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Plant Physiol. (1999) 119: 429-434
Blue Light and Abscisic Acid Independently Induce Heterophyllous
Switch in Marsilea quadrifolia1
Bai-Ling Lin* and
Wen-Jen Yang2
Institute of Molecular Biology, Academia Sinica, Nankang, Taipei
115, Taiwan, Republic of China (B.-L.L., W.-J.Y.); and Graduate
Institute of Biotechnology, Chinese Culture University, Taipei 111, Taiwan, Republic of China (W.-J.Y.)
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ABSTRACT |
In
natural habitats Marsilea quadrifolia L. produces
different types of leaves above and below the water level. In aseptic cultures growth conditions can be manipulated so that leaves of the
submerged type are produced continuously. Under such conditions the
application of either blue light or an optimal concentration of
abscisic acid (ABA) induced the development of aerial-type leaves. When
fluridone, an inhibitor of ABA biosynthesis, was added to the culture
medium it did not prevent blue light induction of aerial leaf
development. During blue light treatment the endogenous ABA level in
M. quadrifolia leaves remained unchanged. However, after
the plants were transferred to an enriched medium, the ABA level
gradually increased, corresponding to a transition in development from
the submerged type of leaves to aerial leaves. These results indicate
that the blue light signal is not mediated by ABA. Therefore, in the
regulation of heterophyllous determination, discrete pathways exist in
response to environmental signals.
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INTRODUCTION |
Many aquatic plants produce distinct types of leaves in the parts
of the shoot above and below the water level (Allsopp, 1965 ; Sculthorpe, 1967). The submerged leaves are linear or dissected, with
undifferentiated mesophyll and few stomata in the epidermis (Gaudet,
1964; Schmidt and Millington, 1968; Deschamp and Cooke, 1985; Young et
al., 1987). In contrast, the aerial leaves are entire and broad, having
differentiated mesophyll and stomata in both the upper and lower
epidermis (Gaudet, 1964; Schmidt and Millington, 1968; Deschamp and
Cooke, 1985; Young et al., 1987). During the life cycle of a plant this
type of heterophylly is reversible in response to environmental changes
(Allsopp, 1965; Sculthorpe, 1967). In addition to the position relative
to the water surface, other environmental factors have been examined individually. In general, long photoperiods, high fluence rates, high
temperatures, an aerobic atmosphere, or osmotic stress favor the
development of aerial leaves (for reviews, see Allsopp, 1965; Trewavas
and Jones, 1991). However, the effects of environmental changes are
dosage dependent and there is interplay between these signals (McCully
and Dale, 1961; Bostrack and Millington, 1962; Gaudet, 1965; Schmidt
and Millington, 1968; Bodkin et al., 1980). Therefore, the leaf form is
the final result of interactions among environmental stimuli and
manifests the greatest adaptive relevance.
From a series of experiments with Marsilea
drummondii in aseptic cultures, Allsopp (1965) concluded that
various factors triggering the heterophyllous switch contributed to the
"hydration state" of the cell, i.e. culture conditions may have an
effect on heterophylly by changing the cellular solute concentration.
Indeed, when ABA, the phytohormone known to mediate the signal of
osmotic stress, was applied at an optimal range of concentrations to
the culture medium of Marsilea quadrifolia, it was able to
substitute for the various environmental changes and induce the aerial
type morphology (Liu, 1984). In addition to M. quadrifolia,
this has also been shown in Potamogeton nodosus (Anderson,
1978), Limnophila indica (Mohan Ram and Rao, 1982),
Callitriche heterophylla (Deschamp and Cooke, 1983),
Ranunculus flabellaris (Young and Horton, 1985), Hippuris vulgaris (Kane and Albert, 1987a), and
Proserpinaca palustris (Kane and Albert, 1987b). The
question immediately arises whether ABA is the endogenous physiological
agent for inducing heterophyllous switch. In H. vulgaris
there is a good correlation between the increase in endogenous ABA
content and the induction of aerial leaf development by osmotic stress
(Goliber and Feldman, 1989), supporting the hypothesis that, upon
reaching the water surface, desiccation of the shoot tip causes an
increase in endogenous ABA, which triggers aerial leaf development
(Anderson, 1978).
