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Plant Physiol. (1998) 116: 637-641
Induction and Regulation of Expression of a
Low-CO2-Induced Mitochondrial Carbonic Anhydrase in
Chlamydomonas reinhardtii
Mats Eriksson1, *,
Per Villand,
Per Gardeström, and
Göran Samuelsson
Department of Plant Physiology, Umeå University, S-901 87 Umeå,
Sweden
 |
ABSTRACT |
The time course of and the influence
of light intensity and light quality on the induction of a
mitochondrial carbonic anhydrase (CA) in the unicellular green alga
Chlamydomonas reinhardtii was characterized using
western and northern blots. This CA was expressed only under
low-CO2 conditions (ambient air). In asynchronously grown
cells, the mRNA was detected 15 min after transfer from air containing
5% CO2 to ambient air, and the 21-kD polypeptide was
detected on western blots after 1 h. When transferred back to air
containing 5% CO2, the mRNA disappeared within 1 h
and the polypeptide was degraded within 3 d. Photosynthesis was
required for the induction in asynchronous cultures. The induction
increased with light up to 500 µmol m 2
s1, where saturation occurred. In cells grown
synchronously, however, expression of the mitochondrial CA was also
detected in darkness. Under such conditions the expression followed a
circadian rhythm, with mRNA appearing in the dark 30 min before the
light was turned on. Algae left in darkness continued this rhythm for
several days.
| |
INTRODUCTION |
Many unicellular green algae induce a CCM when cells grown under
high-CO2 conditions (5% CO2) are
transferred to low-CO2 conditions (ambient air)
(Badger and Price, 1992 ). This mechanism allows the algal cell to
concentrate the available carbon close to the active site of Rubisco,
ensuring efficient photosynthesis even under
CO2-limiting conditions. In Chlamydomonas
reinhardtii at least seven polypeptides are synthesized during the
induction of the CCM (Bailly and Coleman, 1988; Manuel and Moroney,
1988; Spalding and Jeffrey, 1989; Burow et al., 1996), but only one protein, a pCA, has been positively identified as a component of the
CCM. Of the other low-CO2-induced polypeptides,
one has been identified as an Ala aminotransferase (Chen et al., 1996), one has been proposed to be a chloroplast envelope carrier protein (Chen et al., 1997), and in an earlier report we identified one as an
mtCA (Eriksson et al., 1996). Although these three proteins are all
induced by low CO2, it is not known whether they
play a direct role in the CCM. The identity, localization, and function of the other low-CO2-induced polypeptides have
yet to be resolved.
pCA has been thoroughly studied, and many aspects of its induction have
been characterized. It is encoded by two genes, Cah1 and
Cah2, of which Cah1 is expressed only under
low-CO2 conditions and Cah2 is
expressed only under high-CO2 conditions
(Fujiwara et al., 1990). The induction of Cah1 is inhibited
by mixotrophic growth on acetate (Spalding and Ogren, 1982; Moroney et
al., 1987; Fett and Coleman, 1994). In asynchronously grown C. reinhardtii, the expression of Cah1 is dependent on
both light quality and light intensity. The protein is not expressed
unless light of blue wavelengths is present (Dionisio et al., 1989b),
and the expression increases with increasing light intensity (Dionisio et al., 1989a). In synchronously grown C. reinhardtii
cultures, Cah1 is expressed mainly at the beginning of the
light period. The first transcripts are seen 30 min before the light is
turned on, indicating that the protein is under the control of a
circadian clock (Rawat and Moroney, 1995; Fujiwara et al., 1996).
In the present study we characterized the regulation of expression of
mtCA in response to CO2, red light, acetate, and
light intensity under asynchronous growth, as well as the influence of
light/dark cycles under synchronous growth.
| |
MATERIALS AND METHODS |
Algal Strain and Culture Conditions
Chlamydomonas reinhardtii, cell wall-deficient strain
CW 92, was grown in batch cultures at 25°C under continuous light at an intensity of 150 µmol m2
s1. Bottles containing 800 mL of minimal medium
were vigorously bubbled with air containing 5% CO2. For
low-CO2 conditions, the cultures were bubbled
with air. The major components of the medium were prepared according to
the method of Sueoka (1960), and the trace element solution was
prepared according to the method of Hutner et al. (1950). Light
intensities were measured with an LI-185a quantum meter (Li-Cor,
Lincoln, NE).
