fog-2, a Germ-Line-Specific Sex Determination Gene Required for Hermaphrodite Spermatogenesis in Caenorhabditis elegans

INVESTIGATIONS

fog-2, a Germ-Line-Specific Sex Determination Gene Required for Hermaphrodite Spermatogenesis in Caenorhabditis elegans

T. Schedl and J. Kimble
Laboratory of Cell and Molecular Biology, Graduate School, and Department of Biochemistry, College of Agriculture and Life Sciences, University of Wisconsin, Madison, Wisconsin 53706

This paper describes the isolation and characterization of 16 mutations in the germ-line sex determination gene fog-2 (fog for feminization of the germ line). In the nematode Caenorhabditis elegans there are normally two sexes, self-fertilizing hermaphrodites (XX) and males (XO). Wild-type XX animals are hermaphrodite in the germ line (spermatogenesis followed by oogenesis), and female in the soma. fog-2 loss-of-function mutations transform XX animals into females while XO animals are unaffected. Thus, wild-type fog-2 is necessary for spermatogenesis in hermaphrodites but not males. The fem genes and fog-1 are each essential for specification of spermatogenesis in both XX and XO animals. fog-2 acts as a positive regulator of the fem genes and fog-1. The tra-2 and tra-3 genes act as negative regulators of the fem genes and fog-1 to allow oogenesis. Two models are discussed for how fog-2 might positively regulate the fem genes and fog-1 to permit spermatogenesis; fog-2 may act as a negative regulator of tra-2 and tra-3, or fog-2 may act positively on the fem genes and fog-1 rendering them insensitive to the negative action of tra-2 and tra-3.

This article has been cited by other articles:

V. Katju, E. M. LaBeau, K. J. Lipinski, and U. Bergthorsson
Sex Change by Gene Conversion in a Caenorhabditis elegans fog-2 Mutant
Genetics, September 1, 2008; 180(1): 669 - 672.
[Abstract] [Full Text] [PDF]

S. L. Noble, B. L. Allen, L. K. Goh, K. Nordick, and T. C. Evans
Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development
J. Cell Biol., August 11, 2008; 182(3): 559 - 572.
[Abstract] [Full Text] [PDF]

P. R. Boag, A. Atalay, S. Robida, V. Reinke, and T. K. Blackwell
Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis
J. Cell Biol., August 11, 2008; 182(3): 543 - 557.
[Abstract] [Full Text] [PDF]

S. Miyata, J. Begun, E. R. Troemel, and F. M. Ausubel
DAF-16-Dependent Suppression of Immunity During Reproduction in Caenorhabditis elegans
Genetics, February 1, 2008; 178(2): 903 - 918.
[Abstract] [Full Text] [PDF]

L. R. Garcia, B. LeBoeuf, and P. Koo
Diversity in Mating Behavior of Hermaphroditic and Male-Female Caenorhabditis Nematodes
Genetics, April 1, 2007; 175(4): 1761 - 1771.
[Abstract] [Full Text] [PDF]

M. Shimada, K. Kanematsu, K. Tanaka, H. Yokosawa, and H. Kawahara
Proteasomal Ubiquitin Receptor RPN-10 Controls Sex Determination in Caenorhabditis elegans
Mol. Biol. Cell, December 1, 2006; 17(12): 5356 - 5371.
[Abstract] [Full Text] [PDF]

R. Lyczak, L. Zweier, T. Group, M. A. Murrow, C. Snyder, L. Kulovitz, A. Beatty, K. Smith, and B. Bowerman
The puromycin-sensitive aminopeptidase PAM-1 is required for meiotic exit and anteroposterior polarity in the one-cell Caenorhabditis elegans embryo
Development, November 1, 2006; 133(21): 4281 - 4292.
[Abstract] [Full Text] [PDF]

J. H. Thomas
Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants
Genome Res., August 1, 2006; 16(8): 1017 - 1030.
[Abstract] [Full Text] [PDF]