In nature aerial-type leaves are also produced below the water surface
in Hippuris ssp. (McCully and Dale, 1961; Bodkin
et al., 1980). Moreover, many growth conditions used in the laboratory to induce the formation of aerial leaves on submerged shoots do not
seem to involve the desiccation of the responsive tissues (Allsopp,
1955; Jones, 1955; McCully and Dale, 1961; Bostrack and Millington,
1962; Gaudet, 1963, 1965; Schmidt and Millington, 1968; Bodkin et al.,
1980). In nature the rhizome of M. quadrifolia is either
rooted in the mud or traverses the water, and so the only portions of
the plant that are exposed to dry air are the upper part of the petiole
and the blades of the aerial leaf. If the accumulation of ABA is due to
desiccation of these parts of the plant, then there has to be an
earlier signal causing the petiole to elongate beyond the water level
(Liu, 1984). Therefore, factors other than desiccation must evoke an
equally effective mechanism to induce morphogenesis. The question,
then, is whether these factors are also mediated by ABA.
In H. vulgaris, the effect of high fluence on aerial leaf
formation has been correlated with a detectable level of ABA (Goliber, 1989). It has been, therefore, suggested that high fluence increases photosynthetic activity and hence the cell solute content, thereby presenting a form of osmotic stress to the cell (Goliber, 1989). This
explanation is appealing because it not only suggests that the light
signal uses ABA as a second messenger to turn on downstream responses,
but it implies that photomorphogenesis is a result of elevated
photosynthesis. Blue light is a potent photomorphogen (Kaufman, 1993;
Deng, 1994; Short and Briggs, 1994; Ahmad and Cashmore, 1996) and has
been shown to induce aerial form development in Marsilea
vestita (Gaudet, 1965); therefore, we investigated its effects. We
present data showing that the blue light signal is not mediated by ABA
and that photomorphogenesis and photosynthesis are uncoupled.
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MATERIALS AND METHODS |
Plant Materials, Growth Conditions, and Treatments
Aseptic cultures of Marsilea quadrifolia L. were
established according to the method of Liu (1984). Plants were cultured
in a liquid basal medium (Laetsch, 1967) supplemented with 3% Suc and
propagated by cutting the rhizomes into two-node segments to induce the
formation of new shoots from the axillary buds. Clones of the same
plant were used in the experiments reported here. Cultures were kept in
a growth chamber set at 25°C with a 16-h photoperiod, and
illumination was provided by fluorescent tubes (FL40D-EX, Mitsubishi,
Tokyo, Japan) emitting a near-sunlight spectrum to reach 40 µmol
m 2 s1 at the culture
level. Treatments were applied to the newly developed shoots 7 d
after subculture. Other than the treatments indicated in the text, the
culture conditions were kept the same.
ABA or fluridone was added from a 1000× stock solution to the culture
medium to reach the indicated final concentrations. Light sources of
various colors were provided by filtering the output of the fluorescent
tubes through cellophane sheets purchased from a local supplier. The
transmission spectra of the cellophane filters were measured and
recorded with a diode array spectrophotometer (model 8452A,
Hewlett-Packard; Fig. 1). The fluence
rate under each light was adjusted to the same as that of the control.
The length of the petiole was measured with a ruler on plants removed from the culture flask. Six to 10 plants were used in each treatment and the experiments were repeated three times. The resulting leaf morphology and the patterns of changes in petiole length were consistent in the repeated experiments. The measurements of petiole length varied up to 20% between the experiments. Table II shows data
from one experiment.
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| Figure 1.
Transmission spectra of cellophane filters
providing the light sources of different colors for testing the effect
on heterophylly. The transmittance was measured and recorded with a
diode array spectrophotometer.
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Table II.
The progressive effects of various treatments on
petiole elongation in M. quadrifolia
Results are shown as petiole length (average ± SD)
recorded after 3 weeks of treatment. Aside from the indicated
treatments, other culture conditions were kept the same.
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Alternatively, plants were cultured in liquid MS medium (Murashige and
Skoog, 1962) supplemented with 3% Suc. The osmotic potentials of the
culture media were measured with a vapor pressure osmometer (model
5100C, Wescor, Logan, UT). To obtain plant materials grown in the
field, cultured plants were transferred to a plot (1 × 2 m)
in the experimental field of the Institute of Botany, Academia Sinica,
and the water level was kept approximately 1 cm in depth.
