|
Plant Physiol. (1998) 116: 503-509
Anion Channels and the Stimulation of Anthocyanin Accumulation by
Blue Light in Arabidopsis Seedlings1
Bosl Noh and
Edgar P. Spalding*
Department of Botany, University of Wisconsin, 430 Lincoln Drive,
Madison, Wisconsin 53706
 |
ABSTRACT |
Activation of anion channels by blue
light begins within seconds of irradiation in seedlings and is related
to the ensuing growth inhibition.
5-Nitro-2-(3-phenylpropylamino)-benzoic acid (NPPB) is a potent,
selective, and reversible blocker of these anion channels in
Arabidopsis thaliana. Here we show that 20 µm NPPB blocked 72% of the blue-light-induced
accumulation of anthocyanin pigments in seedlings. Feeding biosynthetic
intermediates to wild-type and tt5 seedlings provided
evidence that NPPB prevented blue light from up-regulating one or more
steps between and including phenylalanine ammonia lyase and chalcone
isomerase. NPPB was found to have no significant effect on the
blue-light-induced increase in transcript levels of
PAL1, CHS, CHI, or
DFR, which are genes that encode anthocyanin-biosynthetic enzymes. Immunoblots revealed that NPPB also
did not inhibit the accumulation of the chalcone synthase, chalcone
isomerase, or flavanone-3-hydroxylase proteins. This is in contrast to
the reduced anthocyanin accumulation displayed by a mutant lacking the
HY4 blue-light receptor, as hy4 displayed reduced
expression of the above enzymes. Taken together, the data indicate that
blue light acting through HY4 leads to an increase in the amount of
biosynthetic enzymes, but blue light must also act through a separate,
anion-channel-dependent system to create a fully functional
biosynthetic pathway.
| |
INTRODUCTION |
Anthocyanin pigments accumulate in response to light in the
seedlings of many species. This accumulation is preceded by increased transcription of genes encoding enzymes in the anthocyanin-biosynthetic pathway, which is shown in Figure 1. A
view that has emerged from various photobiological, biochemical, and
genetic studies is that transcriptional control of the biosynthetic
enzymes accounts for the effects of light on anthocyanin accumulation
(Mol et al., 1996 ). Even when the inductive treatment is something
other than light, such as a pathogen-related elicitor or a nutrient
deficiency, transcriptional control of these genes has satisfactorily
explained the resulting anthocyanin accumulation (Chappel and
Hahlbrock, 1984; Dangl, 1991; Dixon and Pavia, 1995).
View larger version (10K):
[in this window]
[in a new window]
| Figure 1.
The anthocyanin biosynthetic pathway. The chemical
intermediates and the gene symbols for several of the cloned
biosynthetic enzymes are shown.
|
|
In seedlings of species such as mustard and tomato, phytochrome is the
important photoreceptor controlling the accumulation of anthocyanins (Lange et al., 1970; Batschauer et al., 1991; Frohnmeyer et al., 1992; Neuhaus et al., 1993). However, phytochrome is
much less important to the accumulation of anthocyanins in Arabidopsis
seedlings. Instead, one or more photoreceptors specific for blue light
is largely responsible for the gene activation and pigment accumulation
induced by visible wavelengths (Feinbaum et al., 1991; Kubasek et al.,
1992; Batschauer et al., 1996). It is clear that the flavoprotein
photoreceptor encoded by the HY4 gene (Ahmad and Cashmore,
1993) functions importantly in the response to blue light (Ahmad et
al., 1995; Jackson and Jenkins, 1995). In parsley and Arabidopsis
radiation in the UVA and UVB wavelength bands is also very effective
(Bruns et al., 1986; Ohl et al., 1989; Kubasek et al., 1992; Christie
and Jenkins, 1996), operating synergistically with blue light through
separate receptors (Fuglevand et al., 1996).
In the case of phytochrome-mediated anthocyanin accumulation,
information about how the photoreceptor is coupled to the increase in
transcription is beginning to emerge: a role for cGMP has been supported by the results of microinjection studies performed with a
phytochrome-deficient mutant of tomato (Neuhaus et al., 1993). As for
the blue light and UV receptor(s) responsible for anthocyanin accumulation in Arabidopsis, the effects of pharmacological agents indicated that an increase in cytoplasmic Ca2+ is
somehow involved in, although not sufficient to cause, the light-induced increase in CHS mRNA in suspension-cultured cells (Christie and Jenkins, 1996). Also, the effects of kinase and phosphatase inhibitors indicate a role for phosphorylation in the
signal cascade (Christie and Jenkins, 1996). Unfortunately, the role
proposed for Ca2+ does not agree with the recent
finding that blue light does not induce detectable changes in
cytoplasmic Ca2+ in aequorin-expressing
Arabidopsis seedlings (Lewis et al., 1997). Perhaps the response
mechanism of suspension-cultured cells differs from that of etiolated
seedlings, or the requirement for Ca2+ is
satisfied by small increases in its concentration that could not be
detected by measuring aequorin luminescence.