For time-course experiments of induction, cells were concentrated by
centrifugation (5 min, 2000g), resuspended in fresh medium, and bubbled with air. Samples for northern- and western-blot analyses were withdrawn before the induction and 0.5, 1, 1.5, 3, 6, 12, and
24 h after the cells were transferred to air conditions. After 24 h of air bubbling, the culture was split into two fractions. One fraction was left under low-CO2 conditions
for 1 week, and the other was transferred back to
high-CO2 conditions. Samples for northern-blot
analysis were withdrawn from the latter fraction 15, 30, 45, and 60 min
after the transfer. Samples for western-blot analysis were collected
36, 48, 60, and 72 h after the low-to-high CO2 transfer.
Mixotrophic growth was obtained by the addition of sodium acetate to a
final concentration of 20 mm. To prevent depletion of
acetate and other nutrients, the cultures were diluted with fresh
medium every 24 h. For studies of the induction at different light
intensities, flasks with 80-mL cultures were positioned at different
distances from the lamp (HPI-T 400 W, Philips, Eindhoven, The
Netherlands) to obtain the desired light intensities.
To measure the induction under red light,
high-CO2-grown cells were transferred to a
DW3 oxygen electrode reaction chamber (Hansatech, King's Lynn, UK) and
illuminated by light filtered through an interference filter (Schott,
Mainz, Germany), transmitting light with a wavelength of 684 nm. The
design of the DW3 oxygen electrode reaction chamber prevents ambient
room light from reaching the sample. Light can only enter through a
hole directly connected to the light source. The light intensity
that was used for induction was 10 µmol
m2 s1. Samples for
western-blot analysis were withdrawn after 4 h of induction.
To obtain synchronized cultures, cells were grown under
high-CO2 conditions for 3 d with 12-h
light/12-h dark cycles. After the fourth light period, the culture was
switched to low CO2 and divided into two
fractions. One was left under the light/dark regime, and the other was
transferred to continuous darkness. Samples for northern- and
western-blot analyses were withdrawn during the light period 1, 6, and
11 h after the onset of light, and during the dark period 1, 6, and 11.5 h after the light was turned off. During the continuous
dark treatments, the flasks were covered with three layers of aluminum
foil, wrapped in black plastic, and placed in a darkroom. Cells were
harvested under dim green light.
Western Analysis
The samples were separated by SDS-PAGE (12.5% polyacrylamide) as
described by Laemmli (1970) using the Mini-Protean II slab-gel apparatus (Bio-Rad). The polypeptides were electroblotted to
nitrocellulose filters for immunodetection with antisera raised against
the mtCA (Villand et al., 1997). Horseradish peroxidase-linked
secondary antibody and enhanced chemoluminescence western blotting
detection reagents from Amersham were used for detection. The methods
used were described by Harlow and Lane (1988). Protein concentrations of the samples were determined using the Bio-Rad protein assay according to the manufacturer's instructions.
Northern Analysis
RNA was isolated from 4 mL (5-10 µg chlorophyll
mL1) of culture using the TRIzol reagent (Life
Technologies) according to the manufacturer's instructions.
Glyoxal-denatured northern-blot analysis was performed according to the
method of Sambrook et al. (1989) with 32P-labeled
Mca12 cDNA (Eriksson et
al., 1996) as the probe. Hybridization and washing were done at 65°C.
The hybridization signals were quantified with a PhosphorImager
(Bio-Rad).
| |
RESULTS AND DISCUSSION |
Time Course of Induction and Degradation of mtCA
Experiments were performed to determine the time course of the
induction of mtCA under low-CO2 conditions, as
well as its repression when low-CO2 cells were
transferred to conditions of high CO2 (Fig.
