Abstract
During spermatogenesis, pluripotent germ cells differentiate to become efficient delivery vehicles to the oocyte of paternal DNA. Though male and female germ cells both undergo meiosis to produce haploid complements of DNA, at the same time they also each undergo distinct differentiation processes that result in either sperm or oocytes. This review will discuss our current understanding of mechanisms of sperm formation and differentiation in Caenorhabditis elegans gained from studies that employ a combination of molecular, transcriptomic, and cell biological approaches. Many of these processes also occur during spermatogenesis in other organisms but with differences in timing, molecular machinery, and morphology. In C. elegans, sperm differentiation is implemented by varied modes of gene regulation, including the genomic organization of genes important for sperm formation, the generation of sperm-specific small RNAs, and the interplay of specific transcriptional activators. As sperm formation progresses, chromatin is systematically remodeled to allow first for the implementation of differentiation programs, then for sperm-specific DNA packaging required for transit of paternal genetic and epigenetic information. Sperm also exhibit distinctive features of meiotic progression, including the formation of a unique karyosome state and the centrosomal-based segregation of chromosomes during symmetric meiotic divisions. Sperm-specific organelles are also assembled and remodeled as cells complete meiosis and individualize in preparation for activation, morphogenesis, and the acquisition of motility. Finally, in addition to DNA, sperm contribute specific cellular factors that contribute to successful embryogenesis.
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References
Achanzar WE, Ward S (1997) A nematode gene required for sperm vesicle fusion. J Cell Sci 110(Pt 9):1073–1081
Aitken RJ, De Iuliis GN (2007) Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online 14(6):727–733
Albertson DG (1984) Formation of the first cleavage spindle in nematode embryos. Dev Biol 101(1):61–72
Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1(1):15–26
Aoki K, Moriguchi H, Yoshioka T, Okawa K, Tabara H (2007) In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans. EMBO J 26(24):5007–5019
Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442(7099):203–207
Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318(5851):761–764
Arduengo PM, Appleberry OK, Chuang P, L’Hernault SW (1998) The presenilin protein family member SPE-4 localizes to an ER/Golgi derived organelle and is required for proper cytoplasmic partitioning during Caenorhabditis elegans spermatogenesis. J Cell Sci 111(Pt 24):3645–3654
Arico JK, Katz DJ, van der Vlag J, Kelly WG (2011) Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells. PLoS Genet 7(6):e1001391
Bae YK, Kim E, L’Hernault SW, Barr MM (2009) The CIL-1 PI 5-phosphatase localizes TRP Polycystins to cilia and activates sperm in C. elegans. Curr Biol 19(19):1599–1607
Bamps S, Hope IA (2008) Large-scale gene expression pattern analysis, in situ, in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7(3):175–183
Barton MK, Schedl TB, Kimble J (1987) Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans. Genetics 115(1):107–119
Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, Kasschau KD, Chaves DA, Gu W, Vasale JJ, Duan S, Conte D Jr, Luo S, Schroth GP, Carrington JC, Bartel DP, Mello CC (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31(1):67–78
Beanan MJ, Strome S (1992) Characterization of a germ-line proliferation mutation in C. elegans. Development 116(3):755–766
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409(6818):363–366
Beshore EL, McEwen TJ, Jud MC, Marshall JK, Schisa JA, Bennett KL (2011) C. elegans dicer interacts with the P-granule component GLH-1 and both regulate germline RNPs. Dev Biol 350(2):370–381
Bettegowda A, Wilkinson MF (2011) Transcription and post-transcriptional regulation of spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365(1546):1637–1651
Braun RE (2001) Packaging paternal chromosomes with protamine. Nat Genet 28(1):10–12
Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128(6):1089–1103
Browning H, Strome S (1996) A sperm-supplied factor required for embryogenesis in C. elegans. Development 122(1):391–404
Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, Schumacher JM, Golden A (2006) The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133(4):697–709
Buttery SM, Ekman GC, Seavy M, Stewart M, Roberts TM (2003) Dissection of the Ascaris sperm motility machinery identifies key proteins involved in major sperm protein-based amoeboid locomotion. Mol Biol Cell 14(12):5082–5088
Byrd DT, Kimble J (2009) Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin Cell Dev Biol 20(9):1107–1113
Caron C, Govin J, Rousseaux S, Khochbin S (2005) How to pack the genome for a safe trip. Prog Mol Subcell Biol 38:65–89
Chatterjee I, Richmond A, Putiri E, Shakes DC, Singson A (2005) The Caenorhabditis elegans spe-38 gene encodes a novel four-pass integral membrane protein required for sperm function at fertilization. Development 132(12):2795–2808
Chu D, Liu H, Nix P, Wu T, Ralston E, Yates J, Meyer B (2006) Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 443(7107):101–105
Conine CC, Batista PJ, Gu W, Claycomb JM, Chaves DA, Shirayama M, Mello CC (2010) Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26 G-RNAs and thermotolerant sperm in Caenorhabditis elegans. Proc Natl Acad Sci USA 107(8):3588–3593
Cowan CR, Hyman AA (2004) Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 431(7004):92–96
Dammermann A, Maddox PS, Desai A, Oegema K (2008) SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the gamma-tubulin-mediated addition of centriolar microtubules. J Cell Biol 180(4):771–785
Das PP, Bagijn MP, Goldstein LD, Woolford JR, Lehrbach NJ, Sapetschnig A, Buhecha HR, Gilchrist MJ, Howe KL, Stark R, Matthews N, Berezikov E, Ketting RF, Tavare S, Miska EA (2008) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol Cell 31(1):79–90
del Castillo-Olivares A, Kulkarni M, Smith HE (2009) Regulation of sperm gene expression by the GATA factor ELT-1. Dev Biol 333(2):397–408
Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2(6):819–830
Dernburg AF (2001) Here, there, and everywhere: kinetochore function on holocentric chromosomes. J Cell Biol 153(6):F33–F38
Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO (2000) A conserved checkpoint pathway mediates DNA damage—induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5(3):435–443
Geldziler B, Chatterjee I, Singson A (2005) The genetic and molecular analysis of spe-19, a gene required for sperm activation in Caenorhabditis elegans. Dev Biol 283(2):424–436
Gent JI, Schvarzstein M, Villeneuve AM, Gu SG, Jantsch V, Fire AZ, Baudrimont A (2009) A Caenorhabditis elegans RNA-directed RNA polymerase in sperm development and endogenous RNAi. Genetics 183(4):1297–1314
Gleason EJ, Lindsey WC, Kroft TL, Singson AW, L’Hernault SW (2006) spe-10 encodes a DHHC-CRD zinc-finger membrane protein required for endoplasmic reticulum/Golgi membrane morphogenesis during Caenorhabditis elegans spermatogenesis. Genetics 172(1):145–158
Golden A, Sadler PL, Wallenfang MR, Schumacher JM, Hamill DR, Bates G, Bowerman B, Seydoux G, Shakes DC (2000) Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J Cell Biol 151(7):1469–1482
Golden DE, Gerbasi VR, Sontheimer EJ (2008) An inside job for siRNAs. Mol Cell 31(3):309–312
Goldstein B, Hird SN (1996) Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122(5):1467–1474
Gosney R, Liau WS, Lamunyon CW (2008) A novel function for the presenilin family member spe-4: inhibition of spermatid activation in Caenorhabditis elegans. BMC Dev Biol 8:44
Govin J, Caron C, Lestrat C, Rousseaux S, Khochbin S (2004) The role of histones in chromatin remodelling during mammalian spermiogenesis. Eur J Biochem 271(17):3459–3469
Grishok A, Pasquinelli AE, Conte D, Li N, Parrish S, Ha I, Baillie DL, Fire A, Ruvkun G, Mello CC (2001) Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106(1):23–34
Grivna ST, Beyret E, Wang Z, Lin H (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20(13):1709–1714
Gruzova MN, Parfenov VN (1993) Karyosphere in oogenesis and intranuclear morphogenesis. Int Rev Cytol 144:1–52
Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC (2007) A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315(5818):1587–1590
Hamill DR, Severson AF, Carter JC, Bowerman B (2002) Centrosome maturation and mitotic spindle assembly in C. elegans require SPD-5, a protein with multiple coiled-coil domains. Dev Cell 3(5):673–684
Han T, Manoharan AP, Harkins TT, Bouffard P, Fitzpatrick C, Chu DS, Thierry-Mieg D, Thierry-Mieg J, Kim JK (2009) 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans. Proc Natl Acad Sci USA 106(44):18674–18679
Hansen D, Schedl T (2012) Stem cell proliferation versus meiotic fate decision in C. elegans. Advances in Experimental Medicine and Biology 757:71–99. (Chap. 4, this volume) Springer, New York
Hill DP, Shakes DC, Ward S, Strome S (1989) A sperm-supplied product essential for initiation of normal embryogenesis in Caenorhabditis elegans is encoded by the paternal-effect embryonic-lethal gene, spe-11. Dev Biol 136(1):154–166
Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, Draper BW, Ketting RF (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129(1):69–82
Howe M, McDonald KL, Albertson DG, Meyer BJ (2001) HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J Cell Biol 153(6):1227–1238
Hsu J, Sun Z, Li X, Reuben M, Tatchell K, Bishop D, Grushcow J, Brame C, Caldwell J, Hunt D, Lin R, Smith M, Allis C (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102(3):279–291
Italiano JE Jr, Roberts TM, Stewart M, Fontana CA (1996) Reconstitution in vitro of the motile apparatus from the amoeboid sperm of Ascaris shows that filament assembly and bundling move membranes. Cell 84(1):105–114
Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J (2007) Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol 308(1):206–221
Jaramillo-Lambert A, Harigaya Y, Vitt J, Villeneuve A, Engebrecht J (2010) Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr Biol 20(23):2078–2089
Jenkins N, Saam JR, Mango SE (2006) CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 313(5791):1298–1301
Johnston WL, Krizus A, Dennis JW (2010) Eggshell chitin and chitin-interacting proteins prevent polyspermy in C. elegans. Curr Biol 20(21):1932–1937
Justine JL (2002) Male and female gametes and fertilization. In: Biology of nematodes. Taylor & Francis, London
Justine JL, Jamieson BGM (2000) Nematode, vol IX, part B. Progress in male gamete ultrastructure and phylogeny. Reproductive biology of invertebrates, vol IX, part B. Wiley, Chichester
Kato M, de Lencastre A, Pincus Z, Slack FJ (2009) Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 10(5):R54
Kelleher JF, Mandell MA, Moulder G, Hill KL, L’Hernault SW, Barstead R, Titus MA (2000) Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Curr Biol 10(23):1489–1496
Kelly WG, Schaner CE, Dernburg AF, Lee M-H, Kim SK, Villeneuve AM, Reinke V (2002) X chromosome silencing in the germline of C. elegans. Development 129(2):479–492
Ketola I, Rahman N, Toppari J, Bielinska M, Porter-Tinge SB, Tapanainen JS, Huhtaniemi IT, Wilson DB, Heikinheimo M (1999) Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 140(3):1470–1480
Ketola I, Pentikainen V, Vaskivuo T, Ilvesmaki V, Herva R, Dunkel L, Tapanainen JS, Toppari J, Heikinheimo M (2000) Expression of transcription factor GATA-4 during human testicular development and disease. J Clin Endocrinol Metab 85(10):3925–3931
Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15(20):2654–2659
Kim DY, Roy R (2006) Cell cycle regulators control centrosome elimination during oogenesis in Caenorhabditis elegans. J Cell Biol 174(6):751–757
Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10(2):126–139
Kim S, Spike CA, Greenstein D (2012) Control of oocyte growth and meiotic maturation in C. elegans. Advances in Experimental Medicine and Biology 757:277–320. (Chap. 10, this volume) Springer, New York
Kimble J, Crittenden SL (2007) Control of germline stem cells, entry into meiosis, and the sperm/oocyte decision in C. elegans. Annu Rev Cell Dev Biol 23:405–433
Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434(7033):583–589
Kimmins S, Kotaja N, Davidson I, Sassone-Corsi P (2004) Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128(1):5–12