Measurement of ABA Content
Endogenous ABA was extracted from M. quadrifolia leaves
with 80% methanol according to the method of Walker-Simmons (1987) and
quantified with an ELISA using monoclonal antibodies against ABA
(Idetek, San Bruno, CA). As an internal standard for monitoring recovery, 0.2 pmol (10 µCi) of
DL-cis,trans-[U-3H]ABA
(Amersham) was added to the extract from each gram of fresh tissue. In
a total of 50 samples the recovery was 74% ± 12%.
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RESULTS |
Blue Light Induction of Heterophyllous Switch
The aerial leaf of M. quadrifolia resembles a four-leaf
clover, with quadrifid lamina expanded at an angle to the petiole (Fig.
2, B, D, and F), whereas the submerged
leaf has divided, oblanceolate leaflets, expanded in the plane of the
petiole (Fig. 2, A-E). Under our culture conditions, in basal medium
and a 16-h photoperiod at 25°C, M. quadrifolia plants
continued to produce the submerged type of leaves (Fig. 2A). When the
plants were irradiated with blue light, while other culture parameters
remained the same, aerial leaves were induced (Fig. 2B). We determined
the action spectra for heterophyllous transition by irradiating the
plants with various lights at the same fluence rate. When other culture conditions were kept unchanged, aerial leaf development was inducible by blue or purple, but not by red, yellow, or green light (Table I; see Fig. 1 for the spectra of the
light sources).
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| Figure 2.
The effects of blue light and fluridone on
heterophyllous switch in M. quadrifolia. Plants were
cultured aseptically in a basal medium (Laetsch, 1967) supplemented
with 3% Suc and were kept at 25°C with 16-h photoperiod. A, Control
plant grown under the stated conditions for 3 weeks. B, Plant cultured
under control conditions for 7 d (as the shoot apex reached the
position indicated by the arrowhead) and then transferred to blue light
and grown for another 2 weeks. Note the production of aerial leaflet
morphology, the elongation of petioles and roots, the formation of
lateral roots, and the shortening of the internodes in the part of
plant developed under blue light (to the right of the arrowhead). C,
Plant grown under control conditions for 7 d (as in A and B)
initially and then with the addition of 1 µM fluridone to
the culture medium for 2 weeks. The part of the plant to the right of
the arrowhead was produced in the presence of 1 µM
fluridone. Note the reduction in the coloration of shoot tissues and in
the size of the organs. D, Plant as in C except blue light was applied
simultaneously with fluridone. Note the formation of aerial
characteristics under blue light in the presence of 1 µM
fluridone. E, Leaflet morphology of a submerged-type leaf produced in
the presence of 1 µM fluridone as described in C. F,
Leaflet morphology of an aerial leaf produced under blue light in the
presence of 1 µM fluridone as described in D. Scale
bars = 1 cm (A-D), 2 mm (E), and 4 mm (F).
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Table I.
The effect of light quality on the induction of
heterophyllous switch in M. quadrifolia
Plants were transferred to the indicated light sources 7 d after
subculture. The final leaf type was recorded 2 weeks later. Growth
conditions other than the light regime were kept the same. The fluence
rate was adjusted to 40 µmol m2 s1 at the
culture level under each light source.
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In responding to the inductive irradiation, the developmental switch
occurred only in that part of the plant newly produced during the
treatment; the tissues already formed were unaffected (Fig. 2B). The
switch occurred in various organs. In addition to the formation of the
characteristic aerial lamina, the morphological changes induced by blue
light included elongation of petioles and roots, lateral root
formation, and shortening of internodes (Fig. 2B). These responses to
blue light are similar, if not identical, to those induced by ABA (Liu,
1984).
ABA Effects
Since the effect of ABA is dosage dependent (Liu, 1984), we tested
a range of ABA concentrations (10 nM to 100 µM) under our culture conditions. ABA at higher than 0.5 µM is effective in inducing aerial leaf development. At
high concentrations (10, 50, and 100 µM), the leaves were
smaller and growth was gradually retarded (data not shown). These
results are similar to those reported by Liu (1984). We therefore
routinely used 1 µM ABA as the optimal concentration in
further experiments.