The rapid inhibition of hypocotyl elongation in
etiolated seedlings is a blue-light response that, until the
present work, was not obviously related to anthocyanin
accumulation. The growth inhibition begins after a lag time of
approximately 30 s, depending on the fluence rate of blue light
and the species used. Preceding the onset of rapid growth inhibition by
a few seconds is the activation of anion channels at the plasma
membrane of growing cells (Cho and Spalding, 1996). The channel
activation increases the conductance of the membrane to anions such as
Cl , facilitating a passive flux of anions down
their gradient in electrochemical potential, i.e. out of the cell. The
electric current produced by this flux shifts the membrane potential to more positive values. Thus, a depolarization of the membrane quickly precedes the onset of growth inhibition induced by blue light (Spalding
and Cosgrove, 1989).
An anion-channel blocker known as NPPB potently,
selectively, and reversibly blocks the blue-light-activated anion
channel of Arabidopsis, as well as the blue-light-induced membrane
depolarization in intact seedlings (Cho and Spalding, 1996; Lewis et
al., 1997). Consistent with this channel activation being a
signal-transducing event, treatment of seedlings with NPPB renders
hypocotyl growth less sensitive to blue light (Cho and Spalding, 1996).
HY4 is not the photoreceptor mediating the rapid growth inhibition, as a normal response was observed in a null hy4 mutant
(B.M. Parks and E.P. Spalding, unpublished observations).
Superimposed on the rapid inhibition of hypocotyl growth by blue light
is an inhibition that begins after 8 h of blue light. Unlike the
rapid response, this persistent long-term inhibition is mediated by the
HY4 photoreceptor (B.M. Parks and E.P. Spalding, unpublished
observations). The emerging picture is that two genetically separable,
blue-light-specific photosensory systems control hypocotyl elongation
in Arabidopsis. At least one includes anion-channel activation as an
important component. The present results indicate that elements of the
photosensory systems controlling hypocotyl growth are important to the
blue-light-induced accumulation of anthocyanins in Arabidopsis
seedlings.
| |
MATERIALS AND METHODS |
Plant Growth and Medium Composition
Seeds of Arabidopsis thaliana (ecotype Landsberg) were
sown on 0.8% agar containing 1 mm
CaCl2 and 1 mm KCl. The plates were placed in darkness at 4°C for 2 d and then irradiated with red light (2 µmol m2 s1)
for 0.5 h at room temperature. For some experiments, the plates also contained 1% Suc. In the naringenin-feeding experiments, tt5 mutants (Shirley et al., 1992, 1995) were grown on 0.8%
agar, 0.5 Murashige-Skoog salts, and 1% Suc.
When used, NPPB (Calbiochem) dissolved in DMSO, Phe (dissolved in 50%
ethanol; Sigma), and naringenin (dissolved in 50% ethanol; Sigma) were
added to the medium after autoclaving. The final concentration of NPPB
used depended on the experiment, but the concentration of naringenin
and Phe used was 100 µm. Control experiments confirmed that none of the solvents at the concentrations present in the final
growth medium, which did not exceed 0.16%, affected anthocyanin accumulation or seedling growth. Seedlings were grown under blue light
(65 µmol m2 s1, 94%
of which was between 400 and 500 nm) produced by two bulbs (F20T12/BB,
Phillips Lighting, Somerset, NJ) for 4 d following the cold
treatment except when used for RNA blots, in which case they were grown
in complete darkness for 3 d and moved to blue light for the
various indicated periods. Irradiating agar plates containing NPPB for
4 d with blue light did not diminish the effects of the drug on
seedlings subsequently grown on them, indicating that NPPB is stable in
blue light.
