1 Laboratory of Genetics, University of Wisconsin, Madison, WI 53706, USA
2 Department of Biochemistry, University of Wisconsin, Madison, WI 53706,
USA
Author for correspondence (e-mail:
amasino{at}biochem.wisc.edu)
Accepted 13 October 2005
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SUMMARY |
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Key words: Winter annuals, FLOWERING LOCUS C (FLC), FRIGIDA (FRI), Flowering time, CCCH zinc finger
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Introduction |
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One of the first examples of the use of natural variation to explore the
genetic basis of the differences in Arabidopsis life-history traits
was the study of the flowering habit in winter-versus summer-annual
accessions. Napp-Zinn first identified FRIGIDA (FRI), as a
locus that plays a major role in conferring a vernalization requirement upon
certain winter-annual accessions
(Napp-Zinn, 1979). Later
studies indicated that a second locus, FLOWERING LOCUS C
(FLC), is required for FRI to confer the vernalization
requirement (Koornneef et al.,
1994
; Lee et al.,
1994b
). FRI encodes a plant-specific protein
(Johanson et al., 2000
) that
elevates FLC expression to a level that effectively represses
flowering (Michaels and Amasino,
1999
). FLC encodes a MADS-box transcriptional regulator
that is a potent floral repressor, and vernalization promotes flowering by
repressing FLC expression
(Michaels and Amasino, 1999
;
Sheldon et al., 1999
). Many
naturally occurring rapid-cycling accessions have weak or non-functional
alleles of FRI (Gazzani et al.,
2003
; Hagenblad and Nordborg,
2002
; Johanson et al.,
2000
; Le Corre et al.,
2002
; Werner et al.,
2005
) and/or FLC
(Michaels et al., 2003
;
Werner et al., 2005
); without
FRI or FLC activity these accessions no longer require
vernalization for rapid flowering.
FLC inhibits flowering, at least in part, by repressing the
expression of a set of floral promotion genes, including FLOWERING LOCUS
T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1
(SOC1; AGL20 - The Arabidopsis Information Resource)
(Borner et al., 2000;
Kardailsky et al., 1999
;
Kobayashi et al., 1999
;
Lee et al., 2000
;
Samach et al., 2000
).
FT and SOC1 are promoters of flowering, and are often
referred to as floral integrators because their expression is also positively
regulated by other flowering pathways, such as the photoperiod pathway
(Borner et al., 2000
;
Kardailsky et al., 1999
;
Kobayashi et al., 1999
;
Lee et al., 2000
;
Samach et al., 2000
). Thus in
a typical winter-annual life cycle, elevated FLC expression represses
the expression of the floral integrators in the fall season. Exposure to
prolonged cold during the winter represses FLC and alleviates the
repression of the floral integrators, permitting rapid flowering in response
to the lengthening days of the spring.
Genetic screens in rapid-cycling accessions have identified a class of
mutants, known as the autonomous-pathway mutants, that have a late-flowering
phenotype similar to that of FRI-containing winter annuals.
Autonomous-pathway mutants display elevated levels of FLC; therefore,
the autonomous-pathway components are negative regulators of FLC
(Michaels and Amasino, 1999;
Michaels and Amasino, 2001
;
Sheldon et al., 1999
). Lesions
in flc completely suppress the effects of the autonomous-pathway
mutants, suggesting that the products of autonomous-pathway genes affect
flowering solely by the downregulation of FLC
(Michaels and Amasino, 2001
).
FRI activity is epistatic to the autonomous pathway and acts by
promoting FLC expression to levels that are sufficient to block the
floral transition. The delayed flowering and high levels of FLC
observed in FRI-containing lines or in autonomous-pathway mutants are
both eliminated by vernalization (Michaels
and Amasino, 1999
; Sheldon et
al., 1999
).
