Onychophoran Hox genes and the evolution of arthropod Hox gene expression

Frontiers in Zoology

Volumn 11, Issue 1, 2014, Pages

  Janssen, Ralf ^a   Eriksson, Bo J ^b   Tait, Noel N ^c   Budd, Graham E ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF VIENNA   (Austria)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

Body patterning; Development; Phylogeny; Segmentation; Tagmosis

Indexed keywords

EID: 84897570605     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-11-22     Document Type: Article

References (69)

1. Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ, Telford MJ, Philippe H, Rebecchi L, Peterson KJ, Pisani D. MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc Natl Acad Sci USA 2011, 108:15920-15924. 10.1073/pnas.1105499108, 3179045, 21896763.
2. Dunlop JA, Arango CP. Pycnogonid affinities: a review. J Zool Syst Evol Res 2005, 43:8-21.
3. Giribet G, Edgecombe GD. Reevaluating the arthropod tree of life. Annu Rev Entomol 2012, 57:167-186. 10.1146/annurev-ento-120710-100659, 21910637.
4. Dohle W. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name " Tetraconata" for the monophyletic unit Crustacea + Hexapoda. Ann Soc Entomol Fr 2001, 37:85-103.
5. Whittington HB. The lobopod animal Aysheaia pedunculata Walcott, Middle Cambrian, Burgess Shale, British Columbia. Philos Trans R Soc Lond B Biol Sci 1978, 284:165-197.
6. Thompson I, Jones DS. A possible onychophoran from the Middle Pennsylvanian Mazon Creek Beds of northern Illinois. J Paleontol 1980, 54:588-596.
7. Dzik J, Krumbiegel G. The oldest 'onychophoran' Xenusion: a link connecting phyla?. Lethaia 1989, 22:169-181.
8. Ou Q, Liu J, Shu D, Han J, Zhang Z, Wan X, Lei Q. A rare onychophoran-like lobopodian from the Lower Cambrian Chengjiang Lagerstätte, Southwest China, and its phylogenetic implications. J Paleontol 2011, 85:587-594.
9. Budd GE. Tardigrades as 'stem-group arthropods': the evidence from the Cambrian fauna. Zool Anz 2001, 240:265-279.
10. Janssen R, Eriksson BJ, Budd GE, Akam M, Prpic NM. Gene expression patterns in an onychophoran reveal that regionalization predates limb segmentation in pan-arthropods. Evol Dev 2010, 12:363-372. 10.1111/j.1525-142X.2010.00423.x, 20618432.
11. Daley AC, Budd GE, Caron JB, Edgecombe GD, Collins D. The Burgess Shale anomalocaridid Hurdia and its significance for early euarthropod evolution. Science 2009, 323:1597-1600. 10.1126/science.1169514, 19299617.
12. Daley AC, Budd GE. New anomalocaridid appendages from the Burgess Shale, Canada. Palaeontology 2010, 53:721-738.
13. Klingler M, Tautz D. Formation of embryonic axes and blastoderm pattern in Drosophila. Development, Genetics, Epigenetics and Environmental Regulation 1999, 311-330. Berlin: Springer, Russo VEA, Cove DJ, Edgar LG, Jaenisch R, Salamini F.
14. Pankratz MJ, Jäckle H. Blastoderm segmentation. The development of Drosophila melanogaster 1993, 467-516. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, Bate M, Martinez Arias A.
15. Damen WGM. Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 2007, 236:1379-1391. 10.1002/dvdy.21157, 17440988.
16. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570. 10.1038/276565a0, 103000.
17. Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci USA 1982, 79:7380-7384. 10.1073/pnas.79.23.7380, 347343, 6961417.
18. Lawrence PA, Morata G. Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell 1994, 78:181-189. 10.1016/0092-8674(94)90289-5, 7913879.
19. Akam M. Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. Int J Dev Biol 1998, 42:445-451.
20. Pultz MA, Diederich RJ, Cribbs DL, Kaufman TC. The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. Genes Dev 1988, 2:901-920. 10.1101/gad.2.7.901, 2850265.
21. Hughes CL, Kaufman TC. RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 2000, 127:3683-3694.
22. Pavlopoulos A, Kontarakis Z, Liubicich DM, Serano JM, Akam M, Patel NH, Averof M. Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean. Proc Natl Acad Sci USA 2009, 106:13897-13902. 10.1073/pnas.0902804106, 2728992, 19666530.
23. Khadjeh S, Turetzek N, Pechmann M, Schwager EE, Wimmer EA, Damen WG, Prpic NM. Divergent role of the Hox gene Antennapedia in spiders is responsible for the convergent evolution of abdominal limb repression. Proc Natl Acad Sci USA 2012, 109:4921-4926. 10.1073/pnas.1116421109, 3323954, 22421434.
