The genome of Romanomermis culicivorax: Revealing fundamental changes in the core developmental genetic toolkit in Nematoda

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Schiffer, Philipp H ^a   Kroiher, Michael ^a   Kraus, Christopher ^a   Koutsovoulos, Georgios D ^b   Kumar, Sujai ^b   R Camps, Julia I ^a   Nsah, Ndifon A ^a   Stappert, Dominik ^a   Morris, Krystalynne ^c   Heger, Peter ^a   Altmüller, Janine ^d   Frommolt, Peter ^d   Nürnberg, Peter ^d   Thomas, W K ^c   Blaxter, Mark L ^b   Schierenberg, Einhard ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF NEW HAMPSHIRE   (United States)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Caenorhabditis; Development; Evolution; Genome; Mermithida; Nematode; Romanomermis

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; DEVELOPMENTAL GENE; ECDYSOZOA; EMBRYO DEVELOPMENT; GENOME; IN SITU HYBRIDIZATION; NONHUMAN; ROMANOMERMIS CULICIVORAX; TRIBOLIUM CASTANEUM; TRICHINELLA SPIRALIS;

ARTHROPODA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; CHROMADOREA; ECDYSOZOA; ENOPLEA; MERMITHIDA; NEMATODA; ROMANOMERMIS; ROMANOMERMIS CULICIVORAX; TRIBOLIUM CASTANEUM; TRICHINELLA SPIRALIS; VERTEBRATA;

ANIMALS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; ENOPLIDA; GENE LIBRARY; GENOME, HELMINTH; TRANSCRIPTOME; TRIBOLIUM; TRICHINELLA SPIRALIS;

EID: 84891029458     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-923     Document Type: Article

References (128)

1. Maduro MF. Cell fate specification in the C. elegans embryo. Dev Dyn 2010, 239:1315-1329.
2. Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64-119. 10.1016/0012-1606(83)90201-4, 6684600.
3. Blaxter M, de Ley P, Garey J, Liu L, Scheldeman P, Vierstraete A, Vanfleteren J, Mackey L, Dorris M, Frisse L. A molecular evolutionary framework for the phylum Nematoda. Nature 1998, 392(6671):71-75. 10.1038/32160, 9510248.
4. Meldal B, Debenham N, de Ley P, de Ley I, Vanfleteren J, Vierstraete A, Bert W, Borgonie G, Moens T, Tyler P, Austen M, Blaxter M, Rodgers A, Lambshead P. An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 2007, 42(3):622-636. 10.1016/j.ympev.2006.08.025, 17084644.
5. Boveri T. Die Entwicklung von Ascaris megalocephala mit besonderer Ruecksicht auf die Kernverhaeltnisse 1899, Fischer: Festschrift fuer Carl von Kupffer; Jena.
6. Müller H. Beitrag zur Embryonalentwicklung von Ascaris megalocephala. Zoologica 1903, 41:60.
7. Vangestel S, Houthoofd W, Bert W, Borgonie G. The early embryonic development of the satellite organism Pristionchus pacificus: differences and similarities with Caenorhabditis elegans. Nematology 2008, 10:301-312.
8. Skiba F, Schierenberg E. Cell lineages, developmental timing, and spatial pattern formation in embryos of free-living soil nematodes. Dev Biol 1992, 151(2):597-610. 10.1016/0012-1606(92)90197-O, 1601187.
9. 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(4):507-515. 10.1387/ijdb.082718vl, 19378252.
10. Brauchle M, Kiontke K, Macmenamin P, Fitch DHA, Piano F. Evolution of early embryogenesis in rhabditid nematodes. Dev Biol 2009, 335:253-262. 10.1016/j.ydbio.2009.07.033, 2763944, 19643102.
11. 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. 10.1006/dbio.1998.9054, 9851839.
12. Wiegner O, Schierenberg E. Regulative development in a nematode embryo: a hierarchy of cell fate transformations. Dev Biol 1999, 215:1-12. 10.1006/dbio.1999.9423, 10525346.
