. 28.

    L’Hernault, S. W., 2006 Spermatogenesis. WormBook Feb 20 1–14. 10.1895/wormbook.1.85.1.

    Not in our library10.1895/wormbook.1.85.1

29. 29.

    Li H. Handsaker B. Wysoker A. Fennell T. Ruan J., 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079

    Not in our library10.1093/bioinformatics/btp352

30. 30.

    Luitjens C. Gallegos M. Kraemer B. Kimble J. Wickens M., 2000 CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev. 14: 2596–2609

    Not in our library10.1101/gad.831700

31. 31.

    Ma X. Zhu Y. Li C. Xue P. Zhao Y., 2014 Characterisation of Caenorhabditis elegans sperm transcriptome and proteome. BMC Genomics 15: 168

    Not in our library10.1186/1471-2164-15-168

32. 32.

    Morgan D. E. Crittenden S. L. Kimble J., 2010 The C. elegans adult male germline: Stem cells and sexual dimorphism. Dev. Biol. 346: 204–214

    Not in our library10.1016/j.ydbio.2010.07.022

33. 33.

    Okkema P. G. Kimble J., 1991 Molecular analysis of tra-2, a sex determining gene in Caenorhabditis elegans. EMBO J. 10: 171–176

    Not in our library10.1002/j.1460-2075.1991.tb07933.x

34. 34.

    Puoti A. Kimble J., 1999 The Caenorhabditis elegans sex determination gene mog-1 encodes a member of the DEAH-box protein family. Mol. Cell. Biol. 19: 2189–2197

    Not in our library10.1128/mcb.19.3.2189

35. 35.
    The hermaphrodite sperm/oocyte switch requires the Caenorhabditis elegans homologs of PRP2 and PRP22 · 2000

    Not checked
36. 36.
    Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data · 2013

    Corrected
37. 37.

    Reinke V. Gil I. S. Ward S. Kazmer K., 2004 Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311–323

    Not in our library10.1242/dev.00914

38. 38.

    Reinke V. Smith H. E. Nance J. Wang J. Van Doren C., 2000 A global profile of germline gene expression in C. elegans. Mol. Cell 6: 605–616

    Not in our library10.1016/s1097-2765(00)00059-9

39. 39.

    Rog O. Dernburg A. F., 2013 Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr. Opin. Cell Biol. 25: 349–356

    Not in our library10.1016/j.ceb.2013.03.003

40. 40.

    Schedl T. Kimble J., 1988 fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43–61

    Not in our library10.1093/genetics/119.1.43

Cited by papers we hold 1

• A comprehensive survey of C. elegans argonaute proteins reveals organism-wide gene regulatory networks and functions · 2023
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.