Anthocyanin Extraction and Quantification
Seedlings were harvested from the agar plates, quickly weighed,
and placed into microcentrifuge tubes containing 350 µL of 18%
1-propanol, 1% HCl, and 81% water. The tubes were placed in boiling
water for 3 min (Lange et al., 1970) and then incubated in darkness for
at least 2 h at room temperature. After a brief centrifugation to
pellet the tissue, 250 µL of the solution was removed and brought to
a final volume of 550 µL by adding solvent. The amount of
anthocyanins in the resulting extract was quantified spectrophotometrically. The values are reported as
A535  2(A650) g1 fresh weight (Lange et al., 1970).
RNA Extraction and Blot Analysis
Seedlings grown in complete darkness for 3 d were treated
with blue light for 0, 24, or 72 h before being frozen in liquid nitrogen. Total RNA was isolated from frozen seedlings by using a total
RNA kit (RNeasy, Qiagen, Chatsworth, CA). RNA was loaded onto a
denaturing agarose gel, electrophoresed, transferred to a nylon
membrane (Micron Separations, Westboro, MA), and hybridized with
radioactive, random-primed DNA probes prepared using the cDNA of the
indicated genes as a template. The cDNAs were obtained from Dr.
Frederick Ausubel (CHS; Feinbaum and Ausbel, 1988), Dr. Brenda Shirley (CHI and DFR; Shirley et al.,
1992), and Dr. Keith Davis (PAL1 gene-specific probe; Wanner
et al., 1995). To standardize the signal in each lane, a DNA probe
complementary to rRNA (Delseny et al., 1983) was also hybridized to the
membrane. Hybridization signals from each probe were quantified with a
phosphor imager (Molecular Dynamics, Sunnyvale, CA), and the amount of
mRNA relative to rRNA was determined for each gene.
Protein Extraction and Immunodetection
Seedlings grown for 4 d in blue light on agar medium
containing 1% Suc, 1 mm CaCl2, and 1 mm KCl were harvested, frozen in liquid nitrogen, ground in
1× SDS sample buffer, and boiled for 15 min. Protein samples were
quantified by a protein assay kit (Bio-Rad), and separated on 10%
SDS-polyacrylamide gel before blotting to a nitrocellulose filter
(Bio-Rad). Equal loading was verified by staining a blot with Ponceau S
(Sigma). Blots were probed with polyclonal antibodies raised against
CHS (Burbulis et al., 1996), CHI, and F3H that were obtained from Dr.
Brenda Shirley (Virginia Polytechnic Institute, Blacksburg) and then with peroxidase-conjugated rabbit anti-chicken IgY (Jackson
ImmunoResearch Labs, West Grove, PA). The chemiluminescence produced by
the secondary antibody (enhanced chemiluminescence, Amersham) was
detected by radiographic film.
| |
RESULTS AND DISCUSSION |
Anion-Channel Blocker Inhibits Anthocyanin Accumulation Induced by
Blue Light
The starting point for the present work was the observation that
NPPB, a pharmacological blocker of the blue-light-activated anion
channel in Arabidopsis (Cho and Spalding, 1996), inhibited the
accumulation of anthocyanins by seedlings grown in blue light. Figure
2A shows that the anthocyanin content of
blue-light-grown seedlings was reduced by 72% when 20 µm
NPPB was included in the agar growth medium. Approximately 4 µm NPPB produced half-maximal inhibition (Fig. 2B). The
straightforward interpretation of this result is that NPPB blocked the
anion channel, preventing transduction of the blue-light stimulus
beyond the channel-activation stage.
View larger version (15K):
[in this window]
[in a new window]
| Figure 2.
The inhibition of anthocyanin accumulation by
NPPB. A, Wild-type seedlings grown in blue light on agar containing the
indicated concentrations of NPPB (means ± se;
n = 3-5). B, Comparison of the inhibitory effects
of NPPB on blue-light-induced anthocyanin accumulation and membrane
depolarization. The data in A and previously published data on the
blue-light-induced membrane depolarization were normalized to the
control value (0 µm NPPB) and plotted against NPPB
concentration. The dashed line indicates the concentration of NPPB that
produced half-maximal inhibition. abs., Absorbance; F.W., fresh
weight.
|
|
However, NPPB may have inhibited anthocyanin accumulation by affecting
some unrelated component of the response. A comparison of the
inhibitory effects of NPPB on blue-light-induced anthocyanin accumulation and anion-channel activation would address this
potentially misleading alternative. If the concentrations of NPPB
required to block the membrane depolarization and anthocyanin
accumulation differed significantly, a causal relationship between the
two would be doubtful. Normalizing the data in Figure 2A relative to
the control value (0 NPPB) and plotting them against NPPB concentration (Fig. 2B), along with similarly normalized depolarization data obtained
by Cho and Spalding (1996) revealed that the two responses were very
similarly sensitive to the drug. The close agreement of the two curves
in Figure 2B, particularly the essentially identical values for the
half-maximal-inhibition concentration, is consistent with the target of
the drug being the anion channel in both cases; blocking the anion
channel appears to prevent blue light from inducing the accumulation of
anthocyanins.