K. Sato, M. Sato, A. Audhya, K. Oegema, P. Schweinsberg, and B. D. Grant
Dynamic Regulation of Caveolin-1 Trafficking in the Germ Line and Embryo of Caenorhabditis elegans
Mol. Biol. Cell, July 1, 2006; 17(7): 3085 - 3094.
[Abstract] [Full Text] [PDF]

Y. Suzuki and M. Han
Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development.
Genes & Dev., February 15, 2006; 20(4): 423 - 428.
[Abstract] [Full Text] [PDF]

C. Corrigan, R. Subramanian, and M. A. Miller
Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation
Development, December 1, 2005; 132(23): 5225 - 5237.
[Abstract] [Full Text] [PDF]

J. L. Bachorik and J. Kimble
Redundant control of the Caenorhabditis elegans sperm/oocyte switch by PUF-8 and FBF-1, two distinct PUF RNA-binding proteins
PNAS, August 2, 2005; 102(31): 10893 - 10897.
[Abstract] [Full Text] [PDF]

K. Sha and A. Fire
Imprinting Capacity of Gamete Lineages in Caenorhabditis elegans
Genetics, August 1, 2005; 170(4): 1633 - 1652.
[Abstract] [Full Text] [PDF]

E. M. Maine, D. Hansen, D. Springer, and V. E. Vought
Caenorhabditis elegans atx-2 Promotes Germline Proliferation and the Oocyte Fate
Genetics, October 1, 2004; 168(2): 817 - 830.
[Abstract] [Full Text] [PDF]

R. Ciosk, M. DePalma, and J. R. Priess
ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline
Development, October 1, 2004; 131(19): 4831 - 4841.
[Abstract] [Full Text] [PDF]

L. D. Mathies, M. Schvarzstein, K. M. Morphy, R. Blelloch, A. M. Spence, and J. Kimble
TRA-1/GLI controls development of somatic gonadal precursors in C. elegans
Development, September 1, 2004; 131(17): 4333 - 4343.
[Abstract] [Full Text] [PDF]

J. Lipton, G. Kleemann, R. Ghosh, R. Lints, and S. W. Emmons
Mate Searching in Caenorhabditis elegans: A Genetic Model for Sex Drive in a Simple Invertebrate
J. Neurosci., August 25, 2004; 24(34): 7427 - 7434.
[Abstract] [Full Text] [PDF]

M. A. Miller, P. J. Ruest, M. Kosinski, S. K. Hanks, and D. Greenstein
An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans
Genes & Dev., January 15, 2003; 17(2): 187 - 200.
[Abstract] [Full Text] [PDF]

J. Hodgkin
Exploring the Envelope: Systematic Alteration in the Sex-Determination System of the Nematode Caenorhabditis elegans
Genetics, October 1, 2002; 162(2): 767 - 780.
[Abstract] [Full Text] [PDF]

A. D. Stewart and P. C. Phillips
Selection and Maintenance of Androdioecy in Caenorhabditis elegans
Genetics, March 1, 2002; 160(3): 975 - 982.
[Abstract] [Full Text] [PDF]

N. Arantes-Oliveira, J. Apfeld, A. Dillin, and C. Kenyon
Regulation of Life-Span by Germ-Line Stem Cells in Caenorhabditis elegans
Science, January 18, 2002; 295(5554): 502 - 505.
[Abstract] [Full Text] [PDF]

M.-H. Lee and T. Schedl
Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development
Genes & Dev., September 15, 2001; 15(18): 2408 - 2420.
[Abstract] [Full Text] [PDF]

R. E. Navarro, E. Y. Shim, Y. Kohara, A. Singson, and T. K. Blackwell
cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans
Development, September 1, 2001; 128(17): 3221 - 3232.
[Abstract] [Full Text] [PDF]

P.-J. Chen, S. Cho, S.-W. Jin, and R. E. Ellis
Specification of Germ Cell Fates by FOG-3 Has Been Conserved During Nematode Evolution
Genetics, August 1, 2001; 158(4): 1513 - 1525.
[Abstract] [Full Text] [PDF]