1). In the northern-blot hybridization
experiments, transcripts were observed 30 min after the transfer to
low-CO2 conditions (Fig. 1A). A rapid increase in
the amount of transcript occurred during the first hours of induction,
reaching a maximum after about 6 h. The amount of transcripts was
slightly lower at 12 and 24 h after the transfer. Transcripts were
also detected in cells grown for 1 week under
low-CO2 conditions, but the amount had decreased
to what is typically found after 1 h of induction. The 21-kD mtCA
polypeptide was first observed 1 h after the induction, as
revealed by western-blot analysis (Fig. 1B). The amount of the
polypeptide increased during the first 24 h, after which the level
remained relatively constant for at least 1 week. The difference in
induction kinetics between mRNA and protein levels reflects the
stability of the protein. When the protein is fully induced, less mRNA
is needed to keep a constant pool of mtCA. When a
low-CO2-adapted culture was switched back to high
CO2, the mRNA disappeared after less then 1 h (Fig. 1A) and the amount of protein decreased gradually over 3 d
(Fig. 1C).
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| Figure 1.
Time-course experiments of the induction and
degradation of mtCA. A, Northern analysis of the relative amounts of
the mtCA mRNA. High-CO2-grown cells were transferred to
low-CO2 conditions at time 0. After 24 h, the culture
was transferred back to high-CO2 conditions. The triangle
represents cells left on low CO2 for 1 week. All lanes on
the northern blot contained 5 µg of total RNA. B, Western blot of the
induction of mtCA. Numbers represent hours after transfer to low
CO2. All lanes contained 0.5 µg of protein. C, Western
blot of the degradation of mtCA. Numbers represent hours after transfer
from low CO2 to high CO2. All lanes contained 0.5 µg of protein.
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There are two genes that encode pCA in C. reinhardtii: one
is expressed under low CO2 and one is expressed
under high CO2 (Fujiwara et al., 1990).
Transcripts for the low-CO2-induced form, Cah1, are present 1 h after the switch to low
CO2, reaching a maximum after 2 h. When
switched back to high CO2, the mRNA disappears after 1 h. The time scale for the regulation of the
Cah2 gene is similar, but this gene is induced by high
CO2 and repressed by low
CO2, and its mRNA is present in lower amounts.
The Cah1 gene product is detectable after 2 h, and the
amount of protein increased for 6 h, the longest time of induction
examined (Dionisio-Sese et al., 1990). The similarities of the time
courses for the induction of mtCA and pCA may indicate that mtCA also
has an important function in the CCM.
Expression of mtCA under Mixotrophic Growth
When the growth medium was supplemented with acetate, the
induction of mtCA was almost totally inhibited (Fig.
2A). Only a small amount of mtCA was
observed on western blots, as compared with cells transferred to
low-CO2 conditions in the absence of acetate. In
another set of experiments, a culture of
low-CO2-adapted phototrophic cells was split into
three fractions. One was left under low-CO2
phototrophic conditions, a second was left at low CO2 but supplemented with acetate, and a third
was transferred to high-CO2 conditions (Fig. 2B).
After 3 d, no mtCA could be detected in the acetate-supplemented
culture or in the culture transferred back to high
CO2. However, the amount of mtCA in the control
culture was unchanged.
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| Figure 2.
Western-blot analysis of the induction and
degradation of mtCA under mixotrophic and phototrophic growth. A,
Amount of mtCA in cells adapted to low-CO2 conditions for 4 or 8 h in the absence ( Ac) or presence (+Ac) of acetate in the
growth medium. All lanes contained 0.5 µg of protein. B, Amount of
mtCA in low-CO2-adapted phototrophic cells after transfer
to three different growth conditions for 3 d.
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Mixotrophic growth on acetate has also been reported to repress the
induction of pCA and the CCM (Spalding and Ogren, 1982; Moroney et al.,
1987; Fett and Coleman, 1994). A possible explanation for the lack of
induction under low-CO2 conditions in
acetate-supplemented medium is that when acetate is metabolized
CO2 is produced. This CO2
release might be sufficient to mimic high-CO2
conditions.
