Diversification of arthropod Hox genes as a paradigm for the evolution of gene functions

Seminars in Cell and Developmental Biology

Volumn 7, Issue 4, 1996, Pages 539-551

  Averof, Michails ^a   Dawes, Rachel ^b   Ferrier, David ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b WELLCOME CRC INSTITUTE   (United Kingdom)

Author keywords

Arthropods; Evolution; Gene duplication; Hox genes; Regulatory elements

Indexed keywords

ARTHROPODA; METAZOA;

EID: 0000716873     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1996.0068     Document Type: Article

References (127)

1. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283-302
2. Manak RJ, Scott MP (1994) A class act: conservation of homeodomain protein functions. Development Supplement 61-71
3. Slack JMW, Holland PWH, Graham CF (1993) The zootype and the phylotypic stage. Nature 361:490-492
4. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:567-570
5. Kaufman TC, Seeger MA, Olsen G (1990) Molecular and genetic organization of the Antennapedia gene complex of Drosophila melanogaster. Adv Genet 27:309-362
6. Schubert FR, Nieselt-Struwe K, Gruss P (1993) The Antenna-pedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proc Natl Acad Sci USA 90:143-147
7. Garcia-Fernàndez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563-566
8. Bürglin TR (1994) A comprehensive classification of homeobox genes, in Guidebook to the Homeobox Genes (Duboule D, ed.) pp 27-71. Oxford University Press, Oxford
9. Akam M, Dawson I, Tear G (1988) Homeotic genes and the control of segment diversity. Development Supplement 123-134
10. Dollé P, Fraulob V, Duboule D (1994) Developmental expression of the mouse Evx-2 gene: relationship with the evolution of the HOM/Hox complex. Development Supplement 143-153
11. Wang BB, Muller-Immergluck MM, Austin J, Robinson NT, Chisholm A, Kenyon C (1993) A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74:2942
12. Valerius MT, Li H, Stock JL, Weinstein M, Kaur S, Singh G, Potter SS (1995) gsh-1 - a novel murine homeobox gene expressed in the central nervous system. Developmental Dynamics 203:337-351
13. Wright CVE, Schnegelsberg P, De Robertis EM (1988) XlHbox8: a novel Xenopus homeo protein restricted to a narrow band of endoderm. Development 104:787-794
14. Wysocka-Diller J, Aisemberg GO, Macagno ER (1995) A novel homeobox cluster expressed in repeated structures of the midgut. Dev Biol 171:439-447
15. Warren RW, Nagy L, Selegue J, Gates J, Carroll S (1994) Evolution of homeotic gene regulation and function in flies and butterflies. Nature 372:458-461
16. DeLorenzi M, Bienz M (1990) Expression of Abdominal-B homeoproteins in Drosophila embryos. Development 108:323-329
17. Casanova J, Sánchez-Herrero E, Morata G (1986) Identification and characterization of a parasegment specific regulatory element of the Abdominal-B gene of Drosophila. Cell 47:627-636
18. Celniker SE, Sharma S, Keelan DJ, Lewis EB (1990) The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J 9:4277-4286
19. Kelsh R, Dawson I, Akam M (1993) An analysis of Abdominal-B expression in the locust Schistocerca gregaria. Development 117:293-305
20. Castelli-Gair J, Greig S, Micklem G, Akam M (1994) Dissecting the temporal requirements for homeotic gene function. Development 120:1983-1995
21. Castelli-Gair J, Akam M (1995) How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metemeres. Development 121:2973-2982
22. Averof M, Akam M (1995) Insect-crustacean relationships: insights from comparative developmental and molecular studies. Phil Trans Roy Soc Lond (Biol) 347:293-303
23. Boore JL, Collins TM, Standon D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376:163-165
24. Friedrich M, TautzD (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165-167
25. Patel NH, Kornberg TB, Goodman CS (1989) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201-212