13. Voronov DA, Panchin YV. Cell lineage in marine nematode Enoplus brevis. Dev 1998, 125:143-150.
14. Schulze J, Schierenberg E. Evolution of embryonic development in nematodes. EvoDevo 2011, 2:18. 10.1186/2041-9139-2-18, 3195109, 21929824.
15. Schulze J, Houthoofd W, Uenk J, Vangestel S, Schierenberg E. Plectus - a stepping stone in embryonic cell lineage evolution of nematodes. EvoDevo 2012, 3:13. 10.1186/2041-9139-3-13, 3464786, 22748136.
16. True JR, Haag ES. Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 2001, 3(2):109-119. 10.1046/j.1525-142x.2001.003002109.x, 11341673.
17. C elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282(5396):2012-2018. C elegans Sequencing Consortium.
18. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D'eustachio P, Fitch DHA, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, et al. The genome sequence of, Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 2003, 1(2):E45. 261899, 14624247.
19. Mortazavi A, Schwarz EM, Williams B, Schaeffer L, Antoshechkin I, Wold BJ, Sternberg PW. Scaffolding a Caenorhabditis nematode genome with RNA-seq. Genome Res 2010, 20(12):1740-1747. 10.1101/gr.111021.110, 2990000, 20980554.
20. Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, Dinkelacker I, Fulton L, Fulton R, Godfrey J, Minx P, Mitreva M, Roeseler W, Tian H, Witte H, Yang SP, Wilson RK, Sommer RJ. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genet 2008, 40(10):1193-1198. 10.1038/ng.227, 3816844, 18806794.
21. Jex AR, Liu S, Li B, Young ND, Hall RS, Li Y, Yang L, Zeng N, Xu X, Xiong Z, Chen F, Wu X, Zhang G, Fang X, Kang Y, Anderson GA, Harris TW, Campbell BE, Vlaminck J, Wang T, Cantacessi C, Schwarz EM, Ranganathan S, Geldhof P, Nejsum P, Sternberg PW, Yang H, Wang J, Wang J, Gasser RB. Ascaris suum draft genome. Nature 2011, 479(7374):529-533. 10.1038/nature10553, 22031327.
22. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, Angiuoli SV, Creasy T, Amedeo P, Haas B, El-Sayed NM, Wortman JR, Feldblyum T, Tallon L, Schatz M, Shumway M, Koo H, Salzberg SL, Schobel S, Pertea M, Pop M, White O, Barton GJ, Carlow CKS, Crawford MJ, Daub J, et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317(5845):1756-1760. 10.1126/science.1145406, 2613796, 17885136.
23. Godel C, Kumar S, Koutsovoulos G, Ludin P, Nilsson D, Comandatore F, Wrobel N, Thompson M, Schmid CD, Goto S, Bringaud F, Wolstenholme A, Bandi C, Epe C, Kaminsky R, Blaxter M, Mäser P. The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB J 2012, 26(11):4650-4661. 10.1096/fj.12-205096, 3475251, 22889830.
24. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, Mcveigh P, Pesole G, Poulain J, Robinson-Rechavi M, et al. Genome sequence of the metazoan plant-parasitic nematode, Meloidogyne incognita. Nature Biotechnol 2008, 26(8):909-915.
25. Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, Mcveigh P, Takanashi T, Tsai IJ, Assefa SA, Cock PJA, Otto TD, Hunt M, Reid AJ, Sanchez-Flores A, Tsuchihara K, Yokoi T, Larsson MC, Miwa J, Maule AG, Sahashi N, Jones JT, Berriman M. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 2011, 7(9):e1002219. 10.1371/journal.ppat.1002219, 3164644, 21909270.
26. Srinivasan J, Dillman AR, Macchietto MG, Heikkinen L, Lakso M, Fracchia KM, Antoshechkin I, Mortazavi A, Wong G, Sternberg PW. The draft genome and transcriptome of Panagrellus redivivus are shaped by the harsh demands of a free-living lifestyle. Genetics 2013, 193(4):1279-1295. 10.1534/genetics.112.148809, 3606103, 23410827.
