A sex-specific transcription factor controls male identity in a simultaneous hermaphrodite

Nature Communications

Volumn 4, Issue , 2013, Pages

  Chong, Tracy ^a   Collins, James J ^a   Brubacher, John L ^b   Zarkower, David ^c   Newmark, Phillip A ^a,d  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Canadian Mennonite University   (Canada)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DMD 1 PROTEIN; MALE ABNORMAL 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL; DEVELOPMENTAL BIOLOGY; FLATWORM; GENE EXPRESSION; HERMAPHRODITE; IDENTIFICATION METHOD; MALE; METAZOAN; REPRODUCTIVE BEHAVIOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GENE EXPRESSION; GERM CELL; HERMAPHRODITISM; LOPHOTROCHOZOA; MALE; MALE GENITAL SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; REGENERATION; SCHMIDTEA MEDITERRANEA; SEXUAL DEVELOPMENT; TESTIS; TURBELLARIA;

ANIMALS; BRAIN; CELL DIFFERENTIATION; DISORDERS OF SEX DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENES, HELMINTH; GENITALIA, MALE; GERM CELLS; MALE; MOLECULAR SEQUENCE DATA; NEURONS; PLANARIANS; REGENERATION; REPRODUCTION, ASEXUAL; SEQUENCE HOMOLOGY, AMINO ACID; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS;

ANIMALIA; LOPHOTROCHOZOA; METAZOA; PLANARIA; PLATYHELMINTHES; SCHISTOSOMA MANSONI; SCHMIDTEA MEDITERRANEA;

EID: 84878725585     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2811     Document Type: Article

References (60)