Anion Channels Influence the Anthocyanin Pathway between Phe and
Naringenin
The tt5 mutant of Arabidopsis lacks detectable CHI
protein (Fig. 1) and is unable to produce anthocyanins unless supplied with the intermediate naringenin (Shirley et al., 1992, 1995). We
verified that tt5 seedlings grown in the absence of
naringenin did not accumulate detectable levels of anthocyanins in our
blue-light conditions, but when supplied with 100 µm
naringenin, anthocyanins accumulated to greater than wild-type levels
(Fig. 3). NPPB (20 µm) did
not reduce the levels of anthocyanins in tt5 seedlings fed
naringenin (Fig. 3). This result is evidence that neither the
conversion of naringenin into anthocyanins nor the vacuolar accumulation of anthocyanins is impaired in NPPB-treated seedlings. Instead, NPPB appears to affect one or more of the steps that lead to
the production of naringenin.
View larger version (33K):
[in this window]
[in a new window]
| Figure 3.
Identification of the biosynthetic step(s)
affected by NPPB. NPPB inhibited anthocyanin accumulation in wild-type
seedlings fed Phe to the same degree as controls, indicating that one
or more steps downstream of PAL was affected. NPPB did not inhibit naringenin-dependent anthocyanin accumulation in tt5
seedlings, indicating that steps downstream of CHI were not affected by
NPPB. The results displayed are averages ± se;
n = 4. abs., Absorbance; F.W., fresh weight.
|
|
The three genes in Arabidopsis that encode PAL provide a point for
carbon to enter the anthocyanin biosynthetic pathway (Fig. 1).
Unfortunately, no mutants lacking PAL activity are known, so narrowing
down the site of NPPB action with an experiment directly analogous to
the tt5 experiment was not possible. However, we observed
that wild-type seedlings supplied with exogenous Phe accumulated
anthocyanins above the control levels, presumably because more
substrate was present at the head of the pathway. Contrary to the
naringenin-feeding experiment, NPPB blocked anthocyanin accumulation by
Phe-fed seedlings with typical effectiveness (Fig. 3). This result
would seem to rule out the possibility that NPPB inhibited anthocyanin
accumulation (Figs. 2 and 3) by slowing the production of Phe or by
shunting it into a competing pathway, such as the protein-synthesis
pathway. Instead, the results shown in Figure 3 may be taken as
evidence that the up-regulation by blue light of one or more steps
between and including PAL and CHI was inhibited by NPPB. We observed
variable results when seedlings were fed the intermediates cinnamate or
4-coumarate in analogous experiments, so we cannot safely pinpoint the
NPPB-affected site(s) at present.
CHS, often referred to as the key enzyme in the pathway, catalyzes the
first committed step in anthocyanin biosynthesis (Martin, 1993). Its
place in the pathway is immediately upstream of CHI (Fig. 1). Although
it is not known whether CHS (or any other enzyme in the pathway) is
truly rate limiting (Martin, 1993), its expression is strongly induced
by blue light (Feinbaum et al., 1991; Kubasek et al., 1992; Ahmad et
al., 1995; Jackson and Jenkins, 1995; Batschauer et al., 1996), and
many studies have shown its expression to be well correlated with
anthocyanin levels regardless of the inducing agent (Chappell and
Halbrock, 1984; Weiss et al., 1990; Deikman and Hammer, 1995; Tamari et
al., 1995). We hypothesized that the blue-light induction of
CHS and/or other genes in the pathway depends upon
anion-channel activation. If true, this would provide a
transcription-based explanation for the inhibition of anthocyanin accumulation by NPPB, and place the anion channel in a signaling pathway that reaches the nucleus to affect gene expression.