Light-Intensity Dependence
Using a reporter gene system, we found that the expression of the
mtCA genes depends on light intensity (Villand et al., 1997). In the
present study we examined the dependence of light intensity in more
detail, both at the mRNA and protein levels, to determine whether the
light-regulated induction is controlled at the level of transcription
or at the level of translation.
Using asynchronous cultures, no induction of mtCA mRNA was detected in
darkness, but within 15 min after transfer to
low-CO2 conditions the mtCA mRNA was observed
(Fig. 3A). When mRNA levels were
monitored 1 h after the transfer, the light response of mtCA expression resembled the light-response curve for photosynthesis, with
saturation occurring at approximately 500 µmol
m2 s1. Western-blot
analysis of cells grown for 2 h under
low-CO2 conditions revealed a similar pattern at
the protein level (Fig. 3B).
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| Figure 3.
Induction of mtCA under different light
intensities. A, The relative amount of mtCA mRNA after transfer to
low-CO2 conditions for 15 ( ), 30 ( ), and 60 ( ) min
under different light intensities. All lanes on the northern blot
contained 5 µg of total RNA. B, Western blot of mtCA after 2 h
of induction to low-CO2 conditions under different light
intensities. The light intensities were: lane 1, 25; lane 2, 75; lane
3, 150; lane 4, 300; lane 5, 450; and lane 6, 1200 µmol
m2 s1. All lanes contained 0.5 µg of
protein.
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In asynchronous cultures the induction of Cah1 not only
requires low CO2 but also light and a functioning
photosynthetic apparatus (Spalding and Ogren, 1982; Spencer et al.,
1983; Dionisio-Sese et al., 1990). Dionisio et al. (1989a) observed
that the induction of Cah1 was stimulated by higher light
intensities. A low induction was observed at 2 µmol
m2 s1, but the
induction increased dramatically up to 70 µmol
m2 s1, which was the
highest light intensity used. They also observed that when 10 µm DCMU (an inhibitor of the photosynthetic electron transport chain) was added before the carbon switch, no induction of
the CA occurred.
These results show that the expression of both mtCA and pCA are
dependent on photosynthetic electron transport. However, whether this
is because the induction is regulated by the redox state of the
electron transport chain, the production of energy, or some other
aspect of photosynthesis cannot be determined from these experiments.
The fact that light dependency is observed at the mRNA level shows that
the regulation is not at the level of translation.
Light-Quality Dependence
pCA has been shown to be regulated by light quality (Dionisio et
al., 1989b). No induction was observed at 25 µmol
m2 s1 red light.
However, if the red light was supplemented with 6 µmol
m2 s1 blue light,
induction occurred. In the present study we examined the induction of
mtCA under 10 µmol m2
s1 red light (684 nm; Fig.
4). A clear induction was seen at this low light intensity, demonstrating that the expression of mtCA is not
regulated by differences in the light quality in the same way as pCA
expression.
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| Figure 4.
The induction of mtCA under red light.
Western-blot analysis of samples withdrawn from the culture before (5%
CO2) and after (air) 4 h of induction under red light
(684 nm) of 10 µmol m2 s1. Both lanes
contained 0.5 µg of protein.
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Circadian Rhythm of mtCA mRNA Expression
If a plant is grown under a light/dark regime, many genes are
expressed in a diurnal manner. For some of these genes, the oscillating
expression follows a circadian rhythm. A circadian rhythm has a period
of about 24 h and is governed by an endogenous clock that is reset
every day by an exogenous stimulus such as light. If this stimulus is
withdrawn, the circadian rhythm continues to oscillate but with a
decreasing amplitude. A circadian rhythm is also temperature
compensated and will proceed at almost the same rate even if the
ambient temperature is changed. A diurnal rhythm, however, will not
continue in the absence of the entraining stimulus and is not
temperature compensated (Pittendrigh, 1960).