26. Calman WT (1909) Crustacea. A Treatise on Zoology 7 (Lankester ER, ed.). Adam and Charles Black, London
27. Averof M, Akam M (1993) HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans. Curr Biol 3:73-78
28. Cartwright P, Dick M, Buss LW (1993) HOM/Hox type homeoboxes in the chelicerate Limulus polyphemus. Mol Phyl Evol 2:185-192
29. Shankland M, Martin dale MQ, Nardelli-Haefliger D, Baxter E, Price DJ (1991) Origin of segmental identity in the development of the leech nervous system. Development Supplement 2:29-38
30. Aisemberg GO, Macagno ER (1994) Lox1, an Antennapedia-class homeobox gene, is expressed during leech gangliogenesis in both transient and stable central neurons. Dev Biol 161:455-465
31. Wong VY, Aisemberg GO, Wen-Biao G, Macagno ER (1995) The leech homeobox gene Lox4 may determine segmental differentiation of identified neurons. J Neurosci 15:5551-5559
32. Nardelli-Haefliger D, Shankland M (1992) Lox2, a putative leech segment identity gene, is expressed in the same segmental domain in different stem cell lineages. Development 116:697-710
33. Dick MH, Buss LW (1994) A PCR-based survey of homeobox genes in Ctenodrillus serratus (Annelida: Polychaeta). Mol Phyl Evol 3:146-158
34. Snow P, Buss LW (1994) HOM/Hox-type homeoboxes from Stylaria lacustris (Annelida: Oligochaeta). Mol Phyl Evol 3:360-364
35. Averof M, Akam M (1995) Hox genes and the diversification of insect and crustacean body plans. Nature 376:420-423
36. Macias A, Casanova J, Morata G (1990) Expression and regulation of the abd-A gene of Drosophila. Development 110:1197-1207
37. Gaunt SJ, Krumlauf R, Duboule D (1989) Mouse homeo-genes within a subfamily, Hox-1.4, -2.6 and -5.1, display similar anteroposterior domains of expression in the embryo, but show stage- and tissue-dependent differences in their regulation. Development 107:131-141
38. 2 genes display dynamic dorsoventral patterns of gene expression during central nervous system development. Development 112:255-264
39. Hunt P, Gulisano M, Cook M, Sham M-H, Faiella A, Wilkinson D, Boncinelli E, Krumlauf R (1991) A distinct Hox code for the branchial region of the vertebrate head. Nature 353:861-864
40. Wakimoto BT, Turner FR, Kaufman TC (1984) Defects in embryogenesis in mutants associated with the Antennapedia gene complex of Drosophila melanogaster. Dev Biol 102:147-172
41. Doe CQ, Hiromi X Gehring WJ, Goodman CS (1988) Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science 239:170-175
42. Rushlow C, Levine M (1990) Role of the zerknüllt gene in dorsal-ventral pattern formation in Drosophila. Adv Genet 27:277-307
43. Falciani F, Hausdorf B, Schroeder R, Akam M, Tautz D, Dennell R, Brown S (1996) Class 3 Hox genes in insects and the origin of zen. PNAS, in press
44. Rushlow C, Doyle H, Hoey T, Levine M (1987) Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev 1:1268-1279
45. Randazzo FM, Seeger MA, Huss CA, Sweeney MA, Cecil JK, Kaufman TC (1993) Structural changes in the Antennapedia complex of Drosophila pseudoobscura. Genetics 133:319-330
46. Terol J, Perez-Alonso M, Frutos Rd (1995) Molecular characterization of the zerknüllt region of the Antennapedia complex of D. subobscura. Chromosoma 103:613-624
47. Frönhofer HG, Nüsslein-Volhard C (1986) Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324:120-125
48. Driever W, Nüsslein-Volhard C (1988) The Bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54:95-104
49. Schröder R, Sander K (1993) A comparison of transplantable bicoid activity and partial bicoid homeobox sequences in several Drosophila and blowfly species (Calliphoridae). Roux's Arch Dev Biol 203:34-43
50. Mann RS (1995) The functional specificity of homeotic gene function. BioEssays 17:855-863
