Stripy Ftz target genes are coordinately regulated by Ftz-F1.
During development, cascades of regulatory genes act in a hierarchical fashion to subdivide the embryo into increasingly specified body regions. This has been best characterized in Drosophila, where genes encoding regulatory transcription factors form a network to direct the development of the basic segmented body plan. The pair-rule genes are pivotal in this process as they are responsible for the first subdivision of the embryo into repeated metameric units. The Drosophila pair-rule gene fushi tarazu (ftz) is a derived Hox gene expressed in and required for the development of alternate parasegments. Previous studies suggested that Ftz achieves its distinct regulatory specificity as a segmentation protein by interacting with a ubiquitously expressed cofactor, the nuclear receptor Ftz-F1. However, the downstream target genes regulated by Ftz and other pair-rule genes to direct segment formation are not known. In this study, we selected candidate Ftz targets by virtue of their early expression in Ftz-like stripes. This identified two new Ftz target genes, drumstick (drm) and no ocelli (noc), and confirmed that Ftz regulates a serotonin receptor (5-HT2). These are the earliest Ftz targets identified to date and all are coordinately regulated by Ftz-F1. Engrailed (En), the best-characterized Ftz/Ftz-F1 downstream target, is not an intermediate in regulation. The drm genomic region harbors two separate seven-stripe enhancers, identified by virtue of predicted Ftz-F1 binding sites, and these sites are necessary for stripe expression in vivo. We propose that pair-rule genes, exemplified by Ftz/Ftz-F1, promote segmentation by acting at different hierarchical levels, regulating first, other segmentation genes; second, other regulatory genes that in turn control specific cellular processes such as tissue differentiation; and, third, 'segmentation realizator genes' that are directly involved in morphogenesis.
Hou
Hui Ying
HY
Department of Entomology, University of Maryland, College Park, 20742, USA.
Heffer
Alison
A
Anderson
W Ray
WR
Liu
Jingnan
J
Bowler
Timothy
T
Pick
Leslie
L
D000818:Animals; D004268:DNA-Binding Proteins / Q000235:genetics*; D004330:Drosophila / Q000196:embryology / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics*; D004742:Enhancer Elements, Genetic; D018507:Gene Expression Regulation, Developmental; D010858:Pigmentation / Q000235:genetics*; D014157:Transcription Factors / Q000235:genetics*
D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D014157:Transcription Factors; C499712:nuclear hormone receptor FTZ-F1, Drosophila
Genes Dev. 1990 Mar;4(3):433-43
2110923
Mech Dev. 1994 Nov;48(2):119-28
7873402
Mech Dev. 1999 Sep;87(1-2):77-91
10495273
Mech Dev. 1994 Sep;47(3):241-51
7848871
Development. 1997 Feb;124(4):839-47
9043065
Mech Dev. 2001 Sep;107(1-2):39-53
11520662
Development. 1997 Apr;124(7):1343-54
9118805
Dev Dyn. 2005 Mar;232(3):685-94
15712202
Development. 2001 Apr;128(7):1109-18
11245576
Nature. 1997 Feb 6;385(6616):552-5
9020364