Kitagawa R (2009) Key players in chromosome segregation in Caenorhabditis elegans. Front Biosci 14:1529–1557
Klass M, Ammons D, Ward S (1988) Conservation in the 5′ flanking sequences of transcribed members of the Caenorhabditis elegans major sperm protein gene family. J Mol Biol 199(1):15–22
Knight SW, Bass BL (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 293(5538):2269–2271
Kulkarni M, Shakes DC, Guevel K, Smith HE (2012) SPE-44 implements sperm cell fate. PLoS Genet. 8(4):e1002678
Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131(4):839–849
LaMunyon CW, Ward S (1995) Sperm precedence in a hermaphroditic nematode (Caenorhabditis elegans) is due to competitive superiority of male sperm. Experientia 51(8):817–823
LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B Biol Sci 265(1409):1997–2002
LeClaire LL 3rd, Stewart M, Roberts TM (2003) A 48 kDa integral membrane phosphoprotein orchestrates the cytoskeletal dynamics that generate amoeboid cell motility in Ascaris sperm. J Cell Sci 116(Pt 13):2655–2663
Lee DL, Anya AO (1967) The structure and development of the spermatozoon of Aspiculuris tetraptera (Nematoda). J Cell Sci 2(4):537–544
Lewis JD, Abbott DW, Ausio J (2003) A haploid affair: core histone transitions during spermatogenesis. Biochem Cell Biol 81(3):131–140
L’Hernault SW (2006) Spermatogenesis. WormBook:1–14
L’Hernault SW, Arduengo PM (1992) Mutation of a putative sperm membrane protein in Caenorhabditis elegans prevents sperm differentiation but not its associated meiotic divisions. J Cell Biol 119(1):55–68
L’Hernault SW, Shakes DC, Ward S (1988) Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120(2):435–452
Li K, Xu EY, Cecil JK, Turner FR, Megraw TL, Kaufman TC (1998) Drosophila centrosomin protein is required for male meiosis and assembly of the flagellar axoneme. J Cell Biol 141(2):455–467
Lui DY, Colaiácovo MP (2012) Meiotic development in C. elegans. In: Schedl T (ed) Advances in experimental medicine and biology, Chap. 6. Springer, Boston
Maddox PS, Oegema K, Desai A, Cheeseman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res 12(6):641–653
Maeda I, Kohara Y, Yamamoto M, Sugimoto A (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11(3):171–176
Malone CD, Hannon GJ (2009) Small RNAs as guardians of the genome. Cell 136(4):656–668
Marcello MR, Singaravelu G, Singson A (2012) Fertilization. Advances in Experimental Medicine and Biology 757:321–350. (Chap. 11, this volume) Springer, New York
McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205(1):111–128
McNally KL, McNally FJ (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282(1):218–230
Miller D, Brinkworth M, Iles D (2009) Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139(2):287–301
Miller D, Brinkworth M, Iles D (2010) Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139(2):287–301
Minniti AN, Sadler C, Ward S (1996) Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites. Genetics 143(1):213–223
Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7(12):1248–1255
Morgan DE, Crittenden SL, Kimble J (2010) The C. elegans adult male germline: stem cells and sexual dimorphism. Dev Biol 346(2):204–214
Motegi F, Sugimoto A (2006) Sequential functioning of the ECT-2 RhoGEF, RHO-1 and CDC-42 establishes cell polarity in Caenorhabditis elegans embryos. Nat Cell Biol 8(9):978–985
Muhlrad PJ, Ward S (2002) Spermiogenesis initiation in Caenorhabditis elegans involves a casein kinase 1 encoded by the spe-6 gene. Genetics 161(1):143–155
Nance J, Minniti AN, Sadler C, Ward S (1999) spe-12 encodes a sperm cell surface protein that promotes spermiogenesis in Caenorhabditis elegans. Genetics 152(1):209–220
Nance J, Davis EB, Ward S (2000) spe-29 encodes a small predicted membrane protein required for the initiation of sperm activation in Caenorhabditis elegans. Genetics 156(4):1623–1633
Nelson GA, Ward S (1980) Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19(2):457–464
Nelson GA, Lew KK, Ward S (1978) Intersex, a temperature-sensitive mutant of the nematode Caenorhabditis elegans. Dev Biol 66(2):386–409
Nelson GA, Roberts TM, Ward S (1982) Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin. J Cell Biol 92(1):121–131
