The identity and developmental pattern of the four organ types constituting the flower is governed by three developmental functions, A, B and C, which are defined by homeotic genes and established in two adjacent whorls. In this report we morphologically and genetically characterise mutants of two genes, STYLOSA (STY) and FISTULATA (FIS) which control floral homeotic meristem- and organ-identity genes and developmental events in all floral whorls. The morphology of the reproductive organs in the first and second whorls of sty fis double mutant flowers indicate that the two genes are part of the mechanism to prevent ectopic expression of the C-function in the perianth of wild-type flowers. This is verified by the detection of the expansion of the expression domain of the class C gene PLENA (PLE) towards the perianth. Interestingly, in the second whorl of sty and fis mutants, spatial differences in stamenoid features and in the pattern of ectopic expression of the PLE gene were observed. This suggests that, with respect to the negative control of PLE, petals are composed of two regions, a lateral and a central one. Mutation in ple is epistatic to most of the sty/fis-related homeotic defects. PLE, however, is not the primary target of STY/FIS control, because dramatic reduction of expression of FIMBRIATA, meristem identity genes (FLORICAULA and SQUAMOSA) and of class B organ identity genes (GLOBOSA) occur before changes in the PLE expression pattern. We propose that STY/FIS are hierarchically high-ranking genes that control cadastral component(s) of the A-function. SQUAMOSA as a potential target of this control is discussed. Retarded growth of second whorl organs, subdivision of third whorl primordia and the failure to initiate them in sty/fis mutants may be mediated by the FIMBRIATA gene.

REFERENCES

Bowman
J. L.
,
Alvarez
J.
,
Weigel
D.
,
Meyerowitz
E.
,
Smyth
D. R.
(
1993
)
Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes.
Development
119
,
721
743
Bradley
D.
,
Carpenter
R.
,
Sommer
H.
,
Hartley
N.
,
Coen
E.
(
1993
)
Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum.
Cell
72
,
85
95
Carpenter
R.
,
Coen
E. S.
(
1990
)
Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus.
Genes Dev
4
,
1483
1493
Carpenter
R.
,
Copsey
L.
,
Vincent
C.
,
Doyle
S.
,
Magrath
R.
,
Coen
E.
(
1995
)
Control of flower development and phyllotaxy by meristem identity genes in Antirrhinum.
Plant Cell
7
,
2001
2011
Coen
E. S.
,
Meyerowitz
E. M.
(
1991
)
The war of the whorls: genetic interactions controlling flower development.
Nature
353
,
31
37
Coen
E. S.
,
Romero
J. M.
,
Doyle
S.
,
Elliott
R.
,
Murphy
G.
,
Carpenter
R.
(
1990
)
floricaula: a homeotic gene required for flower development in Antirrhinum majus.
Cell
63
,
1311
1322
Goodrich
J.
,
Puangsomlee
P.
,
Martin
M.
,
Long
D.
,
Meyerowitz
E. M.
,
Coupland
G.
(
1997
)
A Polycomb-group gene regulates homeotic gene expression in Arabidopsis.
Nature
386
,
44
51
Gustafson-Brown
C.
,
Savidge
B.
,
Yanofsky
M. F.
(
1994
)
Regulation of the Arabidopsis floral homeotic gene APETALA1.
Cell
76
,
131
143
Hantke
S. S.
,
Carpenter
R.
,
Coen
E. S.
(
1995
)
Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems.
Development
121
,
27
35
Haughn
G. W.
,
Schultz
E. A.
,
Martinez-Zapater
J. M.
(
1995
)
The regulation of flowering in Arabidopsis thaliana—meristems, morphogenesis, and mutants.
Can. J. Bot
73
,
959
981
Haughn
G. W.
,
Somerville
C. R.
(
1988
)
Genetic control of morphogenesis in Arabidopsis.
Dev. Genet
9
,
73
89
Huijser
P.
,
Klein
J.
,
Lönnig
W.-E.
,
Meijer
H.
,
Saedler
H.
,
Sommer
H.
(
1992
)
Bractomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus.
EMBO J
11
,
1239
1249
Jack
T.
,
Sieburth
L.
,
Meyerowitz
M.
(
1997
)
Targeted misexpression of AGAMOUS in whorl 2 of Arabidopsis flowers.