27. Mitreva M, Jasmer DP, Zarlenga DS, Wang Z, Abubucker S, Martin J, Taylor CM, Yin Y, Fulton LA, Minx P, Yang SP, Warren WC, Fulton RS, Bhonagiri V, Zhang X, Hallsworth-Pepin K, Clifton SW, Mccarter JP, Appleton J, Mardis ER, Wilson RK. The draft genome of the parasitic nematode Trichinella spiralis. Nature Genet 2011, 43(3):228-235. 10.1038/ng.769, 3057868, 21336279.
28. Hope IA. Embryology, Developmental Biology and the Genome. The Biology of Nematodes 2002, 121-145. New York: Tayler & Francis, Lee DL.
29. Kumar S, Schiffer PH, Blaxter M. 959 Nematode Genomes: a semantic wiki for coordinating sequencing projects. Nucl Acids Res 2012, 40(D1):D1295-D1300. 10.1093/nar/gkr826, 3245058, 22058131.
30. Kumar S, Koutsovoulos G, Kaur G, Blaxter M. Toward 959 nematode genomes. Worm 2012, 1:0-8.
31. Petersen JJ. Nematodes as biological control agents: Part I. Mermithidae. Advances in Parasitology 1985, 307-346. London: Academic Press, Baker JR, Muller R.
32. Petersen JJ, Chapman HC, Willis OR, Fukuda T. Release of Romanomermis culicivorax for the control of Anopheles albimanus in El Salvador II. Application of the nematode. Ame J Trop Med Hyg 1978, 27(6):1268-1273.
33. 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(2):426-436. 10.1016/j.ydbio.2007.12.043, 18275948.
34. Schulze J, Schierenberg E. Embryogenesis of Romanomermis culicivorax: an alternative way to construct a nematode. Dev Biol 2009, 334:10-21. 10.1016/j.ydbio.2009.06.009, 19523940.
35. Kent W. BLAT-the BLAST-like alignment tool. Genome Res 2002, 12(4):656. 187518, 11932250.
36. Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 2007, 23(9):1061-1067. 10.1093/bioinformatics/btm071, 17332020.
37. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, Holt C, Sánchez Alvarado A, Yandell M. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 2008, 18:188-196. 2134774, 18025269.
38. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22(13):1658-1659. 10.1093/bioinformatics/btl158, 16731699.
39. Stanke M, Waack S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 2003, 19(2):ii215-ii225.
40. Wang J, Mitreva M, Berriman M, Thorne A, Magrini V, Koutsovoulos G, Kumar S, Blaxter ML, Davis RE. Silencing of germline-expressed genes by DNA elimination in somatic cells. Dev Cell 2012, 23(5):1072-1080. 10.1016/j.devcel.2012.09.020, 3620533, 23123092.
41. Nawrocki EP, Kolbe DL, Eddy SR. Infernal 1.0: inference of RNA alignments. Bioinformatics 2009, 25(10):1335-1337. 10.1093/bioinformatics/btp157, 2732312, 19307242.
42. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 1997, 25(5):0955-0964.
43. Kumar S. Data for PhD thesis on next generation nematode genomes. 2012, http://dx.doi.org/10.6084/m9.figshare.96089.
44. Richards S, The T castaneum Genome Consortium The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452(7190):949-955. 10.1038/nature06784, 18362917, The T castaneum Genome Consortium.
45. Schröder R, Beermann A, Wittkopp N, Lutz R. From development to biodiversity-Tribolium castaneum, an insect model organism for short germband development. Dev Genes Evol 2008, 218(3-4):119-126. 10.1007/s00427-008-0214-3, 18392874.
46. Chen F, Mackey AJ, Vermunt JK, Roos DS. Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2007, 2(4):e383. 10.1371/journal.pone.0000383, 1849888, 17440619.