M. A. Miller, V. Q. Nguyen, M.-H. Lee, M. Kosinski, T. Schedl, R. M. Caprioli, and D. Greenstein
A Sperm Cytoskeletal Protein That Signals Oocyte Meiotic Maturation and Ovulation
Science, March 16, 2001; 291(5511): 2144 - 2147.
[Abstract] [Full Text]

D. H. Lum, P. E. Kuwabara, D. Zarkower, and A. M. Spence
Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans
Genes & Dev., December 15, 2000; 14(24): 3153 - 3165.
[Abstract] [Full Text]

E. S. Haag and J. Kimble
Regulatory Elements Required for Development of Caenorhabditis elegans Hermaphrodites Are Conserved in the tra-2 Homologue of C. remanei, a Male/Female Sister Species
Genetics, May 1, 2000; 155(1): 105 - 116.
[Abstract] [Full Text]

D. Gems and D. L. Riddle
Genetic, Behavioral and Environmental Determinants of Male Longevity in Caenorhabditis elegans
Genetics, April 1, 2000; 154(4): 1597 - 1610.
[Abstract] [Full Text]

S. R. Thompson, E. B. Goodwin, and M. Wickens
Rapid Deadenylation and Poly(A)-Dependent Translational Repression Mediated by the Caenorhabditis elegans tra-2 3' Untranslated Region in Xenopus Embryos
Mol. Cell. Biol., March 15, 2000; 20(6): 2129 - 2137.
[Abstract] [Full Text]

R Clifford, M. Lee, S Nayak, M Ohmachi, F Giorgini, and T Schedl
FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline
Development, January 12, 2000; 127(24): 5265 - 5276.
[Abstract] [PDF]

K. Kuznicki, P. Smith, W. Leung-Chiu, A. Estevez, H. Scott, and K. Bennett
Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans
Development, January 7, 2000; 127(13): 2907 - 2916.
[Abstract] [PDF]

A. Mehra, J. Gaudet, L. Heck, P. E. Kuwabara, and A. M. Spence
Negative regulation of male development in Caenorhabditis elegans by a protein-protein interaction between TRA-2A and FEM-3
Genes & Dev., June 1, 1999; 13(11): 1453 - 1463.
[Abstract] [Full Text]

J. M. Schumacher, A. Golden, and P. J. Donovan
AIR-2: An Aurora/Ipl1-related Protein Kinase Associated with Chromosomes and Midbody Microtubules Is Required for Polar Body Extrusion and Cytokinesis in Caenorhabditis elegans Embryos
J. Cell Biol., December 14, 1998; 143(6): 1635 - 1646.
[Abstract] [Full Text] [PDF]

A. Puoti, M. Gallegos, B. Zhang, M.P. Wickens, and J. Kimble
Controls of Cell Fate and Pattern by 3' Untranslated Regions: The Caenorhabditis elegans Sperm/Oocyte Decision
Cold Spring Harb Symp Quant Biol, January 1, 1997; 62(0): 19 - 24.
[Abstract] [PDF]

S. Parkhurst and P. Meneely
Sex determination and dosage compensation: lessons from flies and worms
Science, May 13, 1994; 264(5161): 924 - 932.
[Abstract] [PDF]

S. Mango, E. Lambie, and J Kimble
The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans
Development, January 10, 1994; 120(10): 3019 - 3031.
[Abstract] [PDF]

L Chen, M Krause, M Sepanski, and A Fire
The Caenorhabditis elegans MYOD homologue HLH-1 is essential for proper muscle function and complete morphogenesis
Development, January 6, 1994; 120(6): 1631 - 1641.
[Abstract] [PDF]

C Kenyon
The nematode Caenorhabditis elegans
Science, June 10, 1988; 240(4858): 1448 - 1453.
[Abstract] [PDF]