24. Akam M. Arthropods: developmental diversity within a (super) phylum. Proc Natl Acad Sci USA 2000, 97:4438-4441. 10.1073/pnas.97.9.4438, 34317, 10781039.
25. Damen WGM, Hausdorf M, Seyfarth E-A, Tautz D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 1998, 95:10665-10670. 10.1073/pnas.95.18.10665, 27952, 9724761.
26. Cook CE, Smith LM, Telford MJ, Bastianello A, Akam M. Hox genes and the phylogeny of the arthropods. Curr Biol 2001, 11:759-763. 10.1016/S0960-9822(01)00222-6, 11378385.
27. Hughes CL, Kaufman TC. Hox genes and the evolution of the arthropod body plan. Evol Dev 2002, 4:459-499. 10.1046/j.1525-142X.2002.02034.x, 12492146.
28. Rushlow C, Doyle H, Hoey T, Levine M. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev 1987, 1:1268-1279. 10.1101/gad.1.10.1268, 2892759.
29. Stauber M, Jackle H, Schmidt-Ott U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA 1999, 96:3786-3789. 10.1073/pnas.96.7.3786, 22372, 10097115.
30. Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Roux's Arch Dev Biol 1984, 193:283-295.
31. Stauber M, Prell A, Schmidt-Ott U. A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 2002, 99:274-279. 10.1073/pnas.012292899, 117551, 11773616.
32. Hughes CL, Liu PZ, Kaufman TC. Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol Dev 2004, 6:393-401. 10.1111/j.1525-142X.2004.04048.x, 15509221.
33. Damen WGM, Janssen R, Prpic N-P. Pair rule gene orthologs in spider segmentation. Evol Dev 2005, 7:618-628. 10.1111/j.1525-142X.2005.05065.x, 16336415.
34. Janssen R, Damen WGM. The ten Hox genes of the millipede Glomeris marginata. Dev Genes Evol 2006, 216:451-465. 10.1007/s00427-006-0092-5, 16816968.
35. Papillon D, Telford MJ. Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex. Dev Genes Evol 2007, 217:315-322. 10.1007/s00427-007-0141-8, 17310351.
36. Sharma PP, Schwager EE, Extavour CG, Giribet G. Hox gene expression in the harvestman Phalangium opilio reveals divergent patterning of the chelicerate opisthosoma. Evol Dev 2012, 14:450-463. 10.1111/j.1525-142X.2012.00565.x, 22947318.
37. Whitington PM, Mayer G. The origins of the arthropod nervous system: insights from the Onychophora. Arthropod Struct Dev 2011, 40:193-209. 10.1016/j.asd.2011.01.006, 21315833.
38. Hering L, Henze MJ, Kohler M, Kelber A, Bleidorn C, Leschke M, Nickel B, Meyer M, Kircher M, Sunnucks P, Mayer G. Opsins in Onychophora (velvet worms) suggest a single origin and subsequent diversification of visual pigments in arthropods. Mol Biol Evol 2012, 29:3451-3458. 10.1093/molbev/mss148, 22683812.
39. Eriksson BJ, Fredman D, Steiner G, Schmid A. Characterisation and localization of the opsin protein repertoire in the brain and retinas of a spider and an onychophoran. BMC Evol Biol 2013, 13:186. 10.1186/1471-2148-13-186, 3851285, 24010579.
40. Eriksson BJ, Tait NN, Budd GE, Janssen R, Akam M. Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Genes Evol 2010, 220:117-122. 10.1007/s00427-010-0329-1, 20567844.
41. Janssen R, Budd GE. Deciphering the onychophoran 'segmentation gene cascade': gene expression reveals limited involvement of pair rule gene orthologs in segmentation, but a highly conserved segment polarity gene network. Dev Biol 2013, 382:224-234. 10.1016/j.ydbio.2013.07.010, 23880430.
42. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
43. Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 1992, 89:10915-10919. 10.1073/pnas.89.22.10915, 50453, 1438297.
44. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol 2008, 25:1307-1320. 10.1093/molbev/msn067, 18367465.
45. Guindon S, Gascuel O. A simpel, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2001, 52:696-704.
46. Janssen R, Budd GE. Gene expression suggests conserved aspects of Hox gene regulation in arthropods and provides additional support for monophyletic Myriapoda. EvoDevo 2010, 1:4. 10.1186/2041-9139-1-4, 2938723, 20849647.
47. Grenier JK, Garber TL, Warren R, Whitington PM, Carroll S. Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr Biol 1997, 7:547-553. 10.1016/S0960-9822(06)00253-3, 9259556.
48. Shippy TD, Rogers CD, Beeman RW, Brown SJ, Denell RE. The Tribolium castaneum ortholog of Sex combs reduced controls dorsal ridge development. Genetics 2006, 74:297-307.