51. Gehring WJ (1994) A history of the homeobox, in Guidebook to the Homeobox Genes (Duboule D, ed.) pp 1-10. Oxford University Press, Oxford
52. Treisman J, Harris E, Wilson D, Desplan C (1992) The homeodomain: a new face for the helix-turn-helix? BioEssays 14:145-150
53. Dawes R, Dawson I, Falciani F, Tear G, Akam M (1994) Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120:1561-1572
54. Brown SJ, Hilgenfeld RB, Denell RE (1994) The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc Natl Acad Sci USA 91:12922-12926
55. Wirz J, Fessler L, Gehring WJ (1986) Localization of the Antennapedia protein in the Drosophila embryo and imaginal discs. EMBO J 5:3327-3334
56. Pultz MA, Diederich RJ, Cribbs DL, Kaufman TC (1988) The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. Genes Dev 2:901-920
57. Diederich RJ, Merrill VKL, Pultz MA, Kaufman TC (1989) Isolation, structure and expression of labial, a homeotic gene of the Antennapedia complex involved in Drosophila head development. Genes Dev 3:399-414
58. Gindhart JG, King AN, Kaufman TC (1995) Characterization of the cis-regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139:781-795
59. Hoppler S, Bienz M (1994) Specification of a single cell type by a Drosophila homeotic gene. Cell 76:689-702
60. Martin CH, Mayeda CA, Davis CA, Ericsson CL, Knafels JD, Mathog DR, Celniker SE, Lewis EB, Palazzolo MJ (1995) Complete sequence of the bithorax complex of Drosophila. Proc Natl Acad Sci USA 92:8398-8402
61. Duncan I (1987) The bithorax complex. Annu Rev Genet 21:285-319
62. Hiromi X Kuroiwa A, Gehring WJ (1985) Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43:603-613
63. Izpisúa-Belmonte J-C, Falkenstein H, Dollé P, Renucci A, Duboule D ( 1991) Murine genes related to the Drosophila AbdB homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J 10:2279-2289
64. Buttgereit D, Renkawitzpohl R (1993) Expression of beta-1 tubulin (beta-tub56D) in Drosophila testis stem-cells is regulated by a short upstream sequence while intron elements guide expression in somatic-cells. Molec Gen Genet 241:263-270
65. Edgar BA, Lehman DA, O'Farrell PH (1994) Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development 120:3131-3143
66. Hanks M, Wurst W, Anson-Cartwright L, Auerbach AA, Joyner AL (1995) Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science 269:679-682
67. Gao D, Kimble J (1995) APX-1 can substitute for its homolog LAG-2 to direct cell interactions throughout Caenorhabditis elegans development. Proc Natl Acad Sci USA 92:9839-9842
68. Li X, Noll M (1994) Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory elements. Nature 367:83-87
69. Rothe M, Pehl M, Taubert H, Jäckle H (1992) Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature 359:156-159
70. Mahaffey JW, Diederich RJ, Kaufman TC (1989) Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo. Development 105:167-174
71. Beeman R, Stuart JJ, Haas MS, Denell RE (1989) Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. Dev Biol 133:196-209
72. Beeman RW, Stuart JJ, Brown SJ, Denell RE (1993) Structure and function of the homeotic gene complex (HOM-C) in the beetle, Tribolium castaneum. BioEssays 15:439-444
73. Fleig R, Walldorf U, Gehring WJ, Sander K (1988) In situ localization of the transcripts of a homeobox gene in the honeybee Apis mellifera L. (Hymenoptera). Roux's Arch Dev Biol 197:269-274
74. Fleig R, Walldorf U, Gehring WJ, Sander K (1992) Development of the Deformed protein pattern in the embryo of the honeybee Apis mellifera L. (Hymenoptera). Roux's Arch Dev Biol 201:235-242
75. Tear G (1990) A molecular analysis of embryonic development in the short germ band insect Schistocerca gregaria. PhD thesis. Univ. Cambridge
76. Hayward DC, Patel NH, Rehm EJ, Goodman CS, Ball EE (1995) Sequence and expression of a grasshopper Antennapedia: comparison to Drosophila. Dev Biol 172:452-465