Blue Light Induction of Heterophyllous Switch in the Presence of
Fluridone
Fluridone blocks the conversion of phytoene to phytofluene
(Vaisberg and Schiff, 1976; Bartels and Watson, 1978; Fong and Schiff,
1979), which is a primary step in the carotenoid pathway leading to the
synthesis of a number of compounds including carotenoids, chlorophylls,
and ABA. Fluridone has also been shown to inhibit the accumulation of
endogenous ABA (Moore and Smith, 1984; Moore et al., 1985; Gamble and
Mullet, 1986). If the blue light signal is mediated by ABA and causes
the biosynthesis or accumulation of ABA, then fluridone treatment would
be expected to block the blue light induction of the heterophyllous
transition. Under our growth conditions with regular illumination,
after 1 µM fluridone was added to the culture medium, a
distinctive reduction in the coloration of the newly produced tissues
was observed, indicating an inhibition of carotenoid and chlorophyll
synthesis (Fig. 2, C and E). However, when the cultures were irradiated
with blue light in the presence of 1 µM fluridone,
despite the bleaching, the new leaves still developed into the aerial
form (Fig. 2, D and F). There was a general growth inhibition by 1 µM fluridone, with a gradual decrease in the size of the
new leaves (Fig. 2C; Table II). Higher
concentrations of fluridone (10 and 100 µM) increasingly
inhibited growth but did not prevent the induction of aerial leaf
development by blue light (not shown). These data imply that either ABA
is not synthesized in the carotenoid pathway in M. quadrifolia or blue light action does not require de novo synthesis of ABA.
We used petiole length as an index to compare the growth of leaves in
various treatments. As shown in Table II, blue light and 1 µM ABA, either applied individually or together, caused a
progressive increase in the petiole length of new leaves produced during the 3-week treatment. On the contrary, 1 µM
fluridone caused a progressive decrease in petiole length whether the
plant was grown under blue light or regular light. With 1 µM fluridone and blue light, the first leaves produced on
the plants were comparable to those on plants treated with 1 µM ABA alone, blue light alone, or both (Table II). This
indicates that petiole elongation, a significant feature of aerial leaf
development stimulated by blue light, was initially unaffected by
the inhibitory effect of fluridone. In the given culture conditions,
the leaves produced later were longer in plants irradiated with blue
light than in those treated with 1 µM ABA under regular
light, whereas the petiole length in plants grown in 1 µM
ABA under blue light fell in between (Table II). These data suggest
that, in the control of heterophylly, blue light acts in a pathway
distinct from but interacting with that of ABA. Consequently, the key
issue is whether blue light causes an increase in the endogenous ABA
level.
Endogenous ABA Levels
We then measured the endogenous ABA content in M. quadrifolia leaves grown under various conditions. As shown in
Table III, ABA levels were similar in the
submerged leaves grown in culture and in the aerial leaves whether
induced by blue light in culture or grown in a semidry field.
Therefore, during blue light treatment, the plants did not contain
elevated levels of ABA.
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Table III.
Endogenous ABA levels in the leaves of M. quadrifolia produced under various conditions
Aerial leaves grown in the field or induced by blue light in culture
contain ABA levels similar to submerged leaves produced in culture. ABA
contents are the averages ± SD of three samples.
Leaves were pooled from different plants to give 1 to 2 g fresh
weight of tissue per sample. ABA contents were detected with ELISA
using monoclonal antibodies against ABA.
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As a contrast MS medium (Murashige and Skoog, 1962) was also used to
induce aerial form development. This medium was chosen mainly because
it is commonly used in tissue culture. When the components were
compared, MS medium contained higher concentrations of several major
and minor mineral salts than the basal medium (comparisons not shown).
The osmotic potential in MS medium was 194 mmol
kg1, which is 1.5-fold that in the basal medium
(131 mmol kg1). After being transferred to MS
medium, M. quadrifolia plants continued to produce the
submerged leaves for the first 2 weeks. Starting in the 3rd week with
the formation of a series of transitional characteristics, the leaves
gradually changed from the submerged form to the aerial form (data not
shown). The endogenous ABA measurements in these plants showed
increases in parallel with the morphogenetic transition in the MS
medium (Fig. 3). These results indicate
that the effect of this enriched medium on heterophyllous switch is gradual and is correlated with the accumulation of endogenous ABA.
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| Figure 3.
Relationship between the endogenous ABA level in
leaves of M. quadrifolia and the duration that the
plants were cultured in MS medium. Leaves from several plants were
pooled to give 1 to 2 g fresh weight (gFW) of tissue per sample.
Data points represent the averages and SD of samples
measured in three independent experiments. The SD in the
samples for d 0 and 16 are less than 0.05 nmol/g fresh weight. ABA
contents were determined with ELISA using monoclonal antibodies against
ABA.
