Plectus - a stepping stone in embryonic cell lineage evolution of nematodes

EvoDevo

Einhard Schierenberg¹  Sandra Vangestel²  Jana Uenk¹  Wouter Houthoofd²  Jens Schulze¹ 

[1] Biocenter, University of Cologne, Zülpicher Strasse 47b, Cologne, 50674, Germany;Department of Biology, Ghent University, Ledeganckstraat 35, Ghent, 9000, Belgium

关键词: C. elegans;    Plectus;    developmental system drift;    evolution;    cell specification;    cell lineage;    embryogenesis;    Nematode;   

Others  :  807568
DOI  :  10.1186/2041-9139-3-13

 received in 2012-04-02, accepted in 2012-05-24,  发布年份 2012

【 摘 要 】

Background

Recent studies have challenged the widespread view that the pattern of embryogenesis found in Caenorhabditis elegans (clade 9) is characteristic of nematodes in general. To understand this still largely unexplored landscape of developmental events, we set out to examine more distantly related nematodes in detail for temporospatial differences in pattern formation and cell specification. Members of the genus Plectus (clade 6) seem to be suitable candidates to show variety, with certain idiosyncratic features during early development and the convenient availability of cultivatable species.

Methods

The study was conducted using 4-D lineage analysis, 3-D modeling of developing embryos and laser-induced ablation of individual blastomeres.

Results

Detailed cell lineage studies of several Plectus species reveal that pattern formation and cell fate assignment differ markedly from C. elegans. Descendants of the first somatic founder cell S1 (AB) - but not the progeny of other founder cells - demonstrate extremely variable spatial arrangements illustrating that here distinct early cell-cell interactions between invariant partners, as found in C. elegans, cannot take place. Different from C. elegans, in Plectus alternative positional variations among early S1 blastomeres resulting in a ‘situs inversus’ pattern, nevertheless give rise to adults with normal left-right asymmetries. In addition, laser ablations of early blastomeres uncover inductions between variable cell partners.

Conclusions

Our results suggest that embryonic cell specification in Plectus is not correlated with cell lineage but with position. With this peculiarity, Plectus appears to occupy an intermediate position between basal nematodes displaying a variable early development and the C. elegans-like invariant pattern. We suggest that indeterminate pattern formation associated with late, position-dependent fate assignment represents a plesiomorphic character among nematodes predominant in certain basal clades but lost in derived clades. Thus, the behavior of S1 cells in Plectus can be considered an evolutionary relict in a transition phase between two different developmental strategies.