Plant J
11
,
825
839
Jofuku
K. D.
,
den Boer
B. G. W.
,
Van Montagu
M.
,
Okamuro
J. K.
(
1994
)
Control of Arabidopsis flower and seed development by the homeotic gene APETALA2.
Plant Cell
6
,
1211
1225
Liu
Z.
,
Meyerowitz
E. M.
(
1995
)
LEUNIG regulates AGAMOUS expression in Arabidopsis flowers.
Development
121
,
975
991
Lönnig
W. E.
,
Saedler
H.
(
1994
)
The homeotic Macho mutant of Antirrhinum majus reverts to wild-type or mutates to the homeotic plena phenotype.
Mol. Gen. Genet
245
,
636
643
Mandel
M. A.
,
Gustafson-Brown
C.
,
Savidge
B.
,
Yanofsky
M. F.
(
1992
)
Molecular characterization of the Arabidopsis floral homeotic gene APETALA1.
Nature
360
,
273
277
Okamuro
J. K.
,
den Boer
B. G. W.
,
Jofuku
K. D.
(
1993
)
Regulation of Arabidopsis flower development.
Plant Cell
5
,
1183
1193
Okamuro
J. K.
,
Szeto
W.
,
Lotys-Prass
C.
,
Jofuku
K. D.
(
1997
)
Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1.
Plant Cell
9
,
37
47
Perbal
M.-C.
,
Haughn
G.
,
Saedler
H.
,
Schwarz-Sommer
Z.
(
1996
)
Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking.
Development
122
,
3433
3441
Samach
A.
,
Kohalmi
S. E.
,
Motte
P.
,
Datla
R.
,
Haughn
G. W.
(
1997
)
Divergence of function and regulation of class B floral organ identity genes.
Plant Cell
9
,
559
570
Scanlon
M. J.
,
Scheeberger
R. G.
,
Freeling
M.
(
1996
)
The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain.
Development
122
,
1683
1691
Schultz
E. A.
,
Haughn
G. W.
(
1993
)
Genetic analysis of the floral initiation process (FLIP) in Arabidopsis.
Development
119
,
745
765
Schwarz-Sommer
Z.
,
Hue
I.
,
Huijser
P.
,
Flor
P. J.
,
Hansen
R.
,
Tetens
F.
,
Lönnig
W.-E.
,
Saedler
H.
,
Sommer
H.
(
1992
)
Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development.
EMBO J
11
,
251
263
Schwarz-Sommer
Z.
,
Huijser
P.
,
Nacken
W.
,
Saedler
H.
,
Sommer
H.
(
1990
)
Genetic control of flower development by homeotic genes in Antirrhinum majus.
Science
250
,
931
936
Simon
R.
,
Carpenter
R.
,
Doyle
S.
,
Coen
E.
(
1994
)
Fimbriata controls flower development by mediating between meristem and organ identity genes.
Cell
78
,
99
107
Sommer
H.
,
Beltran
J. P.
,
Huijser
P.
,
Pape
H.
,
Lönnig
W. E.
,
Saedler
H.
,
Schwarz-Sommer
Z.
(
1990
)
Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinummajus: the protein shows homology to transcription factors.
EMBO J
9
,
605
613
Tröbner
W.
,
Ramirez
L.
,
Motte
P.
,
Hue
I.
,
Huijser
P.
,
Lönnig
W.-E.
,
Saedler
H.
,
Sommer
H.
,
Schwarz-Sommer
Z.
(
1992
)
GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis.
EMBO J
11
,
4693
4704
Tsuchimoto
S.
,
van der Krol
A. R.
,
Chua
N. H.
(
1993
)
Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant.
Plant Cell
5
,
843
853
Weigel
D.
,
Meyerowitz
E. M.
(
1994
)
The ABCs of floral homeotic genes.
Cell
78
,
203
209
Yanofsky
M. F.
,
Ma
H.
,
Bowman
J. L.
,
Drews
G. N.
,
Feldmann
K. A.
,
Meyerowitz
E. M.
(
1990
)
The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors.
Nature
346
,
35
39
Zachgo
S.
,
de Andrade Silva
E.
,
Motte
P.
,
Tröbner
W.
,
Saedler
H.
,
Schwarz-Sommer
Z.
(
1995
)
Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant.
Development
121
,
2861
2875
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