We describe the properties of a new gene, sop-3, that is required for the regulated expression of a C. elegans Hox gene, egl-5, in a postembryonic neuroectodermal cell lineage. Regulated expression of egl-5 in this cell lineage is necessary for development of the sensory rays of the male tail. sop-3 encodes a predicted novel protein of 1475 amino acids without clear homologs in other organisms. However, the sequence contains motifs consisting of homopolymeric runs of amino acids found in several other transcriptional regulators, some of which also act in Hox gene regulatory pathways. The genetic properties of sop-3 are very similar to those of sop-1, which encodes a component of the transcriptional Mediator complex, and mutations in the two genes are synthetic lethal. This suggests that SOP-3 may act at the level of the Mediator complex in regulating transcription initiation. In a sop-3 loss-of-function background, egl-5 is expressed ectopically in lineage branches that normally do not express this gene. Such expression is dependent on the Hox gene mab-5, as it is in branches where egl-5 is normally expressed. Ectopic egl-5 expression is also dependent on the Wnt pathway. Thus, sop-3 contributes to the combinatorial control of egl-5 by blocking egl-5 activation by MAB-5 and the Wnt pathway in inappropriate lineage branches.

Reference

Baird
S. E.
,
Fitch
D. H. A.
,
Kassem
I. A. A.
,
Emmons
S. W.
(
1991
)
Pattern formation in the nematode epidermis: determination of the spatial arrangement of peripheral sense organs in the C. elegans male tail.
Development
113
,
515
526
Barr
M. M.
,
Sternberg
P. W.
(
1999
)
A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans.
Nature
401
,
386
389
Bjorklund
S.
,
Almouzni
G.
,
Davidson
I.
,
Nightingale
K. P.
,
Weiss
K.
(
1999
)
Global transcription regulators of eukaryotes.
Cell
96
,
759
767
Boyer
T. G.
,
Martin
M. E. D.
,
Lees
E.
,
Ricciardi
R. P.
,
Berk
A. J.
(
1999
)
Mammalian Srb/Mediator complex is targeted by adenovirus E1A protein.
Nature
399
,
276
279
Brenner
S.
(
1974
)
The genetics of Caenorhabditis elegans.
Genetics
77
,
71
94
Castelli-Gair
J.
(
1998
)
The lines gene of Drosophila is required for specific functions of the Abdominal-B HOX protein.
Development
125
,
1269
1274
Cavallo
R. A.
,
Cox
R. T.
,
Moline
M. M.
,
Roose
J.
,
Polevoy
G. A.
,
Clevers
H.
,
Peifer
M.
,
Bejsovec
A.
(
1998
)
Drosophila Tcf and Groucho interact to repress Wingless signalling activity.
Nature
395
,
604
608
Chisholm
A.
(
1991
)
Control of cell fate in the tail region of C. elegans by the gene egl-5.
Development
111
,
921
932
Chow
K. L.
,
Emmons
S. W.
(
1994
)
HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail.
Development
120
,
2579
2593
Cosma
M. P.
,
Tanaka
T.
,
Nasmyth
K.
(
1999
)
Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle-and developmentally regulated promoter.
Cell
97
,
299
311
de Zulueta.
P.
,
Alexandre
E.
,
Jacq
B.
,
Kerridge
S.
(
1994
)
Homeotic complex and teashirt genes co-operate to establish trunk segmental identities in Drosophila.
Development
120
,
2287
2296
Eisenmann
D. M.
,
Maloof
J. N.
,
Simske
J. S.
,
Kenyon
C.
,
Kim
S. K.
(
1998
)
The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development.
Development
125
,
3667
3680
Fasano
L.
,
Roder
L.
,
Core
N.
,
Alexandre
E.
,
Vola
C.
,
Jacq
B.
,
Kerridge
S.
(
1991
)
The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs.
Cell
64
,
63
79
Ferreira
H. B.
,
Zhang
Y.
,
Zhao
C.
,
Emmons
S. W.
(
1999
)
Patterning of Caenorhabditis elegans posterior structures by the Abdominal-B homolog, egl-5.
Dev. Biol
207
,
215
228
Fire
A.
,
Xu
S.
,
Montgomery
M. K.
,
Kostas
S. A.
,
Driver
S. E.
,
Mello
C. C.
(
1998
)
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.
Nature
391
,
806
811
Gallet
A.
,
Erkner
A.
,
Charroux
B.
,
Fasano
L.
,
Kerridge
S.
(
1998
)
Trunk-specific modulation of wingless signalling in Drosophila by teashirt binding to armadillo.
Curr. Biol
8
,
893
902
Gallet
A.
,
Angelats
C.
,
Erkner
A.
,
Charroux
B.
,
Fasano
L.
,
Kerridge
S.
(
1999
)
The C-terminal domain of armadillo binds to hypophosphorylated teashirt to modulate wingless signalling in Drosophila.
EMBO J
18
,
2208
2217
Gellon
G.
,
McGinnis
W.
(
1998
)
Shaping animal body plans in development and evolution by modulation of Hox expression patterns.
BioEssays
20
,
116
125
Hanna-Rose
W.
,
Hansen
U.
(
1996
)
Active repression mechanisms of eukaryotic transcription repressors.
Trends Genet
12
,
229
234
Hatini
V.
,
Bokor
P.
,
Goto-Mandeville
R.
,
DiNardo
S.
(
2000
)
Tissue-and stage-specific modulation of Wingless signaling by the segment polarity gene lines.