77. White RAH, Wilcox M (1985) Distribution of Ultrabithorax proteins in Drosophila. EMBO J 4:2035-2043
78. Ueno K, Hui C-C, Fukuta M, Suzuki Y (1992) Molecular analysis of the deletion mutants in the E homeotic complex of the silkworm Bombyx mori. Development 114:555-563
79. Kelsh R, Weinzierl ROJ, White RAH, Akam M (1994) Homeotic gene expression in the locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and Abdominal-A proteins. Dev Genet 15:19-31
80. Nagy LM, Booker R, Riddiford LM (1991) Isolation and embryonic expression of an abdominal-A-like gene from the lepidopteran, Manduca sexta. Development 112:119-129
81. Stuart JJ, Brown SJ, Beeman RW, Denell RE (1993) The Tribolium homeotic gene Abdominal is homologous to abdominal-A of the Drosophila bithorax complex. Development 117:233-243
82. Tear G, Akam M, Martinez-Arias A (1990) Isolation of an abdominal-A gene from the locust Schistocerca gregaria and its expression during early embryogenesis. Development 110:915-925
83. Zhao JJ, Lazzarini RA, Pick L (1993) The mouse Hox-1.3 gene is functionally equivalent to the Drosophila Sex combs reduced gene. Genes Dev 7:343-354
84. Sham MH, Hunt P, Nonchev S, Papalopulu N, Graham A, Boncinelli E, Krumlauf R (1992) Analysis of the murine Hox-2.7 gene: conserved alternative transcripts with differential distributions in the nervous system and the potential for shared regulatory elements. EMBO J 11:1825-1836
85. Condie BG, Capecci MR (1993) Mice homozygous for a targeted disruption of Hoxd-3 (Hox4.1) exhibit anterior transformations of the first and second cervical vertebrae, the atlas and the axis. Development 119:579-595
86. Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54:83-93
87. Seeger MA, Kaufman TC (1990) Molecular analysis of the bicoid gene from Drosophila pseudoobscura: identification of conserved domains within coding and non-coding regions of the bicoid mRNA. EMBO J 9:2977-2987
88. Sommer R, Tautz D (1991) Segmentation gene expression in the housefly Musca domestica. Development 113:419-430
89. Carroll SB, Scott MP (1985) Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell 43:47-57
90. Jost W, Yu Y, Pick L, Preiss A, Maier D (1995) Structure and regulation of the fushi tarazu gene from Drosophila hydei. Roux's Arch Dev Biol 205:160-170
91. Macdonald PM, Ingham P, Struhl G (1986) Isolation, structure and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeobox. Cell 47:721-734
92. Frasch M, Hoey T, Rushlow C, Doyle HJ, Levine M (1987) Characterization and localization of the even-skipped protein of Drosophila. EMBO J 6:749-759
93. Nüsslein-Volhard C, Kluding H, Jürgens G (1985) Genes affecting the segmental subdivision of the Drosophila embryo. Cold Spring Harb Symp Quant Biol 50:145-154
94. Doe CQ, Smouse D, and Goodman CS (1988) Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333:376-378
95. Patel NH, Condron BG, Zinn K (1994) Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367:429-434
96. Patel NH, Ball EE, Goodman CS (1992) Changing role of even-skipped during the evolution of insect pattern formation. Nature 357:339-342
97. Spyropoulos DD, Capecchi MR (1994) Targeted disruption of the even-skipped gene, evx1, causes early postimplantation lethality of the mouse conceptus. Genes Dev 8:1949-1961
98. Ahringer J (1996) Posterior patterning by the C. elegans even-skipped homolog vab-7. Genes Dev, in press
99. Mlodzik M, Fjose A, Gehring WJ (1985) Isolation of caudal, a Drosophila homeobox-containing gene with maternal expression whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J 4:2961-2969
100. Macdonald PM, Struhl G (1986) A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324:537-545
101. Xu X, Xu PX, Suzuki Y (1994) A maternal homeobox gene, Bombyx caudal, forms both mRNA and protein concentration gradients spanning anteroposterior axis gastrulation. Development 120:277-285