47. Altschul S, Madden T, Schäffer A. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids .. 1997, [http://nar.oxfordjournals.org/content/25/17/3389.short].
48. Jensen RA. Orthologs and paralogs - we need to get it right. Genome Biol 2001, 2(8):Interactions1002.1-1002.3.
49. Koonin E. Orthologs, paralogs, and evolutionary genomics. Ann Rev Genet 2005, 39:309-338. 10.1146/annurev.genet.39.073003.114725, 16285863.
50. Moreno-Hagelsieb G, Latimer K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 2008, 24(3):319-324. 10.1093/bioinformatics/btm585, 18042555.
51. Shaye DS, Greenwald I. OrthoList: A compendium of C. elegans Genes with human Orthologs. PLoS ONE 2011, 6(5):e20085. 10.1371/journal.pone.0020085, 3102077, 21647448.
52. Tautz D, Domazet-Lošo T. The evolutionary origin of orphan genes. Nat Rev Genet 2011, 12(10):692-702. 10.1038/nrg3053, 21878963.
53. Altschul SF, Gish W, Miller W, Myers EW. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
54. Keeling PJ, Corradi N, Morrison HG, Haag KL, Ebert D, Weiss LM, Akiyoshi DE, Tzipori S. The reduced genome of the parasitic microsporidian enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol Evol 2010, 2(0):304-309. 10.1093/gbe/evq022, 2942035, 20624735.
55. Bird A. DNA methylation patterns and epigenetic memory. Genes & Dev 2002, 16:6-21. 10.1101/gad.947102, 11782440.
56. Gao F, Liu X, Wu XP, Wang XL, Gong D, Lu H, Xia Y, Song Y, Wang J, Du J, Liu S, Han X, Tang Y, Yang H, Jin Q, Zhang X, Liu M. Differential DNA methylation in discrete developmental stages of the parasitic nematode Trichinella spiralis. Genome Biol 2012, 13(10):R100. 10.1186/gb-2012-13-10-r100, 23075480.
57. Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, Delrow J, Boyle T, Kwong S, Bryson TD, Jacobsen SE, Henikoff S. Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 2005, 6(11):R90. 10.1186/gb-2005-6-11-r90, 1297646, 16277745.
58. Martienssen RA, Colot V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 2001, 293(5532):1070-1074. 10.1126/science.293.5532.1070, 11498574.
59. Eisenmann DM. Wnt signaling. WormBook 2005, [http://www.wormbook.org/chapters/www_wntsignaling/wntsignaling.html].
60. Graham LD, Kotze AC, Fernley RT, Hill RJ. Molecular & biochemical parasitology. Mol Biochem Parasitol 2010, 171(2):104-107. [http://dx.doi.org/10.1016/j.molbiopara.2010.03.003], 10.1016/j.molbiopara.2010.03.003, 20226216.
61. Levin M, Hashimshony T, Wagner F, Yanai I. Developmental milestones punctuate gene expression in the caenorhabditis embryo. Dev Cell 2012, 22(5):1101-1108. 10.1016/j.devcel.2012.04.004, 22560298.
62. Phelan P. Innexins: members of an evolutionarily conserved family of gap-junction proteins. Biochimica et Biophysica Acta (BBA) - Biomembranes 2005, 1711(2):225-245.
63. Jones AK, Sattelle DB. Functional genomics of the nicotinic acetylcholine receptor gene family of the nematode, Caenorhabditis elegans. BioEssays 2003, 26:39-49.
64. Antebi A. Nuclear hormone receptors in C. elegans. Wormbook 2006, WormBook, The C. elegans Research Community, http://www.wormbook.org.
65. Altun ZF, Chen B, Wang ZW, Hall DH. High resolution map of Caenorhabditis elegansgap junction proteins. Dev Dyn 2009, 238(8):1936-1950. 10.1002/dvdy.22025, 2732576, 19621339.