				S. L. Noble, B. L. Allen, L. K. Goh, K. Nordick, and T. C. Evans Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development J. Cell Biol., August 11, 2008; 182(3): 559 - 572. [Abstract] [Full Text] [PDF]

				P. R. Boag, A. Atalay, S. Robida, V. Reinke, and T. K. Blackwell Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis J. Cell Biol., August 11, 2008; 182(3): 543 - 557. [Abstract] [Full Text] [PDF]

				S. Miyata, J. Begun, E. R. Troemel, and F. M. Ausubel DAF-16-Dependent Suppression of Immunity During Reproduction in Caenorhabditis elegans Genetics, February 1, 2008; 178(2): 903 - 918. [Abstract] [Full Text] [PDF]

				L. R. Garcia, B. LeBoeuf, and P. Koo Diversity in Mating Behavior of Hermaphroditic and Male-Female Caenorhabditis Nematodes Genetics, April 1, 2007; 175(4): 1761 - 1771. [Abstract] [Full Text] [PDF]

				M. Shimada, K. Kanematsu, K. Tanaka, H. Yokosawa, and H. Kawahara Proteasomal Ubiquitin Receptor RPN-10 Controls Sex Determination in Caenorhabditis elegans Mol. Biol. Cell, December 1, 2006; 17(12): 5356 - 5371. [Abstract] [Full Text] [PDF]

				R. Lyczak, L. Zweier, T. Group, M. A. Murrow, C. Snyder, L. Kulovitz, A. Beatty, K. Smith, and B. Bowerman The puromycin-sensitive aminopeptidase PAM-1 is required for meiotic exit and anteroposterior polarity in the one-cell Caenorhabditis elegans embryo Development, November 1, 2006; 133(21): 4281 - 4292. [Abstract] [Full Text] [PDF]

				J. H. Thomas Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants Genome Res., August 1, 2006; 16(8): 1017 - 1030. [Abstract] [Full Text] [PDF]

				K. Sato, M. Sato, A. Audhya, K. Oegema, P. Schweinsberg, and B. D. Grant Dynamic Regulation of Caveolin-1 Trafficking in the Germ Line and Embryo of Caenorhabditis elegans Mol. Biol. Cell, July 1, 2006; 17(7): 3085 - 3094. [Abstract] [Full Text] [PDF]

				Y. Suzuki and M. Han Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Genes & Dev., February 15, 2006; 20(4): 423 - 428. [Abstract] [Full Text] [PDF]

				C. Corrigan, R. Subramanian, and M. A. Miller Eph and NMDA receptors control Ca2+/calmodulin-dependent protein kinase II activation during C. elegans oocyte meiotic maturation Development, December 1, 2005; 132(23): 5225 - 5237. [Abstract] [Full Text] [PDF]

				J. L. Bachorik and J. Kimble Redundant control of the Caenorhabditis elegans sperm/oocyte switch by PUF-8 and FBF-1, two distinct PUF RNA-binding proteins PNAS, August 2, 2005; 102(31): 10893 - 10897. [Abstract] [Full Text] [PDF]

				K. Sha and A. Fire Imprinting Capacity of Gamete Lineages in Caenorhabditis elegans Genetics, August 1, 2005; 170(4): 1633 - 1652. [Abstract] [Full Text] [PDF]

				E. M. Maine, D. Hansen, D. Springer, and V. E. Vought Caenorhabditis elegans atx-2 Promotes Germline Proliferation and the Oocyte Fate Genetics, October 1, 2004; 168(2): 817 - 830. [Abstract] [Full Text] [PDF]

				R. Ciosk, M. DePalma, and J. R. Priess ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline Development, October 1, 2004; 131(19): 4831 - 4841. [Abstract] [Full Text] [PDF]

				L. D. Mathies, M. Schvarzstein, K. M. Morphy, R. Blelloch, A. M. Spence, and J. Kimble TRA-1/GLI controls development of somatic gonadal precursors in C. elegans Development, September 1, 2004; 131(17): 4333 - 4343. [Abstract] [Full Text] [PDF]