Effect of NPPB on the Expression of
Anthocyanin-Biosynthetic Genes
The mRNA levels of genes encoding four enzymes of the biosynthetic
pathway were measured in seedlings grown in the presence or absence of
NPPB. The RNA blots in Figure 4
demonstrate that blue light increased the amount of mRNA encoding PAL1,
CHS, CHI, and DFR. In particular, after 72 h of growth in blue
light, CHS mRNA was increased approximately 18-fold over that of
seedlings grown for the same length of time in complete darkness. This
increase is consistent with the findings of others (Feinbaum et al.,
1991; Kubasek et al., 1992). The blue-light-induced increase in these same mRNAs was only slightly different in seedlings grown in the presence of 20 µm NPPB. We obtained no evidence that NPPB
reduced the transcript levels for the measured genes to an extent that approached its inhibitory influence on anthocyanin accumulation. In the
case of CHS mRNA, 72 h of blue light induced an 11-fold increase
in NPPB-treated seedlings (Fig. 4). In an experiment that used 1.5-h
blue-light treatments, the same pattern of transcript levels was
observed, although the absolute levels were lower (data not shown).
View larger version (49K):
[in this window]
[in a new window]
| Figure 4.
The effect of NPPB on the blue-light-induced
increase in PAL, CHS, CHI, and DFR mRNA. RNA was isolated from
seedlings harvested after the indicated period of growth in blue light
(BL). Results similar to those displayed were obtained in an
independent, duplicate experiment. max., Maximum.
|
|
It seems improbable that the modest reductions in mRNA levels resulting
from treatment with NPPB were responsible for a significant component
of the drug's large inhibitory effect on anthocyanin accumulation,
unless the slightly reduced mRNA levels somehow translated into
substantially less protein. The effect of NPPB on the protein levels of
three of the biosynthetic enzymes was determined by immunoblot assays.
Figure 5 demonstrates that whether or not the seedlings were treated with 20 µm NPPB,
they expressed similar amounts of CHS, CHI, and F3H. However, it is
not possible to directly compare the RNA (Fig. 4) and protein (Fig. 5)
analyses, because to obtain immunoblot signals well above background,
it was necessary to include Suc in the growth medium.
View larger version (68K):
[in this window]
[in a new window]
| Figure 5.
Immunoblot analysis of the effect of NPPB on the
levels of CHS, CHI, and F3H protein in blue-light-grown seedlings.
Consistent with the RNA blots shown in Figure 4, NPPB had no detectable
effect on the above protein levels. However, lower levels could be
detected in hy4 seedlings. All seedlings were grown in
the presence of Suc.
|
|
Because correlations between Suc, CHS expression, and
anthocyanins have been documented (Tsukaya et al., 1991), we could not safely interpret the ineffectiveness of NPPB on the protein level (Fig.
5) until we had determined that NPPB also inhibited anthocyanin accumulation in the presence of Suc. Figure
6 shows that Suc greatly stimulated
anthocyanin accumulation, and that 20 µm NPPB inhibited this accumulation to the same relative extent as in the absence of Suc.
Thus, Figures 5 and 6 together demonstrate that NPPB inhibited the
blue-light-induced accumulation of anthocyanins without affecting the
amount of CHS, CHI, or F3H protein.
View larger version (36K):
[in this window]
[in a new window]
| Figure 6.
The effect of NPPB and Suc on the accumulation of
anthocyanins by wild-type and hy4 seedlings grown in
blue light. For these experiments, wild type grown in the presence of
Suc is the control group to which the other treatments are compared.
The results displayed are means ± se;
n = 2.
|
|
When grown in blue light, hy4 displays significantly reduced
CHS transcript and anthocyanin levels compared with the wild type (Ahmad et al., 1995; Jackson and Jenkins, 1995; Fuglevand et al.,
1996; Ahmad and Cashmore, 1997). We found that the allele of
hy4 originally isolated by Koornneef et al. (1980) and
considered to be a null (Ahmad and Cashmore, 1997) also accumulated
anthocyanins when grown in the presence of Suc, although less than
one-half that of wild-type seedlings (Fig. 6). This decreased
anthocyanin level is consistent with the lower CHS, CHI, and F3H
protein levels detected in identically grown hy4 seedlings
(Fig. 5), and the lower CHS mRNA reported in other studies
mentioned above. NPPB further reduced the amount of anthocyanins
accumulated by hy4 seedlings to a level below that of
wild-type seedlings, indicating that the inhibitory effects of the drug
and the mutation are additive.
| |
CONCLUSIONS |
It appears that blocking the anion channel with NPPB prevents the
accumulation of anthocyanins without impairing the mechanism responsible for activating the biosynthetic genes we tested or translating their mRNAs. The portion of the biosynthetic pathway that appears to be rate limiting in plants treated with NPPB is that
between and including PAL and CHI. An inference that may be drawn from
these results is that induction of the biosynthetic genes and increases
in the encoded proteins are not sufficient for the accumulation of
anthocyanins in response to blue light. Somehow, blue light acting
through anion channels at the plasma membrane may posttranslationally
modify the activity of these biosynthetic enzymes. Perhaps activation
of the anion channels by blue light results in a direct covalent
modification, such as phosphorylation, of the enzymes to increase their
specific activity. Alternatively, a modification of the cytoplasm
resulting from anion-channel activation, such as a change in pH, may be important for biosynthetic activity.