66. Haag E. The evolution of nematode sex determination: C. elegans as a reference point for comparative biology. WormBook 2005, WormBook, The C. elegans Research Community, http://www.wormbook.org.
67. Tingley GA, Anderson RM. Environmental sex determination and density-dependent population regulation in the entomogenous nematode Romanomermis culicivorax. Parasitol 1986, 92:431-449.
68. Powell JR, Jow MM, Meyer BJ. The T-box transcription factor SEA-1 is an autosomal element of the X:A signal that determines C. elegans sex. Dev Cell 2005, 9(3):339-349. 10.1016/j.devcel.2005.06.009, 2649673, 16139225.
69. Chu DS, Dawes HE, Lieb JD, Chan RC, Kuo AF, Meyer BJ. A molecular link between gene-specific and chromosome-wide transcriptional repression. Genes & Dev 2002, 16(7):796-805. 10.1101/gad.972702, 186330, 11937488.
70. Meyer B. X-Chromosome dosage compensation. WormBook 2005, WormBook, The C. elegans Research Community, http://www.wormbook.org.
71. Zarkower D. Somatic sex determination. WormBook 2006, WormBook, The C. elegans Research Community, http://www.wormbook.org.
72. Kuwabara PE, Okkema PG, Kimble J. tra-2 encodes a membrane protein and may mediate cell communication in the Caenorhabditis elegans sex determination pathway. Mol Biol Cell 1992, 3(4):461-473. 10.1091/mbc.3.4.461, 275596, 1498366.
73. Goodwin EB, Ellis RE. Turning clustering loops: sex determination in Caenorhabditis elegans. Curr Biol 2002, 12(3):R111-R120. 10.1016/S0960-9822(02)00675-9, 11839294.
74. Baldi C, Cho S, Ellis RE. Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 2009, 326(5955):1002-1005. 10.1126/science.1176013, 19965511.
75. Goldstein B, Macara IG. The PAR proteins: fundamental players in animal cell polarization. Dev Cell 2007, 13(5):609-622. 10.1016/j.devcel.2007.10.007, 2964935, 17981131.
76. Bowerman B. Embryonic polarity: Protein stability in asymmetric cell division. Curr Biol 2000, 10(17):R637-R641. 10.1016/S0960-9822(00)00660-6, 10996090.
77. Severson AF, Bowerman B J Cell Biol 2003, 161:21-26. 10.1083/jcb.200210171, 2172887, 12695495, Bowerman B.
78. Gönczy P, Rose LS. Asymmetric cell division and axis formation in the embryo. WormBook 2005-2005. WormBook, The C. elegans Research Community, http://www.wormbook.org.
79. Cheng NN, Kirby CM, Kemphues KJ. Control of cleavage spindle orientation in Caenorhabditis elegans: the role of the genes par-2 and par-3. Genetics 1995, 139(2):549-559. 1206366, 7713417.
80. Wu JC, Rose LS. PAR-3 and PAR-1 inhibit LET-99 localization to generate a cortical band important for spindle positioning in Caenorhabditis elegans embryos. Mol Biol Cell 2007, 18(11):4470-4482. 10.1091/mbc.E07-02-0105, 2043561, 17761536.
81. Doerflinger H, Vogt N, Torres IL, Mirouse V, Koch I, Nusslein-Volhard C, St Johnston D. Bazooka is required for polarisation of the Drosophila anterior-posterior axis. Development 2010, 137(10):1765-1773. 10.1242/dev.045807, 2860254, 20430751.
82. Goldstein B, Frisse L, Thomas W. Embryonic axis specification in nematodes: evolution of the first step in development. Curr Biol 1998, 8(3):157-160. 10.1016/S0960-9822(98)70062-4, 9443914.
83. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR. MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 1996, 87(2):205-216. 10.1016/S0092-8674(00)81339-2, 8861905.
84. Huang N, Mootz D, Walhout A, Vidal M, Hunter CP. MEX-3 interacting proteins link cell polarity to asymmetric gene expression in Caenorhabditis elegans. Development 2002, 129(3):747-759.