In many species, the vernalized state is stably maintained throughout cell
divisions in the absence of continued cold exposure
(Lang, 1965); this mitotic
stability is a hallmark of epigenetic regulation. Screens for mutants that are
insensitive to vernalization have revealed aspects of how vernalization occurs
at a molecular level. Such screens have identified genes, such as
VERNALIZATION INSENSITIVE 3 (VIN3) and VERNALIZATION
2 (VRN2), that encode proteins that are likely to be present in
chromatin-remodeling complexes (Sung and
Amasino, 2004
). Vernalization transiently induces the expression
of VIN3, which facilitates histone modifications at the FLC
locus, resulting in a silent chromatin state
(Bastow et al., 2004
;
Sung and Amasino, 2004
). This
repression is maintained throughout the remainder of the life cycle after
vernalization by the involvement of VERNALIZATION 1 (VRN1), a DNA-binding
protein, and VRN2, a homolog of the Drosophila Suppressor of Zeste
12, which is part of the Enhancer of Zeste transcriptional repressor complex
(Gendall et al., 2001
;
Levy et al., 2002
).
Two classes of gene have recently been identified that are required for the
elevated expression of FLC and that are therefore necessary to
establish the vernalization-requiring, winter-annual habit in
Arabidopsis. One class is required in all situations in which
FLC expression is elevated (i.e. in both FRI-containing
lines and in autonomous-pathway mutants); the other class, which is a subset
of the first class, is required for FRI to elevate FLC
expression, but not for elevated FLC expression in autonomous-pathway
mutants. Many loci of the first class are components of the Arabidopsis
PAF1 transcriptional activator complex
(He et al., 2004;
Oh et al., 2004
;
Zhang and van Nocker, 2002
).
This complex is required for the methylation of lysine 4 on histone 3 in
FLC chromatin (He et al.,
2004
), a modification associated with an active chromatin state.
Mutations in members of this complex also affect the expression of other
members of the FLC clade, such as FLOWERING LOCUS M and
MADS AFFECTING FLOWERING 2, and, as a result, such mutations cause
early flowering in short days (He et al.,
2004
; Oh et al.,
2004
). A member of the second class, FRIGIDA-LIKE 1
(FRL1), is necessary for the promotion of FLC expression in
a FRI-dependent manner; i.e. frl1 mutations are unable to
suppress mutants in the autonomous or the photoperiod pathways, indicating
that FRL1 might act specifically with FRI to promote
FLC expression (Michaels et al.,
2004
).
Here, we report the identification of a gene, FRIGIDA-ESSENTIAL 1 (FES1), that, like FRL1, is required for the upregulation of FLC in the presence of FRI, and hence is necessary for conferring the winter-annual habit in Arabidopsis. FES1 encodes a protein with a CCCH zinc finger, and promotes the expression of FLC in a FRI-dependent manner. Epistasis analysis between FES1, FRL1 and FRI indicate that these genes do not function in a linear pathway, but instead act cooperatively to promote the expression of FLC.
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Materials and methods |
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Growth conditions
Plants were grown under long days (16 hours light/8 hours dark) or short
days (8 hours light/16 hours dark) at 22°C under cool-white fluorescent
lights. For experiments involving vernalization, seeds were plated on
agar-solidified medium containing 0.65 g/liter Peters Excel 15-5-15 fertilizer
(Grace Sierra, Milpitas, CA), and were kept at room temperature overnight to
allow seeds to become metabolically active before being transferred to 2°C
for 40 days. During cold treatment, samples were kept under short-day
conditions (8 hours light/16 hours dark).
T-DNA flanking-sequence analysis
The sequence flanking the T-DNA of fes1-1 and fes1-2 was
obtained by thermal asymmetric interlaced PCR
(Liu et al., 1995), the
details of which are described elsewhere
(Schomburg et al., 2003
).
T-DNA borders were defined by sequencing PCR products obtained using a T-DNA
border primer and a gene-specific primer. The T-DNA border primers used for
each T-DNA insertion population are described on the Arabidopsis Knockout
Facility web site (see
http://www.biotech.wisc.edu/Arabidopsis/Index2.asp).