The inhibitory effect of the hy4 mutation differs from that
of NPPB in that it can be explained by a decrease in the transcript level of biosynthetic genes such as CHS (Ahmad et al., 1995;
Jackson and Jenkins, 1995). Also, the two inhibitory effects are
additive (Fig. 6). The present data led us to propose that blue light
acting through the HY4 photoreceptor increases transcription of the
biosynthetic genes, whereas blue light acting through the
anion-channel-dependent pathway leads to an increase in the specific
activity of one or more enzymes upstream of CHI. Only if both
mechanisms are functional will seedlings accumulate normal levels of
anthocyanins upon exposure to blue light.
| |
FOOTNOTES |
1
This work was supported by the National
Aeronautics and Space Administration/National Science Foundation
Network for Research on Plant Sensory Systems (grant no. IBN-9416016 to
E.P.S.) and by the Department of Energy/National Science
Foundation/U.S. Department of Agriculture Collaborative Program on
Research in Plant Biology (grant no. BIR 92-20331 to the University of
Wisconsin).
*
Corresponding author; e-mail spalding{at}facstaff.wisc.edu; fax
1-608-262-7509.
Received August 1, 1997;
accepted October 23, 1997.
| |
ABBREVIATIONS |
Abbreviations:
CHI, chalcone isomerase.
CHS, chalcone synthase.
DFR, dihydroflavonol 4-reductase.
F3H, flavanone-3hydroxylase.
NPPB, 5-nitro-2-(3-phenylpropylamino)-benzoic acid.
PAL, Phe ammonia-lyase.
| |
ACKNOWLEDGMENTS |
We wish to thank Dr. Brenda Shirley at the Virginia Polytechnic
Institute, Blacksburg, for generously providing us with antibodies and
for helpful advice. We also thank Dr. Brian Parks and Yoo-Sun Noh for
very helpful advice.
| |
LITERATURE CITED |
Ahmad M,
Cashmore AR
(1993)
HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor.
Nature
366:
162-166
[CrossRef][Medline]
Ahmad M,
Cashmore AR
(1997)
The blue-light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thaliana.
Plant J
11:
421-427
[CrossRef][Web of Science][Medline]
Ahmad M,
Lin C,
Cashmore AR
(1995)
Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light responsive anthocyanin accumulation and inhibition of hypocotyl elongation.
Plant J
8:
653-658
[CrossRef][Web of Science][Medline]
Batschauer A,
Ehmann B,
Schäfer E
(1991)
Cloning and characterization of a chalcone synthase gene from mustard and its light-dependent expression.
Plant Mol Biol
16:
175-185
[CrossRef][Web of Science][Medline]
Batschauer A,
Rocholl M,
Kaiser T,
Nagatani A,
Furuya M,
Schäfer E
(1996)
Blue and UV-A light-regulated CHS expression in Arabidopsis independent of phytochrome A and phytochrome B.
Plant J
9:
63-69
Bruns B,
Halbrock K,
Schäfer E
(1986)
Fluence dependence of the ultraviolet-light-induced accumulation of chalcone synthase mRNA and effects of blue and far-red light in cultured parsley cells.
Planta
169:
393-398
[CrossRef][Web of Science]
Burbulis IE,
Iacobucci M,
Shirley BW
(1996)
A null mutation in the first enzyme of flavanoid biosynthesis does not affect male fertility in Arabidopsis.
Plant Cell
8:
1013-1025
[Abstract]
Chappell J,
Hahlbrock K
(1984)
Transcription of plant defense genes in response to UV light or fungal elicitor.
Nature
311:
76-78
[CrossRef]
Cho MH,
Spalding EP
(1996)
An anion channel in Arabidopsis hypocotyls activated by blue light.
Proc Natl Acad Sci USA
93:
8134-8138
[Abstract/Free Full Text]
Christie JM,
Jenkins GI
(1996)
Distinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells.