1. Basch, P. F. Why do schistosomes have separate sexes? Parasitol. Today 6, 160-163 (1990)
2. Kiontke, K. et al. Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc. Natl Acad. Sci. USA 101, 9003-9008 (2004) (Pubitemid 38781600)
3. Eppley, S. M. & Jesson, L. K. Moving to mate: the evolution of separate and combined sexes in multicellular organisms. J. Evol. Biol. 21, 727-736 (2008) (Pubitemid 351521551)
4. Bull, J. J. Sex determination in reptiles. Q. Rev. Biol. 55, 3-21 (1980)
5. Koopman, P., Munsterberg, A., Capel, B., Vivian, N. & Lovell-Badge, R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348, 450-452 (1990) (Pubitemid 120015087)
6. Williams, T. M. & Carroll, S. B. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat. Rev. Genet. 10, 797-804 (2009)
7. Kimble, J. & Crittenden, S. L. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell. Dev. Biol. 23, 405-433 (2007)
8. Kimble, J. & Page, D. C. The mysteries of sexual identity. The germ cell's perspective. Science 316, 400-401 (2007) (Pubitemid 46651478)
9. Blackler, A. W. Germ-cell transfer and sex ratio in Xenopus Laevis. J. Embryol. Exp. Morphol. 13, 51-61 (1965)
10. Hilfiker-Kleiner, D., Dubendorfer, A., Hilfiker, A. & Nothiger, R. Genetic control of sex determination in the germ line and soma of the housefly, Musca domestica. Development 120, 2531-2538 (1994) (Pubitemid 24268827)
11. Casper, A. L. & Van Doren, M. The establishment of sexual identity in the Drosophila germline. Development 136, 3821-3830 (2009)
12. Durcova-Hills, G. & Capel, B. Development of germ cells in the mouse. Curr. Top. Dev. Biol. 83, 185-212 (2008)
13. Steinmann-Zwicky, M., Schmid, H. & Nothiger, R. Cell-autonomous and inductive signals can determine the sex of the germ line of Drosophila by regulating the gene Sxl. Cell 57, 157-166 (1989) (Pubitemid 19098877)
14. Kato, Y., Kobayashi, K., Watanabe, H. & Iguchi, T. Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet. 7, e1001345 (2011)
15. Matson, C. K. et al. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev. Cell 19, 612-624 (2010)
16. Matson, C. K. et al. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476, 101-104 (2011)
17. Matson, C. K. & Zarkower, D. Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat. Rev. Genet. 13, 163-174 (2012)
18. Matsuda, M. et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417, 559-563 (2002) (Pubitemid 34595924)
19. Miller, S. W. et al. A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol. Dev. 5, 251-258 (2003) (Pubitemid 36684609)
20. Raymond, C. S. et al. Evidence for evolutionary conservation of sexdetermining genes. Nature 391, 691-695 (1998) (Pubitemid 28113214)
21. Smith, C. A. et al. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461, 267-271 (2009)
22. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990)
23. Volff, J. N., Zarkower, D., Bardwell, V. J. & Schartl, M. Evolutionary dynamics of the DM domain gene family in metazoans. J. Mol. Evol. 57(Suppl 1): S241-S249 (2003) (Pubitemid 37544013)
24. Newmark, P. A., Wang, Y. & Chong, T. Germ cell specification and regeneration in planarians. Cold Spring Harb. Symp. Quant. Biol. 73, 573-581 (2008)
25. Handberg-Thorsager, M. & Salo, E. The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev. Genes Evol. 217, 403-411 (2007) (Pubitemid 46681652)
26. Sato, K. et al. Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Dev. Growth Differ. 48, 615-628 (2006) (Pubitemid 44722183)
27. Wang, Y., Zayas, R. M., Guo, T. & Newmark, P. A. nanos function is essential for development and regeneration of planarian germ cells. Proc. Natl Acad. Sci. USA 104, 5901-5906 (2007) (Pubitemid 47175631)
28. Chong, T., Stary, J. M., Wang, Y. & Newmark, P. A. Molecular markers to characterize the hermaphroditic reproductive system of the planarian Schmidtea mediterranea. BMC Dev. Biol. 11, 69 (2011)
29. Wang, Y., Stary, J. M., Wilhelm, J. E. & Newmark, P. A. A functional genomic screen in planarians identifies novel regulators of germ cell development. Genes Dev. 24, 2081-2092 (2010)
30. Roberts-Galbraith, R. H. & Newmark, P. A. Follistatin antagonizes Activin signaling and acts with Notum to direct planarian head regeneration. Proc. Natl Acad. Sci. USA 110, 1363-1368 (2013)
31. Wenemoser, D. & Reddien, P. W. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol. 344, 979-991 (2010)
32. Wagner, D. E., Wang, I. E. & Reddien, P. W. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332, 811-816 (2011)
33. Eisenhoffer, G. T., Kang, H. & Sanchez Alvarado, A. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian. Schmidtea mediterranea. Cell Stem Cell 3, 327-339 (2008)
34. Reddien, P. W., Oviedo, N. J., Jennings, J. R., Jenkin, J. C. & Sanchez Alvarado, A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310, 1327-1330 (2005) (Pubitemid 41698864)
35. Guo, T., Peters, A. H. F. M. & Newmark, P. A. A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell 11, 159-169 (2006) (Pubitemid 44138497)
36. Scimone, M. L., Srivastava, M., Bell, G. W. & Reddien, P. W. A regulatory program for excretory system regeneration in planarians. Development 138, 4387-4398 (2011)
37. Hyman, L. The Invertebrates, Vol II: Platyhelminthes and Rhynchocoela (McGraw-Hill Book Company, Inc., New York, 1951)
38. Schwartz, N. B. & McCormack, C. E. Reproduction: gonadal function and its regulation. Annu. Rev. Physiol. 34, 425-472 (1972)
39. Steinberger, E. Hormonal control of mammalian spermatogenesis. Physiol. Rev. 51, 1-22 (1971)
40. Kimura, K., Hachiya, T., Koganezawa, M., Tazawa, T. & Yamamoto, D. Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59, 759-769 (2008)
41. Rezaval, C. et al. Neural circuitry underlying Drosophila female postmating behavioral responses. Curr. Biol. 22, 1155-1165 (2012)
42. Barrios, A., Nurrish, S. & Emmons, S. W. Sensory regulation of C. elegans male mate-searching behavior. Curr. Biol. 18, 1865-1871 (2008)
43. Portman, D. S. Genetic control of sex differences in C. elegans neurobiology and behavior. Adv. Genet. 59, 1-37 (2007)
44. White, J. Q. & Jorgensen, E. M. Sensation in a single neuron pair represses male behavior in hermaphrodites. Neuron 75, 593-600 (2012)
45. Ghirardelli, E. Regeneration in Animals and Related Problems 177-184 (North- Holland Publishing Co., Amsterdam, 1965)
46. Collins, III J. J. et al. Genome-wide analyses reveal a role for peptide hormones in planarian germline development. PLoS Biol. 8, e1000509 (2010)
47. Zarkower, D. DMRT genes in vertebrate gametogenesis. Curr. Top. Dev. Biol. 102, 327-356 (2013)
48. Braendle, C. & Felix, M. A. Sex determination: ways to evolve a hermaphrodite. Curr. Biol. 16, R468-R471 (2006) (Pubitemid 43867302)
49. Baldi, C., Cho, S. & Ellis, R. E. Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326, 1002-1005 (2009)
50. Cebria, F. & Newmark, P. A. Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 132, 3691-3703 (2005) (Pubitemid 41301106)
51. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007) (Pubitemid 350162903)
52. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011)
53. Dimmic, M. W., Rest, J. S., Mindell, D. P. & Goldstein, R. A. rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J. Mol. Evol. 55, 65-73 (2002) (Pubitemid 34634360)
54. Rouhana, L. et al. RNA interference by feeding in vitro synthesized doublestranded RNA to planarians: Methodology and dynamics. Dev. Dyn. (e-pub ahead of print 26 February 2013; doi:10.1002/dvdy.23950)
55. Reddien, P. W., Bermange, A. L., Murfitt, K. J., Jennings, J. R. & Sanchez Alvarado, A. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell 8, 635-649 (2005) (Pubitemid 40585288)
56. Pearson, B. J. et al. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn. 238, 443-450 (2009)
57. King, R. S. & Newmark, P. A. An in situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev. Biol. 13, 8 (2013)
58. Rouhana, L., Vieira, A. P., Roberts-Galbraith, R. H. & Newmark, P. A. PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells. Development 139, 1083-1094 (2012)
59. Lewis, F. Schistosomiasis. Curr. Protoc. Immunol Chapter 19, Unit 19 1 (2001)
60. Campos, A., Cummings, M. P., Reyes, J. L. & Laclette, J. P. Phylogenetic relationships of platyhelminthes based on 18S ribosomal gene sequences. Mol. Phylogenet. Evol. 10, 1-10 (1998). (Pubitemid 128350702)