Histochemical ß-glucuronidase assays and overexpression analyses
The FES1 ß-glucuronidase fusion construct was
generated by PCR amplification of the 2.8 kb genomic region plus 600 bp of the
promoter region of FES1, using FES-PGF
(5'-CACCATGGCGAAATTGCGGAGGATTCTTAGGGTTTA-3') and FES-PGR
(5'-TTACCATACTTTTCGACATACCCCTGCA-3') as primers. The FES1
35S Cauliflower Mosaic Virus construct was generated by PCR amplification of a
2.8 kb section of the FES1 genomic region beginning at the start
codon, using FES-OXF (5'-CACCATGTCTGATTCCGACATGGACATTGA-3') and
FES-OXR (5'-AGTGACATTTGGTTTGATAACTCAGGGTTTACCA-3') as primers. The
resulting PCR product was subcloned into D-TOPO (Invitrogen Life
Technologies). Gateway Technologies were used to generate FES1::GUS
in pMDC163 and 35S::FES1 in pMDC32
(Curtis and Grossniklaus,
2003). Arabidopsis (ecotype Col) plants were transformed
with the Agrobacterium tumefaciens strain LBA4404 by infiltration
(Clough and Bent, 1998
).
Transgenic lines were selected on agar-solidified medium containing 0.65 g/l
Peter's Excel 15-5-15 fertilizer and 25 µg/ml Hygromycin. Staining for
ß-glucuronidase activity was performed as described previously
(Schomburg et al., 2001
).
|
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Results |
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The ability of lesions in FES1 to suppress FRI-mediated
late flowering suggested that FES1 is required for FLC
expression. A number of genes, in addition to FRI, have been
identified as being required for FLC expression
(Bezerra et al., 2004;
Doyle et al., 2005
;
He et al., 2004
;
Michaels et al., 2004
;
Noh et al., 2004a
;
Noh and Amasino, 2003
;
Noh et al., 2004b
;
Oh et al., 2004
;
Zhang and van Nocker, 2002
).
Some of these loci are specifically involved in FLC expression,
whereas others affect the expression of additional members of the FLC
clade, such as FLOWERING LOCUS M (FLM; MAF1 - The
Arabidopsis Information Resource) and MADS AFFECTING FLOWERING 2
(MAF2) (Doyle et al.,
2005
; He et al.,
2004
; Oh et al.,
2004
). Mutants in which the expression of the entire FLC
clade is affected flower early in non-inductive photoperiods, mainly as a
result of the decreased expression of FLM
(He et al., 2004
;
Oh et al., 2004
;
Ratcliffe et al., 2001
;
Scortecci et al., 2001
) and
perhaps MAF2, whereas loss of only FLC expression does not
have a large effect on flowering in the short-day conditions that we used
(Michaels and Amasino, 1999
).
Therefore, fes1-1 and fes1-2 mutants were grown in short
days to assess whether or not the fes1 lesion might affect expression
of the FLC clade. fes1 alleles grown in short days flowered
similarly to, but not earlier than, Columbia and a loss-of-function
flc allele, flc-3 (Fig.
1B). These data indicate that FES1 does not affect the
entire FLC clade, but more likely specifically affects the expression
of FLC.
To evaluate the level at which fes1 caused an early-flowering phenotype in Col FRI, expression studies of FRI and FLC were performed. In fes1 mutants, there is no detectable difference in the expression of FRI, but there is a significant reduction in the expression of FLC when compared with the Col FRI parental line (Fig. 1C). As expected from the fes1 short day phenotype, there was no change in FLM expression (data not shown). Therefore FES1 is necessary for the FRI-mediated increase of FLC mRNA levels. In addition, FES1 is not regulated by FRI (Fig. 1C).
fes1 mutations are unable to suppress the late flowering of autonomous- or photoperiod-pathway mutants
Mutations in autonomous-pathway genes delay flowering in non-vernalized
plants owing to the increased expression of FLC, and, as is the case
with FRI-containing lines, exposure to vernalization promotes rapid
flowering by suppressing FLC expression
(Michaels and Amasino, 2001).