Plant Cell
8:
1555-1567
[Abstract]
Dangl JL
(1991)
Regulatory elements controlling developmental and stress induced expression of phenylpropanoid genes.
In
T Boller,
F Meins,
eds, Plant Gene Research, Vol 8: Genes Involved in Plant Defense.
Springer-Verlag, New York, pp 303-326
Deikman J,
Hammer PE
(1995)
Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana.
Plant Physiol
108:
47-57
[Abstract]
Delseny M,
Cooke P,
Penon P
(1983)
Sequence heterogeneity in radish nuclear ribosomal RNA genes.
Plant Sci Lett
30:
107-119
Dixon RA,
Pavia NL
(1995)
Stress-induced phenylpropanoid metabolism.
Plant Cell
7:
1085-1097
[CrossRef][Web of Science][Medline]
Feinbaum RL,
Ausubel FM
(1988)
Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene.
Mol Cell Biol
8:
1985-1992
[Abstract/Free Full Text]
Feinbaum RL,
Storz G,
Ausbel FM
(1991)
High intensity and blue light regulated expression of chimeric chalcone synthase genes in transgenic Arabidopsis thaliana plants.
Mol Gen Genet
226:
449-456
[CrossRef][Medline]
Frohnmeyer H,
Ehmann B,
Kretsch M,
Rocholl M,
Harter K,
Nagatani A,
Furuya M,
Batschauer A,
Halbrock K,
Schäfer E
(1992)
Differential usage of photoreceptors for chlacone synthase gene expression during plant development.
Plant J
2:
899-906
[CrossRef]
Fuglevand G,
Jackson JA,
Jenkins GI
(1996)
UVB-UVA and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis.
Plant Cell
8:
2347-2357
[Abstract]
Jackson JA,
Jenkins GI
(1995)
Extension-growth responses and expression of flavonoid biosynthesis genes in the Arabidopsis hy4 mutant.
Planta
197:
233-239
[Web of Science][Medline]
Koornneef M, Rolff E, Spruit CJP (1980) Genetic control of
lightinhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzenphysiol Bd
100S: 147-160
Kubasek WL,
Shirley BW,
McKillop A,
Goodman HM,
Briggs W,
Ausbel FM
(1992)
Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings.
Plant Cell
4:
1229-1236
[Abstract/Free Full Text]
Lange H,
Shropshire W Jr,
Mohr H
(1970)
An analysis of phytochrome-mediated anthocyanin synthesis.
Plant Physiol
47:
649-655
Lewis BD,
Karlin-Neumann G,
Davis RW,
Spalding EP
(1997)
Calcium-activated anion channels and membrane depolarization induced by blue light and cold in Arabidopsis seedlings.
Plant Physiol
114:
1327-1334
[Abstract]
Martin CR
(1993)
Structure, function, and regulation of the chalcone synthase.
Int Rev Cytol
147:
233-284
[Web of Science][Medline]
Mol J,
Jenkins GI,
Schäfer E,
Weiss D
(1996)
Signal perception, transduction, and gene expression involved in anthocyanin biosynthesis.
Crit Rev Plant Sci
15:
525-557
Neuhaus G,
Bowler C,
Kern R,
Chua N-H
(1993)
Calcium/calmodulin-dependent and independent phytochrome signal transduction pathways.
Cell
73:
937-952
[CrossRef][Web of Science][Medline]
Ohl S,
Halbrock K,
Schäfer E
(1989)
A stable blue-light derived signal modulates ultraviolet-light induced activation of the chalcone synthase gene in cultured parsley cells.
Planta
177:
228-236
[CrossRef]
Shirley BW,
Hanley S,
Goodman HM
(1992)
Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations.
Plant Cell
4:
333-347
[Abstract/Free Full Text]
Shirley BW,
Kubasek WL,
Storz G,
Bruggemann E,
Koornneef M,
Ausubel FM,
Goodman HM
(1995)
Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis.
Plant J
8:
659-671
[CrossRef][Web of Science][Medline]
Spalding EP,
Cosgrove DJ
(1989)
Large plasma-membrane depolarization precedes rapid blue-light-induced growth inhibition in cucumber.
Planta
178:
407-410
[CrossRef][Web of Science][Medline]
Tamari G,
Bochorov A,
Atzorn R,
Weiss D
(1995)
Methyl jasmonate induces pigmentation and flavonoid gene expression in petunia corollas: a possible role in wound response.