102. Meyer BI, Gruss P (1993) Mouse Cdx-1 expression during gastrulation. Development 117:191-203
103. Subramanian V, Meyer BI, Gruss P (1995) Disruption of the murine homeobox gene Cdx-1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83:641-653
104. Gamer LW, Wright CVE (1993) Murine Cdx-4 bears striking similarities to the Drosophila Caudal gene in its homeodomain sequence and early expression pattern. Mech Dev 43:71-81
105. Frumkin A, Pillemer G, Haffner R, Tarcic N, Gruenbaum Y, Fainsod A (1994) A role for CdxA in gut closure and intestinal epithelia differentiation. Development 120:253-263
106. Waring DA, Kenyon C (1990) Selective silencing of cell communication influences anteroposterior pattern formation in C. elegans. Cell 60:123-131
107. Dalton D, Chadwick R, McGinnis W (1989) Expression and embryonic function of empty spiracles: a Drosophila homeobox gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev 3:1940-1956
108. Cohen SM, Jürgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482-485
109. Simeone A, Acampora D, Gulisano M, Stornaiuolo A, Boncinelli E (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature 358:687-690
110. Kastury K, Druck T, Huebner K, Barletta C, Acampora D, Simeone A, Faiella A, Boncinelli E (1994) Chromosome locations of human EMX and OTX genes. Genomics 22:41-45
111. Finkelstein R, Smouse D, Capaci TM, Spradling AC, Perrimon N (1990) The orthodenticle gene encodes a novel homeodomain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev 4:1516-1527
112. Matsuo I, Kuratani S, Kimura C, Takeda N, Aizawa S (1995) Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev 9:2646-2658
113. Chouinard S, Kaufman TC (1991) Control of expression of the homeotic labial (lab) locus of Drosophila melanogaster. evidence for both positive and negative autogenous regulation. Development 113:1267-1280
114. Kapoun AM, Kaufman TC (1995) A functional analysis of 5', intronic and promoter regions of the homeotic gene proboscipedia in Drosophila melanogaster. Development 121:2127-2141
115. Bergson C, McGinnis W (1990) An autoregulatory enhancer element of the Drosophila homeotic gene Deformed. EMBO J 9:4287-4297
116. Pick L, Schier A, Affolter M, Schmidt-Glenewinkel T, Gehring WJ (1990) Analysis of the ftz upstream element: germ layer-specific enhancers are independently autoregulated. Genes Dev 4:1224-1239
117. Boulet AM, Scott MP (1988) Control elements of the P2 promoter of the Antennapedia gene. Genes Dev 2:1600-1614
118. Zink B, Engstrom Y, Gehring WJ, Paro R (1991) Direct interaction of the Polycomb protein with Antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J 10:153-162
119. Kornfeld K, Saint RB, Beachy PA, Harte PJ, Peattie DA, Hogness DS (1989) Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev 3:243-258
120. Qian S, Capovilla M, Pirrotta V (1991) The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J 10:1415-1425
121. Müller J, Bienz M (1991) Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J 10:3147-3155
122. Chan C-S, Rastelli L, Pirrotta V (1994) A Plycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J 13:2553-2564
123. Christen B, Bienz M (1992) A cis-element mediating Ultrabithorax autoregulation in the central nervous system. Mech Dev 39:73-80
124. Thuringer F, Cohen SM, Bienz M (1993) Dissection of an indirect autoregulatory response of a homeotic Drosophila gene. EMBO J 12:2419-2430
125. Simon J, Chiang A, Bender W, Shimell MJ, O'Connor M (1993) Elements of the Drosophila Bithorax Complex that mediate repression by Polycomb group products. Dev Biol 158:131-144
126. Celniker SE, Keelan DJ, Lewis EB (1989) The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev 3:1424-1436
127. Busturia A, Bienz M (1993) Silencers in Abdominal-B, a homeotic Drosophila gene. EMBO J 12:1415-1425