Therefore, the autonomous-pathway mutants act similarly to Col FRI in
that they require vernalization treatment to flower rapidly. Double-mutant
analyses with autonomous-pathway mutants and fes1 were performed to
determine whether FES1 is specifically required for
FRI-mediated late flowering, or whether FES1 plays a more
general role in FLC upregulation. fes1-4 was unable to
suppress the late flowering of autonomous-pathway mutants fld-3 and
fca-9, and only slightly suppressed another autonomous-pathway mutant
ld-1. Nor was fes1-4 able to suppress the late flowering of
gigantea, a photoperiod mutant
(Fig. 2A). Furthermore, the
inability of fes1 to suppress the late flowering of
autonomous-pathway mutants is due to a failure to reduce the level of
FLC mRNA (Fig. 2B).
These data indicate that FES1 is part of a pathway, involving
FRI, that elevates FLC expression
(Fig. 2C).
|
|
A BLAST search with the FES1 protein-coding region failed to
identify any proteins with extensive sequence identity in
Arabidopsis, although a sequence was identified from poplar that
encodes a protein containing a CCCH zinc finger and that shares 30%
identity with the carboxy-terminal of FES1. FES1 does share
60%
sequence identity in an
20 amino-acid CCCH zinc finger with other CCCH
zinc fingers in Arabidopsis (Fig.
3), but the similarity only extends approximately 50 amino acids
N- and C-terminal of the CCCH zinc finger.
FES1 genetically interacts with FRI and FRL1
Three genes, FRI, FRL1 and FES1, are required
specifically for the upregulation of FLC that is characteristic of
the winter-annual habit in Arabidopsis
(Johanson et al., 2000;
Michaels et al., 2004
). Double
mutants were isolated to determine whether FRI and FES1 are
involved in the same flowering pathway, as was shown with FRI and
FRL1 (Michaels et al.,
2004
). Double mutants displayed phenotypes identical to the single
mutants (Fig. 4A). The failure
to observe an additive phenotype between these mutants suggests that they have
non-redundant roles in delaying the floral transition and are likely to act in
the same genetic pathway.
|
|
Vernalization occurs downstream of FES1
Vernalization promotes rapid flowering of winter-annual
Arabidopsis by silencing the floral repressor FLC
(Michaels and Amasino, 1999;
Sheldon et al., 1999
). Lines
that express FLC from a constitutive promoter are not responsive to
vernalization (Michaels and Amasino,
1999
; Sheldon et al.,
1999
). Lines in which 35S::FES1 rescued the fes1
lesion are fully responsive to vernalization
(Fig. 5A). Furthermore,
FES1 mRNA levels are not affected by vernalization. Thus,
vernalization acts downstream of FES1
(Fig. 5B). This is not
surprising considering that autonomous-pathway mutants are vernalization
responsive, and that mutations in fri, frl1 and fes1 are
unable to suppress mutants in the autonomous pathway.
FES1 is expressed in the shoot/root apex and the vascular system
FLC is expressed in the apex of the shoot/root and in the vascular
tissue (Michaels and Amasino,
2000). Translational fusions to ß-glucuronidase
(GUS) were used to evaluate the relationship of the FES1 and
FLC expression pattern. The FES1::GUS translational fusion
comprised the entire genomic sequence (minus the stop codon and the 3'
untranslated region) plus 600 bp upstream of the start codon. The FLC::GUS
construct has been described previously
(Michaels et al., 2005
). The
FES1::GUS translational fusion was functional; transformants were
identified for GUS analysis in which the transgene rescued the early-flowering
behavior of the fes1-2 lesion. FES1::GUS activity was
detected most strongly in the shoot and root apex, as well as in the vascular
system (Fig. 6A,B). This
expression pattern is similar to the expression pattern of FLC::GUS
(Fig. 6C). In addition,
FES1::GUS was localized to the nucleus
(Fig. 6D).