85. Evans TC, Hunter CP. Translational control of maternal RNAs. WormBook 2005-2005. WormBook, The C. elegans Research Community, http://www.wormbook.org.
86. Gomes JE, Encalada SE, Swan KA, Shelton CA, Carter JC, Bowerman B. The maternal gene spn-4 encodes a predicted RRM protein required for mitotic spindle orientation and cell fate patterning in early C. elegans embryos. Dev 2001, 128(21):4301-4314.
87. Labbé JC, Goldstein B. Embryonic development: A New SPN on cell fate specification. Curr Biol 2002, 12(11):R396-R398. 10.1016/S0960-9822(02)00884-9, 12062074.
88. Simske JS, Hardin J. Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. BioEssays 2001, 23:12-23. 10.1002/1521-1878(200101)23:1<12::AID-BIES1003>3.3.CO;2-I, 11135305.
89. Gilleard JS, McGhee JD. Activation of hypodermal differentiation in the Caenorhabditis elegans embryo by GATA transcription factors ELT-1 and ELT-3. Mol Cell Biol 2001, 21(7):2533-2544. 10.1128/MCB.21.7.2533-2544.2001, 86885, 11259601.
90. Sommer R. As good as they get: cells in nematode vulva development and evolution. Curr Opin Cell Biol 2001, 13(6):715-720. 10.1016/S0955-0674(00)00275-1, 11698187.
91. Kiontke K, Barriere A, Kolotuev I, Podbilewicz B, Sommer R, Fitch DHA, Félix MA. Trends, stasis, and drift in the evolution of nematode vulva development. Curr Biol : CB 2007, 17(22):1925-1937.
92. Sternberg PW. Vulval development. WormBook 2005, WormBook, The C. elegans Research Community, http://www.wormbook.org.
93. Salser SJ, Loer CM, Kenyon C. Multiple HOM-C gene interactions specify cell fates in the nematode central nervous system. Genes & Dev 1993, 7(9):1714-1724. 10.1101/gad.7.9.1714, 8103754.
94. Eisenmann DM, Kim SK. Protruding vulva mutants identify novel loci and Wnt signaling factors that function during Caenorhabditis elegans vulva development. Genetics 2000, 156(3):1097-1116. 1461321, 11063687.
95. Shemer G, Podbilewicz B. LIN-39/Hox triggers cell division and represses EFF-1/fusogen-dependent vulval cell fusion. Genes & Dev 2002, 16(24):3136-3141. 10.1101/gad.251202, 187502, 12502736.
96. Tian H, Schlager B, Xiao H, Sommer RJ. Wnt signaling induces vulva development in the nematode Pristionchus pacificus. Curr Biol 2008, 18(2):142-146. 10.1016/j.cub.2007.12.048, 18207741.
97. Streit A, Kohler R, Marty T, Belfiore M, Takacs-Vellai K, Vigano MA, Schnabel R, Affolter M, Müller F. Conserved Regulation of the Caenorhabditis elegans labial/Hox1 Gene ceh-13. Dev Biol 2002, 242(2):96-108. 10.1006/dbio.2001.0544, 11820809.
98. Aboobaker AA, Blaxter ML. Hox Gene Loss during dynamic evolution of the nematode cluster. Curr Biol 2003, 13:37-40. 10.1016/S0960-9822(02)01399-4, 12526742.
99. Chisholm A. Control of cell fate in the tail region of C. elegans by the gene egl-5. Deve 1991, 111(4):921-932.
100. Aboobaker A, Blaxter M. Hox gene evolution in nematodes: novelty conserved. Current Opinion in Genet & Dev 2003, 13:593-598.
101. Lemons D, McGinnis W. Genomic evolution of Hox gene clusters. Science 2006, 313(5795):1918-1922. 10.1126/science.1132040, 17008523.