				J. Lipton, G. Kleemann, R. Ghosh, R. Lints, and S. W. Emmons Mate Searching in Caenorhabditis elegans: A Genetic Model for Sex Drive in a Simple Invertebrate J. Neurosci., August 25, 2004; 24(34): 7427 - 7434. [Abstract] [Full Text] [PDF]

				M. A. Miller, P. J. Ruest, M. Kosinski, S. K. Hanks, and D. Greenstein An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans Genes & Dev., January 15, 2003; 17(2): 187 - 200. [Abstract] [Full Text] [PDF]

				J. Hodgkin Exploring the Envelope: Systematic Alteration in the Sex-Determination System of the Nematode Caenorhabditis elegans Genetics, October 1, 2002; 162(2): 767 - 780. [Abstract] [Full Text] [PDF]

				A. D. Stewart and P. C. Phillips Selection and Maintenance of Androdioecy in Caenorhabditis elegans Genetics, March 1, 2002; 160(3): 975 - 982. [Abstract] [Full Text] [PDF]

				N. Arantes-Oliveira, J. Apfeld, A. Dillin, and C. Kenyon Regulation of Life-Span by Germ-Line Stem Cells in Caenorhabditis elegans Science, January 18, 2002; 295(5554): 502 - 505. [Abstract] [Full Text] [PDF]

				M.-H. Lee and T. Schedl Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development Genes & Dev., September 15, 2001; 15(18): 2408 - 2420. [Abstract] [Full Text] [PDF]

				R. E. Navarro, E. Y. Shim, Y. Kohara, A. Singson, and T. K. Blackwell cgh-1, a conserved predicted RNA helicase required for gametogenesis and protection from physiological germline apoptosis in C. elegans Development, September 1, 2001; 128(17): 3221 - 3232. [Abstract] [Full Text] [PDF]

				P.-J. Chen, S. Cho, S.-W. Jin, and R. E. Ellis Specification of Germ Cell Fates by FOG-3 Has Been Conserved During Nematode Evolution Genetics, August 1, 2001; 158(4): 1513 - 1525. [Abstract] [Full Text] [PDF]

				M. A. Miller, V. Q. Nguyen, M.-H. Lee, M. Kosinski, T. Schedl, R. M. Caprioli, and D. Greenstein A Sperm Cytoskeletal Protein That Signals Oocyte Meiotic Maturation and Ovulation Science, March 16, 2001; 291(5511): 2144 - 2147. [Abstract] [Full Text]

				D. H. Lum, P. E. Kuwabara, D. Zarkower, and A. M. Spence Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans Genes & Dev., December 15, 2000; 14(24): 3153 - 3165. [Abstract] [Full Text]

				E. S. Haag and J. Kimble Regulatory Elements Required for Development of Caenorhabditis elegans Hermaphrodites Are Conserved in the tra-2 Homologue of C. remanei, a Male/Female Sister Species Genetics, May 1, 2000; 155(1): 105 - 116. [Abstract] [Full Text]

				D. Gems and D. L. Riddle Genetic, Behavioral and Environmental Determinants of Male Longevity in Caenorhabditis elegans Genetics, April 1, 2000; 154(4): 1597 - 1610. [Abstract] [Full Text]

				S. R. Thompson, E. B. Goodwin, and M. Wickens Rapid Deadenylation and Poly(A)-Dependent Translational Repression Mediated by the Caenorhabditis elegans tra-2 3' Untranslated Region in Xenopus Embryos Mol. Cell. Biol., March 15, 2000; 20(6): 2129 - 2137. [Abstract] [Full Text]

				R Clifford, M. Lee, S Nayak, M Ohmachi, F Giorgini, and T Schedl FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline Development, January 12, 2000; 127(24): 5265 - 5276. [Abstract] [PDF]

				K. Kuznicki, P. Smith, W. Leung-Chiu, A. Estevez, H. Scott, and K. Bennett Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans Development, January 7, 2000; 127(13): 2907 - 2916. [Abstract] [PDF]