|
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Discussion |
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It is interesting that there are mutations that repress FLC
expression in both FRI and autonomous-pathway mutants, and other
mutations, like fes1, that suppress FRI, but not
autonomous-pathway mutants. FRL1 is another example of a gene that is
specifically required for FLC activity in a FRI background
but is not required for FLC expression in autonomous-pathway mutants
(Michaels et al., 2004). Thus,
FRL1 and FES1 comprise a class of gene that is highly
FRI specific for the upregulation of FLC expression. In
addition, lesions in ABH1, the large subunit of the mRNA cap-binding
protein, strongly suppress the FRI-mediated promotion of
FLC, like fes1 and frl1, but cause a weak
suppression of certain autonomous-pathway mutants
(Bezerra et al., 2004
). In
other words, the abh1 mutation exhibits a degree of FRI
specificity, but does not affect the FRI pathway as specifically as
fes1 and frl1 do.
Autonomous-pathway mutants are late flowering as a result of the elevated expression of FLC, but the natural route to elevated FLC expression and the associated delay of flowering characteristic of winter-annual Arabidopsis is most often due to the presence of FRI. How FRI, FRL1 and FES1 increase FLC expression at a biochemical level is not known. Genetic analyses using both recessive and dominant alleles of FRI, FRL1 and FES1 revealed that they do not appear to act in a linear pathway to promote FLC expression; rather, FRI, FRL1 and FES1 appear to act in parallel, perhaps in a common protein complex. However, we found no evidence for an interaction between FRI and FES1, or FRL1 and FES1, by yeast two-hybrid analysis.
FES1 encodes a protein with a CCCH zinc finger. This class of zinc
fingers is typically found in proteins that bind to RNA, and such proteins can
participate in mRNA production or degradation. For example, in the mouse,
tristetraprolin (TTP; ZFP36 - Mouse Genome Informatics), a protein containing
two CCCH zinc fingers, binds directly to AU-rich elements within the 3'
untranslated region of target transcripts to facilitate mRNA degradation
(Carballo et al., 1998). The
Arabidopsis HUA1 protein contains six CCCH zinc fingers and is
thought to participate in the pre-mRNA processing of target RNAs
(Cheng et al., 2003
). If FES1
binds to FLC RNA, the phenotype of fes1 mutants is
consistent with FES1 stabilizing or facilitating the processing of
FLC mRNA.
Studies of natural variation in flowering time have revealed that lesions
that reduce or eliminate FRI activity have arisen independently
several times, and that allelic variation in the FRI gene accounts
for most of the natural variation in flowering time
(Gazzani et al., 2003;
Hagenblad and Nordborg, 2002
;
Johanson et al., 2000
;
Le Corre et al., 2002
;
Shindo et al., 2005
;
Werner et al., 2005
).
Mutations in FES1 or FRL1 appear to specifically affect
flowering in cooperation with FRI, and the phenotype caused by these
mutations appears to be identical to that caused by fri
loss-of-function mutations. Thus, FES1 and FRL1 could, in
principle, be targets for natural variation. Recently Werner et al. identified
several early-flowering accessions that appear to contain functional
FRI and FLC alleles
(Werner et al., 2005
).
However, sequence analysis of FES1 in these accessions did not reveal
any obvious changes that may account for the early-flowering phenotype.
Perhaps, fes1 and frl1 lesions have deleterious affects that
have not yet been recognized. Alternatively, there may be undiscovered
examples of allelic variation in FES1 and FRL1 that account
for the natural variation in flowering time.
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ACKNOWLEDGMENTS |
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Footnotes |
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