【 授权许可】

   
2012 Schulze et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Douzery EJ, Snell EA, Bapteste E, Delsuc F, Philippe H: The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci USA 2004, 101:15386-15391.
• [2]Blaxter M: Nematodes (Nematoda). Edited by Hedges SB, Kumar S. Oxford University Press, Oxford; 2009:247-250.
• [3]Poinar GO: The evolutionary history of nematodes: as revealed in stone, amber and mummies. Brill, Leiden; 2011.
• [4]Poinar G, Kerp H, Hass H: Palaeonema phyticum gen. n., sp n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 2008, 10:9-14.
• [5]Meldal BH, Debenham NJ, De Ley P, De Ley IT, Vanfleteren JR, Vierstraete AR, Bert W, Borgonie G, Moens T, Tyler PA, Austen MC, Blaxter ML, Rogers AD, Lambshead PJ: An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 2007, 42:622-636.
• [6]Lambshead PJD, Boucher G: Marine nematode deep-sea biodiversity - hyperdiverse or hype? J Biogeogr 2003, 30:475-485.
• [7]Malakhov VV: Nematodes. Smithsonian Institution Press, Washington; 1994.
• [8]Poinar GO: The Natural History of Nematodes. Prentice Hall, New Jersey; 1983.
• [9]Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DH: Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 2004, 101:9003-9008.
• [10]Lin KT, Broitman-Maduro G, Hung WW, Cervantes S, Maduro MF: Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans. Dev Biol 2009, 325:296-306.
• [11]Wang X, Sommer RJ: Antagonism of LIN-17/Frizzled and LIN-18/Ryk in nematode vulva induction reveals evolutionary alterations in core developmental pathways. PLoS Biol 2011.
• [12]Boveri T: Die Entwicklung von Ascaris megalocephala mit besonderer Rücksicht auf die Kernverhältnisse [in German]. Gustav Fischer Verlag, Jena; 1899:383-430.
• [13]Müller H: Beitrag zur Embryonalentwicklung von Ascaris megalocephala [in German]. Zoologica 1903, 17:1-30.
• [14]Sulston JE, Schierenberg E, White JG, Thomson JN: The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64-119.
• [15]Schierenberg E: Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications. Dev Genes Evol 2005, 215:103-108.
• [16]Schulze J, Schierenberg E: Cellular pattern formation, establishment of polarity and segregation of colored cytoplasm in embryos of the nematode Romanomermis culicivorax. Dev Biol 2008, 315:426-436.
• [17]Schulze J, Schierenberg E: Evolution of embryonic development in nematodes. EvoDevo 2011, 2:18. BioMed Central Full Text
• [18]von Baer KE: Über die Entwickelungsgeschichte der Thiere: Beobachtung und Reflektion. Bornträger, Königsberg; 1828.
• [19]Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, Holovachov O, Bakker J, Helder J: Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 2006, 23:1792-1800.
• [20]Holovachov O, De Ley P: Order Plectida. Edited by Abebe E, Traunspurger W, Andrássy I. CAB International, Wallingford UK; 2006:611-647.
• [21]De Ley P, Blaxter ML: Systematic Position and Phylogeny. Edited by Lee DL. Taylor and Francis, London; 2002:1-30.
• [22]Lahl V, Halama C, Schierenberg E: Comparative and experimental embryogenesis of Plectidae (Nematoda). Dev Genes Evol 2003, 213:18-27.
• [23]Eisenmann DM: Wnt signaling. 2005. http://www.wormbook.org webcite
• [24]Priess JR: Notch signaling in the C. elegans embryo. 2005.
• [25]Schnabel H, Priess J: Specification of Cell Fates in the Early Embryo. Edited by Riddle DL, Blumenthal T, Meyer BJ, Priess J. Cold Spring Harbor Laboratory Press, New York; 1997:361-382.
• [26]Schierenberg E, Carlson C, Sidio W: Cellular development of a nematode: 3-D computer reconstruction of living embryos. Roux’s Arch Dev Biol 1984, 194:61-68.
• [27]Wood WB: Evidence from reversal of handedness in C. elegans embryos for early cell interactions determining cell fates. Nature 1991, 349:536-538.
• [28]Wood WB, Bergmann D, Florance A: Maternal effect of low temperature on handedness determination in C. elegans embryos. Dev Genet 1996, 19:222-230.
• [29]Houthoofd W, Jacobsen K, Mertens C, Vangestel S, Coomans A, Borgonie G: Embryonic cell lineage of the marine nematode Pellioditis marina. Dev Biol 2003, 258:57-69.
• [30]Houthoofd W, Borgonie G: The embryonic cell lineage of the nematode Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea). Nematology 2007, 9:573-584.
• [31]Deppe U, Schierenberg E, Cole T, Krieg C, Schmitt D, Yoder B, von Ehrenstein G: Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 1978, 75:376-380.
• [32]Schulze J, Schierenberg E: Embryogenesis of Romanomermis culicivorax: an alternative way to construct a nematode. Dev Biol 2009, 334:10-21.
• [33]Hench J, Henriksson J, Luppert M, Burglin TR: Spatio-temporal reference model of Caenorhabditis elegans embryogenesis with cell contact maps. Dev Biol 2009, 333:1-13.
• [34]Schnabel R, Hutter H, Moerman D, Schnabel H: Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev Biol 1997, 184:234-265.
• [35]Shelton CA, Bowerman B: Time-dependent responses to glp-1-mediated inductions in early C. elegans embryos. Development 1996, 122:2043-2050.
• [36]Schierenberg E, Junkersdorf B: The role of eggshell and underlying vitelline membrane for normal pattern formation in the early C. elegans embryo. Dev Genes Evol 1992, 202:10-16.