102. Chamberlin HM, Thomas JH. The bromodomain protein LIN-49 and trithorax-related protein LIN-59 affect development and gene expression in Caenorhabditis elegans. Development 2000, 127(4):713-723.
103. Aspöck G, Kagoshima H, Niklaus G, Bürglin TR. Caenorhabditis elegans Has scores of hedgehog related genes: sequence and expression analysis. Genome Res 1999, 9:909-923. http://genome.cshlp.org, 10.1101/gr.9.10.909, 10523520.
104. Domazet-Lošo T, Tautz D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 2010, 468(7325):815-818. 10.1038/nature09632, 21150997.
105. Richardson MK. A phylotypic stage for all animals?. Dev Cell 2012, 22(5):903-904. 10.1016/j.devcel.2012.05.001, 22595663.
106. Kalinka AT, Tomancak P. The evolution of early animal embryos: conservation or divergence?. Trends In Ecology & Evolution 2012, 27(7):385-393. 10.1016/j.tree.2012.03.007, 22520868.
107. De Ley P. A quick tour of nematode diversity and the backbone of nematode phylogeny. WormBook 2006, WormBook, The C. elegans Research Community, http://www.wormbook.org.
108. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal 2011, 17(1).
109. CLCbio White Paper on de Novo Assembly in CLC Assembly Cell 2010, CLC Bio: Whitepaper, CLCbio.
110. Kumar S, Blaxter ML. Simultaneous genome sequencing of symbionts and their hosts. Symbiosis 2012, 55(3):119-126.
111. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27(4):578-579. 10.1093/bioinformatics/btq683, 21149342.
112. Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0. 1996-2010. http://www.repeatmasker.org.
113. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Res 2005, 110(1-4):462-467.
114. Volfovsky N, Haas BJ, Salzberg SL. A clustering method for repeat analysis in DNA sequences. Genome Biol 2001, 2(8):research0027.1-research0027.11.
115. Bao Z, Eddy SR. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 2002, 12(8):1269-1276. 10.1101/gr.88502, 186642, 12176934.
116. Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics 2005, 21(Suppl 1):i351-i358. 10.1093/bioinformatics/bti1018, 15961478.
117. Parkinson J, Mitreva M, Whitton C, Thomson M. A transcriptomic analysis of the phylum Nematoda. Nature Genet 2004, 36:1259-1267. 10.1038/ng1472, 15543149.
118. Gremme G, Brendel V, Sparks ME, Kurtz S. Engineering a software tool for gene structure prediction in higher organisms. Information and Software Technol 2005, 47(15):965-978.
119. Supek F, Vlahovicek K. INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics 2004, 20(14):2329-2330. 10.1093/bioinformatics/bth238, 15059815.
120. Cutter AD, Wasmuth JD, Blaxter ML. The evolution of biased codon and amino acid usage in nematode genomes. Mol Biol Evol 2006, 23(12):2303-2315. 10.1093/molbev/msl097, 16936139.
121. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676. 10.1093/bioinformatics/bti610, 16081474.
122. The Gene Ontology Consortium Gene Ontology: tool for the unification of biology. Nature Genetics 2000, 25:25-29. 10.1038/75556, 3037419, 10802651, The Gene Ontology Consortium.
123. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. InterProScan: protein domains identifier. Nucl Acids Res 2005, 33(Web Server):W116-W120. 10.1093/nar/gki442, 1160203, 15980438.
124. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy S, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucl Acids Res 2004, 33(Database issue):D121-D124.
125. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research 2003, 13(9):2178-2189. 10.1101/gr.1224503, 403725, 12952885.
126. van Dongen S. A Cluster algorithm for graphs. Report - Information Syst 2000, 10:1-40.
127. van Dongen S. Graph Clustering by Flow Simulation. PhD thesis, University of Utrecht 2000. http://www.wormbook.org.
128. Seydoux G, Fire A. Whole-mount in situ hybridization for the detection of RNA in Caenorhabditis elegans embryos. Methods in cell biology 1995, 48:323-337.