Physiol Plant
94:
45-50
[CrossRef]
Tsukaya H,
Ohshima T,
Naito S
(1991)
Sugar-dependent expression of CHS-A gene for chalcone synthase from petunia in transgenic Arabidopsis.
Plant Physiol
97:
1414-1421
[Abstract/Free Full Text]
Wanner LA,
Li G,
Ware D,
Somssich I,
Davis KR
(1995)
The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana.
Plant Mol Biol
27:
327-338
[CrossRef][Medline]
Weiss D,
van Tunen AJ,
Halevy AH,
Mol JNM,
Gerats AGM
(1990)
Stamens and gibberellic acid in the regulation of flavonoid gene expression in the corolla of Petunia hybrida.
Plant Physiol
94:
511-515
[Abstract/Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
C. C.C. Chang, I. Slesak, L. Jorda, A. Sotnikov, M. Melzer, Z. Miszalski, P. M. Mullineaux, J. E. Parker, B. Karpinska, and S. Karpinski
Arabidopsis Chloroplastic Glutathione Peroxidases Play a Role in Cross Talk between Photooxidative Stress and Immune Responses
Plant Physiology,
June 1, 2009;
150(2):
670 - 683.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Peng, D. Hudson, A. Schofield, R. Tsao, R. Yang, H. Gu, Y.-M. Bi, and Steven. J. Rothstein
Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene
J. Exp. Bot.,
August 1, 2008;
59(11):
2933 - 2944.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Wu and E. P. Spalding
Separate functions for nuclear and cytoplasmic cryptochrome 1 during photomorphogenesis of Arabidopsis seedlings
PNAS,
November 20, 2007;
104(47):
18813 - 18818.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. Klychnikov, K. Li, H Lill, and A. de Boer
The V-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14-3-3 proteins
J. Exp. Bot.,
March 1, 2007;
58(5):
1013 - 1023.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Lohmann, M. A. Schottler, C. Brehelin, F. Kessler, R. Bock, E. B. Cahoon, and P. Dormann
Deficiency in Phylloquinone (Vitamin K1) Methylation Affects Prenyl Quinone Distribution, Photosystem I Abundance, and Anthocyanin Accumulation in the Arabidopsis AtmenG Mutant
J. Biol. Chem.,
December 29, 2006;
281(52):
40461 - 40472.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. M. Warpeha, S. S. Lateef, Y. Lapik, M. Anderson, B.-S. Lee, and L. S. Kaufman
G-Protein-Coupled Receptor 1, G-Protein G{alpha}-Subunit 1, and Prephenate Dehydratase 1 Are Required for Blue Light-Induced Production of Phenylalanine in Etiolated Arabidopsis
Plant Physiology,
March 1, 2006;
140(3):
844 - 855.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Zhang, J. Ramirez, D. Reboutier, M. Brault, J. Trouverie, A.-M. Pennarun, Z. Amiar, B. Biligui, L. Galagovsky, and J.-P. Rona
Brassinosteroids Regulate Plasma Membrane Anion Channels in Addition to Proton Pumps During Expansion of Arabidopsis thaliana Cells
Plant Cell Physiol.,
September 1, 2005;
46(9):
1494 - 1504.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. de Meaux, U. Goebel, A. Pop, and T. Mitchell-Olds
Allele-Specific Assay Reveals Functional Variation in the Chalcone Synthase Promoter of Arabidopsis thaliana That Is Compatible with Neutral Evolution
PLANT CELL,
March 1, 2005;
17(3):
676 - 690.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Xiang, B. L. Werner, E'L. M. Christensen, and D. J. Oliver
The Biological Functions of Glutathione Revisited in Arabidopsis Transgenic Plants with Altered Glutathione Levels
Plant Physiology,
June 1, 2001;
126(2):
564 - 574.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Long and G. I. Jenkins
Involvement of Plasma Membrane Redox Activity and Calcium Homeostasis in the UV-B and UV-A /Blue Light Induction of Gene Expression in Arabidopsis
PLANT CELL,
December 1, 1998;
10(12):
2077 - 2086.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
P. Piazza, A. Procissi, G. I. Jenkins, and C. Tonelli
Members of the c1/pl1 Regulatory Gene Family Mediate the Response of Maize Aleurone and Mesocotyl to Different Light Qualities and Cytokinins
Plant Physiology,
March 1, 2002;
128(3):
1077 - 1086.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
Top
Abstract
Introduction