Within the rhabditid phylogeny of nematodes, the great majority of species are gonochoristic, having evolved as obligate male/female species. In contrast, the well-studied nematode model system, Caenorhabditis elegans, is androdioecious, utilizing a hermaphroditic/male reproductive system. We have previously determined that in the arrested oocytes of old-aged C. elegans hermaphrodites with depleted sperm, large cytoplasmic ribonucleoprotein foci form. The formation of these foci is reversible, as they dissociate within 3 h after a male mates with the hermaphrodite, resupplying it with sperm. The functional significance of these oocyte foci is not known and previously has not been clear for a hermaphroditic species in which oocytes of young adults wait only approximately 23 min to be fertilized. One hypothesis is that the foci function to maintain maternal mRNAs in oocytes while fertilization is delayed. In this paper, we examine four gonochoristic rhabditid species: Caenorhabditis remanei, Caenorhabditis sp. CB5161, Caenorhabditis sp. PS1010, and Rhabditella axei DF5006. We demonstrate that in three of these four species, ovulation arrests in unmated females until mating occurs and large cytoplasmic foci develop in arrested oocytes. The oocyte foci contain nuclear pore proteins and, in C. remanei at least, the RNA-binding protein MEX-3 as well as RNA. We speculate that these foci maintain the integrity of ooctyes, possibly maintaining the stability or translational repression of maternal mRNAs in unmated females. We further speculate that their presence in oocytes of old-aged C. elegans hermaphrodites is due to conservation from an ancestral gonochoristic state.
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Aris JP, Blobel G (1989) Yeast nuclear pore envelope proteins cross-react with an antibody against mammalian pore complex proteins. J Cell Biol 108:2059–2067
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
Browning H, Strome S (1996) A sperm-supplied factor required for embryogenesis in C. elegans. Development 122:391–404
Cho S, Jin S-W, Cohen A, Ellis R (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14:1207–1220
Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR (1996) MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87:205–216
Felix M-A (2004) Alternative morphs and plasticity of vulval development in a rhabditid nematode species. Dev Genes Evol 214:55–63
Govindan JA, Cheng H, Harris JE, Greenstein D (2006) Gα0/i and Gαs signaling function in parallel with the MSP/Eph receptor to control meiotic diapause in C. elegans. Curr Biol 16:1257–1268
Haag E (2006) The evolution of nematode sex determination: C. elegans as a reference point for comparative biology. In: WormBook (ed) The C. elegans Research Community, WormBook. http://www.wormbook.org (December 29, 2005)
Hajnal A, Berset T (2002) The C. elegans MAPK phosphatase LIP-1 is required for the G2/M meiotic arrest of developing oocytes. EMBO J 21:4317–4326
Hill RC, de Carvalho CE, Salogiannis J, Schlager B, Pilgrim D, Haag ES (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10:531–538
Kiontke K, Fitch DHA (2005) The phylogenetic relationships of Caenrhabditis and other rhabditids. In: WormBook (ed) The C. elegans Research Community, WormBook, http://www.wormbook.org (August 11, 2005)
Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DHA (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditisim and extensive intron loss. Proc Natl Acad Sci USA 101:9003–9008
McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205:111–128
Miller MA, Nguyen VQ, Lee M-H, Kosinki M, Schedl T, Caprioli RM, Greenstein D (2001) A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291:2144–2147
Pitt JP, Schisa JA, Priess JR (2001) P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Dev Biol 219:315–333
Schisa JA, Pitt JP, Priess JR (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128:1287–1298
We thank Cordell DeMattei for critical reading of the manuscript. MEX-3 antibodies were a gift from J. Priess. We thank Alex Kostin and Emily Petty for assistance with confocal microscopy. J.A.S. is supported by a grant from the NIH, R15 GM078157-01. Stocks were obtained from the C. elegans Genetics Stock Center that is funded by the NIH.
Communicated by D.A. Weisblat
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Jud, M., Razelun, J., Bickel, J. et al. Conservation of large foci formation in arrested oocytes of Caenorhabditis nematodes. Dev Genes Evol 217, 221–226 (2007). https://doi.org/10.1007/s00427-006-0130-3
- Mating system