O’Connell KF, Maxwell KN, White JG (2000) The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. Dev Biol 222(1):55–70
Okamura K, Lai EC (2008) Endogenous small interfering RNAs in animals. Nat Rev Mol Cell Biol 9(9):673–678
Orr-Weaver TL, Parfenov VN, Dudina LM, Kostiuchek DF, Gruzova MN, Parfenov V, Potchukalina G, Dudina L, Kostyuchek D, Gruzova M, Sanyal MK, Taymor ML, Berger MJ (1995) Meiosis in Drosophila: seeing is believing. Proc Natl Acad Sci USA 92 (23):10443–10449
Pavelec DM, Lachowiec J, Duchaine TF, Smith HE, Kennedy S (2009) Requirement for ERI/DICER complex in endogenous RNAi and sperm development in Caenorhabditis elegans. Genetics 183(4):1283–1295
Pelletier L, O’Toole E, Schwager A, Hyman AA, Muller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444(7119):619–623
Peters N, Perez DE, Song MH, Liu Y, Muller-Reichert T, Caron C, Kemphues KJ, O’Connell KF (2010) Control of mitotic and meiotic centriole duplication by the Plk4-related kinase ZYG-1. J Cell Sci 123(Pt 5):795–805
Reinke V (2002) Functional exploration of the C. elegans genome using DNA microarrays. Nat Genet 32(Suppl):541–546
Reinke V, Cutter AD (2009) Germline expression influences operon organization in the Caenorhabditis elegans genome. Genetics 181(4):1219–1228
Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, Kim SK (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6(3):605–616
Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome wide germline enriched and sex biased expression profiles in Caenorhabditis elegans. Development 131(2):311–323
Roberts TM, Pavalko FM, Ward S (1986) Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J Cell Biol 102(5):1787–1796
Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157(2):219–229
Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127(6):1193–1207
Sadler PL, Shakes DC (2000) Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anterior-posterior polarization of the 1-cell embryo. Development 127(2):355–366
Sanyal MK, Taymor ML, Berger MJ (1976) Cytologic features of oocytes in the adult human ovary. Fertil Steril 27(5):501–510
Sassone-Corsi P (2002) Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296(5576):2176–2178
Schumacher JM, Golden A, Donovan PJ (1998) 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 143(6):1635–1646
Schvarzstein M, Wignall SM, Villeneuve AM (2010) Coordinating cohesion, co-orientation, and congression during meiosis: lessons from holocentric chromosomes. Genes Dev 24(3):219–228
Seydoux G, Schedl T (2001) The germline in C. elegans: origins, proliferation, and silencing. Int Rev Cytol 203:139–185
Sha K, Fire A (2005) Imprinting capacity of gamete lineages in Caenorhabditis elegans. Genetics 170(4):1633–1652
Shakes DC, Ward S (1989) Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 134(2):307–316
Shakes DC, Wu JC, Sadler PL, Laprade K, Moore LL, Noritake A, Chu DS (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5(8):e1000611
Shakes DC, Allen AK, Albert KM, Golden A (2011) emb-1 encodes the APC16 subunit of the Caenorhabditis elegans anaphase-promoting complex. Genetics 189(2):549–560
Shepherd AM, Clark SA (1983) The structure and development of the spermatozoon of Aspicularis tetraptera (Nematoda). J Cell Sci 2:537–544
Shim YH, Bonner JJ, Blumenthal T (1995) Activity of a C. elegans GATA transcription factor, ELT-1, expressed in yeast. J Mol Biol 253(5):665–676
Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, Plasterk RH, Fire A (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107(4):465–476
Smith JR, Stanfield GM (2011) TRY-5 is a sperm-activating protease in Caenorhabditis elegans seminal fluid. PLoS Genet 7(11):e1002375
Smith P, Leung-Chiu WM, Montgomery R, Orsborn A, Kuznicki K, Gressman-Coberly E, Mutapcic L, Bennett K (2002) The GLH proteins, Caenorhabditis elegans P granule components, associate with CSN-5 and KGB-1, proteins necessary for fertility, and with ZYX-1, a predicted cytoskeletal protein. Dev Biol 251(2):333–347
Spieth J, Shim YH, Lea K, Conrad R, Blumenthal T (1991) elt-1, an embryonically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol Cell Biol 11(9):4651–4659
Spike C, Meyer N, Racen E, Orsborn A, Kirchner J, Kuznicki K, Yee C, Bennett K, Strome S (2008) Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178(4):1973–1987