• [37]Schierenberg E, Wood WB: Control of cell-cycle timing in early embryos of Caenorhabditis elegans. Dev Biol 1985, 107:337-354.
• [38]Bossinger O, Schierenberg E: Early embryonic induction in C. elegans can be inhibited with polysulfated hydrocarbon dyes. Dev Biol 1996, 176:17-21.
• [39]Goldstein B: Induction of gut in Caenorhabditis elegans embryos. Nature 1992, 357:255-257.
• [40]Schierenberg E: Reversal of cellular polarity and early cell-cell interaction in the embryos of Caenorhabditis elegans. Dev Biol 1987, 122:452-463.
• [41]Bossinger O, Schierenberg E: Cell-cell communication in the embryo of Caenorhabditis elegans. Dev Biol 1992, 151:401-409.
• [42]Laufer JS, Bazzicalupo P, Wood WB: Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 1980, 19:569-577.
• [43]Babu P: Biochemical genetics of C. elegans. Mol Gen Genet 1974, 135:39-44.
• [44]Bischoff M, Schnabel R: Global cell sorting is mediated by local cell-cell interactions in the C. elegans embryo. Dev Biol 2006, 294:432-444.
• [45]Schnabel R, Bischoff M, Hintze A, Schulz AK, Hejnol A, Meinhardt H, Hutter H: Global cell sorting in the C. elegans embryo defines a new mechanism for pattern formation. Dev Biol 2006, 294:418-431.
• [46]Lahl V, Sadler B, Schierenberg E: Egg development in parthenogenetic nematodes: variations in meiosis and axis formation. Int J Dev Biol 2006, 50:393-398.
• [47]Wiegner O, Schierenberg E: Specification of gut cell fate differs significantly between the nematodes Acrobeloides nanus and Caenorhabditis elegans. Dev Biol 1998, 204:3-14.
• [48]Wiegner O, Schierenberg E: Regulative development in a nematode embryo: a hierarchy of cell fate transformations. Dev Biol 1999, 215:1-12.
• [49]Lahl V, Schulze J, Schierenberg E: Differences in embryonic pattern formation between Caenorhabditis elegans and its close parthenogenetic relative Diploscapter coronatus. Int J Dev Biol 2009, 53:507-515.
• [50]Zhao Z, Boyle TJ, Bao Z, Murray JI, Mericle B, Waterston RH: Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Dev Biol 2008, 314:93-99.
• [51]Schierenberg E: Embryological variation during nematode development. 2006. http://www.wormbook.org webcite
• [52]Zur Strassen O: Embryonalentwicklung der Ascaris megalocephala [in German]. Arch Entwicklungsmech 1896, 3:27-105.
• [53]Schierenberg E, Lahl V: Embryology and phylogeny of nematodes. Nematol Monogr Persp 2004, 2:667-679.
• [54]Pohl C: Left-right patterning in the C. elegans embryo: Unique mechanisms and common principles. Commun Integr Biol 2011, 4:34-40.
• [55]Wood WB: Left-right asymmetry in animal development. Annu Rev Cell Dev Biol 1997, 13:53-82.
• [56]zur Strassen O: Der Erbgang der Nematoden-Asymmetrie [in German]. , Willhelmshaven; 1951:77-81.
• [57]Felix MA, Sternberg PW, De Ley P: Sinistral nematode population. Nature 1996, 381:122.
• [58]Okumura T, Utsuno H, Kuroda J, Gittenberger E, Asami T, Matsuno K: The development and evolution of left-right asymmetry in invertebrates: lessons from Drosophila and snails. Dev Dyn 2008, 237:3497-3515.
• [59]Yokoyama T, Copeland NG, Jenkins NA, Montgomery CA, Elder FF, Overbeek PA: Reversal of left-right asymmetry: a situs inversus mutation. Science 1993, 260:679-682.
• [60]Voronov DA, Panchin YV: Cell lineage in marine nematode Enoplus brevis. Development 1998, 125:143-150.
• [61]Houthoofd W, Willems M, Jacobsen K, Coomans A, Borgonie G: The embryonic cell lineage of the nematode Rhabditophanes sp. Int J Dev Biol 2008, 52:963-967.
• [62]Wood WB: Handed asymmetry in nematodes. Semin Cell Dev Biol 1998, 9:53-60.
• [63]Arata Y, Lee JY, Goldstein B, Sawa H: Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo. Development 2010, 137:3337-3345.
• [64]Edgar LG, Goldstein B: Culture and manipulation of embryonic cells. Methods Cell Biol 2012, 107:151-175.
• [65]Boveri T: Die Potenzen der Ascaris Blastomeren bei abgeänderter Furchung. Zugleich ein Beitrag zur Frage qualitativ ungleicher Chromosomenverteilung [in German]. Gustav Fischer Verlag, Jena; 1910:133-214.
• [66]Maduro MF: Cell fate specification in the C. elegans embryo. Dev Dyn 2010, 239:1315-1329.
• [67]Hutter H, Schnabel R: Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development 1995, 121:3417-3424.
• [68]Schierenberg E: Three sons of fortune: early embryogenesis, evolution and ecology of nematodes. Bioessays 2001, 23:841-847.
• [69]Stent GS: The role of cell lineage in development. Philos Trans R Soc Lond B Biol Sci 1985, 312:3-19.
• [70]Felix MA, Barkoulas M: Robustness and flexibility in nematode vulva development. Trends Genet 2012, 28:185-195.
• [71]Haag ES: The evolution of nematode sex determination: C. elegans as a reference point for comparative biology. 2005. http://www.wormbook.org webcite
• [72]True JR, Haag ES: Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 2001, 3:109-119.
• [73]Voronov DA: The embryonic development of Pontonema vulgare (Enoplida: Oncholaimidae) with a discussion of nematode phylogeny. Russ J Nematol 1999, 7:105-114.
• [74]Kumar S, Schiffer PH, Blaxter M: 959 Nematode Genomes: a semantic wiki for coordinating sequencing projects. Nucleic Acids Res 2012, 40:D1295-D1300.
• [75]Sommer RJ, Streit A: Comparative genetics and genomics of nematodes: genome structure, development, and lifestyle. Annu Rev Genet 2011, 45:1-20.