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DISCUSSION |
In M. quadrifolia blue light induction of aerial form
characteristics does not appear to require de novo synthesis of ABA and
does not result in the accumulation of ABA. We therefore conclude that
ABA does not mediate the blue light signal in inducing the heterophyllous switch. This is in contrast to the effect of an enriched
medium, in which the developmental transition is correlated with the
gradual increase in the endogenous ABA level. These data indicate that
environmental stimuli are transduced via multiple signaling pathways
that converge on the master switch of heterophylly. Some but not all of
the environmental signals are mediated by ABA.
A close examination of the aerial-form characteristics in M. quadrifolia suggests that the adaptive value of the developmental switch is related to photosynthetic capacity. While growing with a
rhizome in a liquid environment, the limiting factor for survival is
the availability of light rather than water. The elongation of the
petiole, along with the increase in leaf size and the change in leaflet
shape that maximize the leaf surface area (see Fig. 2), greatly
enhances the ability of the plant to capture light. Aerial form
development thus appears to be a response to a favorable environment
that provides light in abundance. Our results suggest that either blue
light or ABA simulates a favorable environment. The well-established
facts that blue light is a potent photomorphogen and that its energy
can be used in photosynthesis prompt us to suggest that blue light
changes the route of development via a prescribed signaling pathway
involving the fine tuning of photosynthetic capacity. ABA, on the
other hand, is known to be associated with the response to drought
stress and has been shown to down-regulate photosynthetic genes
(for review, see Zeevaart and Creelman, 1988; Skriver and Mundy,
1990; Chandler and Robertson, 1994; Weatherwax et al., 1996). When
aquatic plants reach the surface of water, they experience a drought
stress that is likely mediated by ABA. However, reaching the surface of
the water means a combination of drought stress and the
availability of sunlight. Therefore, the ABA signal may be decoded
by the plant as being both and hence is followed by aerial form
development.
In the presence of fluridone, an inhibitor of the carotenoid
biosynthesis pathway, the photosynthetic pigments appear to be missing
in the newly developed tissues of M. quadrifolia. However, these tissues still respond to blue light induction by changing their
route of development. This clearly shows the uncoupling of
photomorphogenesis and photosynthetic capacity. Although the development of the aerial characteristics has a significant consequence in increasing photosynthetic capability, the latter appears not to be a
prerequisite for such a development. This phenomenon provides a system
for investigating the cross-talk between the signaling pathways
responding to various environmental factors affecting both
morphogenesis and photosynthetic activities.
Quantification of growth by the measurement of petiole length shown in
Table II indicates the interplay among the various factors: blue light,
ABA, and fluridone. Although we calibrated the fluence level of blue
light and tested a range of concentrations of fluridone and ABA, the
data suggest a difference in the effectiveness of each factor. For
example, the blue light level we used appears to be more effective than
the ABA level in inducing petiole elongation. Moreover, the application
of both blue light and ABA at the given levels results in an averaging
rather than an additive effect. The nature of the dosage or
effectiveness and the interaction of these factors remain to be defined
at the cellular and molecular levels. The data presented here indicate
that the morphogenetic determination involved in heterophyllous
transition in M. quadrifolia is not only qualitative but
also quantitative.
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FOOTNOTES |
1
This work was supported by grants to B.-L.L.
from Academia Sinica and the National Science Council (no.
NSC85-2311-B-001-091), Republic of China.
2
Present address: Graduate Institute of Life
Sciences, National Sun Yat-sen University, Kaoshiung 804, Taiwan,
Republic of China.
*
Corresponding author; e-mail mblbl{at}ccvax.sinica.edu.tw; fax
886-2-2788-3739.
Received May 28, 1998;
accepted November 10, 1998.
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ABBREVIATIONS |
Abbreviation:
MS, Murashige and Skoog.
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ACKNOWLEDGMENTS |
We thank Drs. Sham Goyal, Judy Jernstedt, and Wen-Yuan Kao for
the measurements of osmotic potential; Ms. Yi-Chieh Chang and Mr.
Hsueh-Jen Liao for technical assistance; and the Institute of Botany,
Academia Sinica, for the use of the experimental field. We are grateful
to Drs. M.M. Green, Roger Hangarter, and Tuan-hua David Ho, as well as
two anonymous reviewers, for comments concerning the manuscript.
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Abstract
Introduction