Genes Dev
14
,
1364
1376
Herman
M. A.
,
Vassilieva
L. L.
,
Horvitz
H. R.
,
Shaw
J. E.
,
Herman
R. K.
(
1995
)
The C. elegans gene lin-44, which controls the polarity of certain asymmetric cell divisions, encodes a Wnt protein and acts cell nonautonomously.
Cell
83
,
101
110
Hunter
C. P.
,
Harris
J. M.
,
Maloof
J. N.
,
Kenyon
C.
(
1999
)
Hox gene expression in a single Caenorhabditis elegans cell is regulated by a caudal homolog and intercellular signals that inhibit Wnt signaling.
Development
126
,
805
814
Ito
M.
,
Yuan
C. X.
,
Malik
S.
,
Gu
W.
,
Fondell
J. D.
,
Yamamura
S.
,
Fu
Z. Y.
,
Zhang
X.
,
Qin
J.
,
Roeder
R. G.
(
1999
)
Identity between TRAP and SMCC complexes indicates novel pathways for the function of nuclear receptors and diverse mammalian activators.
Mol. Cell
3
,
361
370
Kornberg
R. D.
,
Lorch
Y.
(
1999
)
Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome.
Cell
98
,
285
294
Korswagen
H. C.
,
Herman
M. A.
,
Clevers
H. C.
(
2000
)
Distinct beta-catenins mediate adhesion and signalling functions in C. elegans.
Nature
406
,
527
532
Laughon
A.
,
Carroll
S. B.
,
Storfer
F. A.
,
Riley
P. D.
,
Scott
M. P.
(
1985
)
Common properties of proteins encoded by the Antennapedia complex genes of Drosophila melanogaster.
Cold Spring Harb. Symp. Quant. Biol
50
,
253
262
Lin
R.
,
Hill
R. J.
,
Priess
J. R.
(
1998
)
POP-1 and anterior-posterior fate decisions in C. elegans embryos.
Cell
92
,
229
239
Lints
R.
,
Emmons
S. W.
(
1999
)
Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGF-family signaling pathway and a Hox gene.
Development
126
,
5819
5831
Maloof
J. N.
,
Whangbo
J.
,
Harris
J. M.
,
Jongeward
G. D.
,
Kenyon
C.
(
1999
)
A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans.
Development
126
,
37
49
Mann
R. S.
,
Abu-Shaar
M.
(
1996
)
Nuclear import of the homeodomain protein Extradenticle in response to Wg and Dpp signalling.
Nature
383
,
630
633
Marshall
H.
,
Morrison
A.
,
Studer
M.
,
Popperl
H.
,
Krumlauf
R.
(
1996
)
Retinoids and Hox genes.
FASEB J
10
,
969
978
McGinnis
N.
,
Ragnhildstveit
E.
,
Veraksa
A.
,
McGinnis
W.
(
1998
)
A cap ‘n’ collar protein isoform contains a selective Hox repressor function.
Development
125
,
4553
4564
Mohler
J.
,
Mahaffey
J. W.
,
Deutsch
E.
,
Vani
K.
(
1995
)
Control of Drosophila head segment identity by the bZIP homeotic gene cnc.
Development
121
,
237
247
Petcherski
A. G.
,
Kimble
J.
(
2000
)
LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway.
Nature
405
,
364
368
Pflugrad
A.
,
Meir
J. Y.
,
Barnes
T. M.
,
Miller
D. M.,
III
(
1997
)
The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans.
Development
124
,
1699
1709
Rieckhof
G. E.
,
Casares
F.
,
Ryook
H. D.
,
Abu-Shaar
M.
,
Mann
R. S.
(
1997
)
Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein.
Cell
91
,
171
183
Roose
J.
,
Molenaar
M.
,
Peterson
J.
,
Hurenkamp
J.
,
Brantjes
H.
,
Moerer
P.
,
van de Wetering
M.
,
Destree
O.
,
Clevers
H.
(
1998
)
The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors.
Nature
395
,
608
612
Salser
S. J.
,
Kenyon
C.
(
1996
)
A C. elegans Hox gene switches on, off, on and off again to regulate proliferation, differentiation and morphogenesis.
Development
122
,
1651
1661
Singh
N.
,
Han
M.
(
1995
)
sur-2, a novel gene, functions late in the let-60 ras -mediated signaling pathway during Caenorhabditis elegans vulval induction.
Genes Dev
9
,
2251
2265
Smoller
D.
,
Friedel
C.
,
Schmid
A.
,
Bettler
D.
,
Lam
L.
,
Yedvobnick
B.
(
1990
)
The Drosophila neurogenic locus mastermind encodes a nuclear protein unusually rich in amino acid homopolymers.
Genes Dev
4
,
1688
1700
Struhl
K.
(
1999
)
Fundamentally different logic of gene regulation in eukaryotes and prokaryotes.
Cell
98
,
1
4
Waring
D. A.
,
Kenyon
C.
(
1991
)
Regulation of cellular responsiveness to inductive signals in the developing C. elegans nervous system.
Nature
350
,
712
715
Zhang
H.
,
Emmons
S. W.
(
2000
)
A C. elegans mediator protein confers regulatory selectivity on lineage-specific expression of a transcription factor gene.
Genes Dev
14
,
2161
2172
Zhao
C.
,
Emmons
S. W.
(
1995
)
A transcription factor controlling development of peripheral sense organs in C. elegans.
Nature
373
,
74
78
This content is only available via PDF.