Stanfield GM, Villeneuve AM (2006) Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16(3):252–263
Suh N, Blelloch R (2011) Small RNAs in early mammalian development: from gametes to gastrulation. Development 138(9):1653–1661
Turpeenniemi TA (1998) Ultrastructure of spermatozoa in the nematode Halalaimus dimorphus (Nemata: Oxystominidae). J Nematol 30(4):391–403
Varkey JP, Jansma PL, Minniti AN, Ward S (1993) The Caenorhabditis elegans spe-6 gene is required for major sperm protein assembly and shows second site non-complementation with an unlinked deficiency. Genetics 133(1):79–86
Varkey JP, Muhlrad PJ, Minniti AN, Do B, Ward S (1995) The Caenorhabditis elegans spe-26 gene is necessary to form spermatids and encodes a protein similar to the actin-associated proteins kelch and scruin. Genes Dev 9(9):1074–1086
Wallenfang MR, Seydoux G (2000) Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408(6808):89–92
Wang G, Reinke V (2008) A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr Biol 18(12):861–867
Wang X, Zhao Y, Wong K, Ehlers P, Kohara Y, Jones SJ, Marra MA, Holt RA, Moerman DG, Hansen D (2009) Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 10:213
Ward S (1986) The asymmetric localization of gene products during the development of Caenorhabditis elegans spermatozoa. Gametogenesis and the early embryo. A.R. Liss, New York, pp. 55–75
Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73(2):304–321
Ward S, Argon Y, Nelson GA (1981) Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans. J Cell Biol 91(1):26–44
Ward S, Hogan E, Nelson GA (1983) The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol 98(1):70–79
Washington NL, Ward S (2006) FER-1 regulates Ca2 + − mediated membrane fusion during C. elegans spermatogenesis. J Cell Sci 119 (Pt 12):2552–2562
Wignall SM, Villeneuve AM (2009) Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11(7):839–844
Wolf N, Hirsh D, McIntosh JR (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63(2):155–169
Wu TF, Chu DS (2008) Epigenetic processes implemented during spermatogenesis distinguish the paternal pronucleus in the embryo. Reprod Biomed Online 16(1):13–22
Wu JC, Go AC, Samson M, Cintra T, Mirsoian S, Wu TF, Jow MM, Routman EJ, Chu DS (2012) Sperm development and motility are regulated by PP1 phosphatases in Caenorhabditis elegans. Genetics 190(1):143–157
Yi K, Buttery SM, Stewart M, Roberts TM (2007) A Ser/Thr kinase required for membrane-associated assembly of the major sperm protein motility apparatus in the amoeboid sperm of Ascaris. Mol Biol Cell 18(5):1816–1825
Yushin VV, Commans A (2005) ltrastructure of sperm development in the free-living marine nematode Metachromadora itoi (Chromadoria, Desmodorida). Acta Zoologica 86(4):255–265
Zanetti S, Puoti A (2012) Sex determination in the C. elegans germline. Advances in Experimental Medicine and Biology 757:41–69. (Chap. 3, this volume) Springer, New York
Zeng Y, Cullen BR (2003) Sequence requirements for micro RNA processing and function in human cells. RNA 9(1):112–123
Zhu GD, L’Hernault SW (2003) The Caenorhabditis elegans spe-39 gene is required for intracellular membrane reorganization during spermatogenesis. Genetics 165(1):145–157
Zhu GD, Salazar G, Zlatic SA, Fiza B, Doucette MM, Heilman CJ, Levey AI, Faundez V, L’Hernault SW (2009) SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol Biol Cell 20(4):1223–1240
Acknowledgments
We thank David Greenstein and Harold Smith for sharing data prior to publication. We thank Meghann Shorrock for assistance with figures. We also thank Dana Byrd, Margaret Jow, and Kari Price for critical reading of this manuscript. This work was supported grants from the National Science Foundation to D.S.C. (MCB-0747515) and the National Institutes of Health to D.S.C. (R15 HD068996) and D.C.S. (R15 GM096309).
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Chu, D.S., Shakes, D.C. (2013). Spermatogenesis. In: Schedl, T. (eds) Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology, vol 757. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4015-4_7
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