49. Shultz JW, Regier JC. Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean + hexapod clade. Proc Biol Sci 2000, 267:1011-1019. 10.1098/rspb.2000.1104, 1690640, 10874751.
50. Regier JC, Shultz JW, Kambic RE. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Biol Sci 2005, 272:395-401. 10.1098/rspb.2004.2917, 1634985, 15734694.
51. von Reumont BM, Jenner RA, Wills MA, Dell'ampio E, Pass G, Ebersberger I, Meyer B, Koenemann S, Iliffe TM, Stamatakis A, Niehuis O, Meusemann K, Misof B. Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Mol Biol Evol 2012, 29:1031-1045. 10.1093/molbev/msr270, 22049065.
52. Rota-Stabelli O, Campbell L, Brinkmann H, Edgecombe GD, Longhorn SJ, Peterson KJ, Pisani D, Philippe H, Telford MJ. A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata. Proc Biol Sci 2011, 278:298-306. 10.1098/rspb.2010.0590, 3013382, 20702459.
53. Sombke A, Lipke E, Kenning M, Müller CH, Hansson BS, Harzsch S. Comparative analysis of deutocerebral neuropils in Chilopoda (Myriapoda): implications for the evolution of the arthropod olfactory system and support for the Mandibulata concept. BMC Neurosci 2012, 13:1-17. 10.1186/1471-2202-13-1, 3320525, 22214384.
54. Hughes CL, Kaufman TC. Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. Development 2002, 19:1225-1238.
55. Abzhanov A, Popadic A, Kaufman TC. Chelicerate Hox genes and the homology of arthropod segments. Evol Dev 1999, 1:77-89. 10.1046/j.1525-142x.1999.99014.x, 11324031.
56. Telford MJ, Thomas RH. Of mites and zen: expression studies in a chelicerate arthropod confirm zen is a divergent Hox gene. Dev Genes Evol 1998, 208:591-594. 10.1007/s004270050219, 9811978.
57. Grbic M, Van Leeuwen T, Clark RM, Rombauts S, Rouze P, Grbic V, Osborne EJ, Dermauw W, Ngoc PC, Ortego F, Hernandez-Crespo P, Diaz I, Martinez M, Navajas M, Sucena E, Magalhaes S, Nagy L, Pace RM, Djuranovic S, Smagghe G, Iga M, Christiaens O, Veenstra JA, Ewer J, Villalobos RM, Hutter JL, Hudson SD, Velez M, Yi SV, Zeng J, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011, 479:487-492. 10.1038/nature10640, 22113690.
58. Aboobaker A, Blaxter M. Hox gene evolution in nematodes: novelty conserved. Curr Opin Genet Dev 2003, 13:593-598. 10.1016/j.gde.2003.10.009, 14638320.
59. Martin-Duran JM, Janssen R, Wennberg S, Budd GE, Hejnol A. Deuterostomic development in the protostome Priapulus caudatus. Curr Biol 2012, 22:2161-2166. 10.1016/j.cub.2012.09.037, 23103190.
60. Schwager EE, Schoppmeier M, Pechmann M, Damen WG. Duplicated Hox genes in the spider Cupiennius salei. Front Zool 2007, 4:1. 10.1186/1742-9994-4-1, 1785372, 17207286.
61. Mann RS. The specificity of homeotic gene function. Bioessays 1995, 17:855-863. 10.1002/bies.950171007, 7487967.
62. Mahaffey JW. Assisting Hox proteins in controlling body form: are there new lessons from flies (and mammals)?. Curr Opin Genet Dev 2005, 15:422-429. 10.1016/j.gde.2005.06.009, 15979870.
63. Joshi R, Sun L, Mann R. Dissecting the functional specificities of two Hox proteins. Genes Dev 2010, 24:1533-1545. 10.1101/gad.1936910, 2904943, 20634319.
64. Reed HC, Hoare T, Thomsen S, Weaver TA, White RA, Akam M, Alonso CR. Alternative splicing modulates Ubx protein function in Drosophila melanogaster. Genetics 2010, 184:745-775. 10.1534/genetics.109.112086, 2845342, 20038634.
65. Castelli-Gair J, Akam M. How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres. Development 1995, 121:2973-2982.
66. Castelli-Gair J. Implications of the spatial and temporal regulation of Hox genes on development and evolution. Int J Dev Biol 1998, 42:437-444.
67. Smolik-Utlaut SM. Dosage requirements of Ultrabithorax and bithoraxoid in the determination of segment identity in Drosophila melanogaster. Genetics 1990, 124:357-366. 1203927, 1968411.
68. Tour E, Hittinger CT, McGinnis W. Evolutionarily conserved domains required for activation and repression functions of the Drosophila Hox protein Ultrabithorax. Development 2005, 132:5271-5281. 10.1242/dev.02138, 16284118.
69. Liubicich DM, Serano JM, Pavlopoulos A, Kontarakis Z, Protas ME, Kwan E, Chatterjee S, Tran KD, Averof M, Patel NH. Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc Natl Acad Sci USA 2009, 106:13892-13896. 10.1073/pnas.0903105106, 2720850, 19666517.