Genes Dev. 2005 Mar 15;19(6):709-18
15769943
PLoS Biol. 2004 Sep;2(9):E271
15340490
Genetics. 1996 Dec;144(4):1673-9
8978054
Development. 1988 Nov;104(3):447-51
3256471
Dev Genet. 1998;23(1):28-34
9706691
Nature. 1992 Apr 16;356(6370):610-2
1348571
Mech Dev. 1997 Nov;68(1-2):157-72
9431813
Mech Dev. 1999 May;83(1-2):95-105
10381570
Development. 2001 Dec;128(24):5129-38
11748148
Dev Biol. 2002 Mar 1;243(1):1-19
11846473
Dev Dyn. 2007 Apr;236(4):991-9
17366631
Mol Cell Biol. 1998 Jun;18(6):3384-94
9584179
Genome Biol. 2002;3(12):RESEARCH0088
12537577
Development. 1999 Apr;126(7):1515-26
10068644
Development. 2002 Aug;129(15):3585-96
12117809
Genes Dev. 1987 Dec;1(10):1212-25
3123316
Mol Cell Biol. 1991 Jul;11(7):3613-23
1675428
Dev Cell. 2006 Oct;11(4):459-70
17011486
Annu Rev Cell Biol. 1986;2:49-80
2881561
Genes Dev. 1988 Mar;2(3):350-60
2897943
Dev Biol. 2006 Nov 1;299(1):78-90
16996052
Development. 1998 Sep;125(17):3427-36
9693146
Cell. 1989 Feb 24;56(4):573-83
2563673
Cell. 1984 Jul;37(3):833-41
6430568
Nature. 1996 Jan 11;379(6561):162-5
8538765
Development. 1993 Feb;117(2):609-23
8330531
Dev Biol. 2004 May 15;269(2):609-22
15110723
Genes Dev. 1990 Jul;4(7):1224-39
1976571
Development. 1989 Apr;105(4):761-7
2598812
Cell. 1985 Nov;43(1):47-57
3000605
Cell. 1989 Apr 21;57(2):223-32
2495181
Chromosoma. 1989 Aug;98(2):81-5
2476281
Curr Biol. 2005 Apr 12;15(7):643-9
15823536
Nat Rev Genet. 2005 Dec;6(12):893-904
16341070
EMBO J. 1992 Oct;11(10):3653-61
1356761
Cell. 1989 Jun 16;57(6):1017-30
2567631
Development. 1994 Apr;120(4):827-41
7600960
Development. 2003 Feb;130(4):719-28
12506002
Dev Biol. 2003 May 1;257(1):153-65
12710964
Cold Spring Harb Symp Quant Biol. 1985;50:145-54
3868475
Nature. 1988 Jan 7;331(6151):73-5
2893285
Genetics. 2000 Jan;154(1):273-84
10628987
Mech Dev. 1999 Sep;87(1-2):67-76
10495272
Nature. 1997 Feb 6;385(6616):548-52
9020363
Cell. 1990 Jan 12;60(1):9-16
2403844
PLoS Biol. 2007 May;5(5):e117
17456005
Dev Biol. 2003 Nov 15;263(2):282-95
14597202
Development. 2007 Sep;134(17):3049-54
17652351
Genes Dev. 1992 Jun;6(6):1082-96
1350560
Mech Dev. 2003 Oct;120(10):1139-51
14568103
EMBO J. 1993 Mar;12(3):1111-9
8096173
Genetics. 1992 Jul;131(3):643-53
1628809
Mol Cell. 1999 Feb;3(2):143-9
10078197
Cell. 1986 Mar 28;44(6):949-57
3955654
Dev Biol. 1984 Mar;102(1):147-72
6421639
New Biol. 1990 Feb;2(2):171-8
1982071
Development. 1996 Jan;122(1):205-14
8565831
Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1450-4
8434005
Semin Cell Dev Biol. 2008 Jun;19(3):263-70
18343171
Dev Cell. 2001 Jul;1(1):27-36
11703921
Nature. 2008 Nov 20;456(7220):400-3
18931655
Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5441-5
7777527
Cell. 1987 Sep 11;50(6):963-74
2887293
Science. 2008 Sep 5;321(5894):1314
18772429
Mech Dev. 1990 Dec;33(1):1-18
1982920
Nature. 1987 Jul 30-Aug 5;328(6129):440-2
2886916
EMBO J. 1990 Dec;9(12):3957-66
2174353
Dev Cell. 2004 Mar;6(3):343-55
15030758
Development. 1993 Dec;119(4):1359-69
8306893
Dev Biol. 1996 May 1;175(2):314-24
8626035
Dev Genes Evol. 1998 Jul;208(5):290-4
9683745