Figure 5 shows that the expression of
mtCA is at least to some extent controlled by a circadian clock when
the cells are grown synchronously in a 12-h light/12-h dark growth
cycle. Cells were grown in high CO2 and switched
to low CO2 at the beginning of the dark period.
The culture was divided into two fractions: one was left in a
light/dark cycle and the other was transferred to continuous darkness.
In both fractions, expression of the CA could be detected 30 min before
the start of the light period. The expression of the gene in the cells
left under the light/dark regime reached a maximum during the early
light period and decreased during the day (Fig. 5A). During the dark
period the expression was completely arrested. No mRNA was seen 1 h after the light was turned off; however, 30 min before the next light
period, the mRNA could be detected again. In the cells kept in
continuous darkness (Fig. 5B), mRNA was detected just before and just
after the light should have been turned on (0.5 and 1 h) during
the following 2 d. Although the induction was about 2 orders of
magnitude less than the corresponding expression in light, induction
for several days under continuous darkness shows that expression of
mtCA is to some extent controlled by a circadian clock and is not
dependent only on the presence of photosynthesis.
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| Figure 5.
Northern-blot analyses of mtCA mRNA levels in
synchronously grown cells. After three light/dark cycles, the culture
was transferred to low CO2 at the beginning of the fourth
dark period. A, Cells left under a light/dark regime. B, Cells
transferred to continuous darkness. Samples for mRNA analyses were
withdrawn 1, 6, and 11 h into the light period and 1, 6, and
11.5 h into the dark period. All lanes on the northern blot
contained 5 µg of total RNA.
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It has been demonstrated that Cah1 is under the control
of a circadian clock (Rawat and Moroney, 1995; Fujiwara et
al., 1996). When Rawat and Moroney (1995) cultured
low-CO2-adapted C. reinhardtii cells
synchronously under a 12-h light/12-h dark growth regime, they observed
that the Cah1 gene showed a diurnal expression, with
transcripts detected 1 h before the light was turned on. They also
observed that the pCA was expressed at the end of the first dark period
when high-CO2-grown synchronous cells were
switched to low CO2 30 min into the dark period.
Fujiwara et al. (1996) also grew low-CO2 cells
synchronously under a 12-h light/12-h dark growth regime and monitored
the diurnal expression of Cah1. They then split the culture
into two fractions: one left in continuous light and the other in
continuous darkness. In both cultures the oscillating expression of the
pCA gene was seen for 3 d, confirming that the gene was under
circadian control. In both studies the oscillating expression of the
Cah1 gene reached a maximum during the early light period,
decreased during the day, and stayed at a very low level during the
dark period.
| |
CONCLUSIONS |
The mtCA is expressed only under low-CO2
conditions, and the expression is inhibited by acetate. Light and
photosynthesis are absolute requirements for the induction of
mtCA under asynchronous growth. One hour after the transfer, the light
response of mtCA induction resembles the light-response curve for
photosynthesis, with saturation occurring at approximately 500 µmol
m2 s1. Photosynthesis
is not an absolute requirement for induction under synchronous growth.
Under such conditions a low expression is seen when cells are
transferred to continuous darkness, indicating that at least some of
the expression is under the control of a circadian clock. The only
difference in regulation between mtCA and pCA is that the induction of
mtCA seems not to be dependent on light of blue wavelengths. This
similarity in regulation is surprising, considering that the promoter
regions of the mtCA and the pCA show no sequence similarity (Villand et
al., 1997). It should also be stressed that mtCA and pCA probably have
two very different roles in the cell: pCA supplies
CO2 at the plasma membrane, and mtCA has been
suggested to be important for buffering the mitochondrial matrix
(Eriksson et al., 1996). The similarity in induction of mtCA and pCA
and the close correlation to the induction of the CCM may indicate that
mtCA has an important function in the CCM.
| |
FOOTNOTES |
1
Present address: Department of Chemistry and
Biochemistry, University of California, 405 Hilgard Avenue, Los
Angeles, CA 90095-1569.
*
Corresponding author; e-mail
mats.eriksson{at}plantphys.umu.se; fax 46-90-786-6676.
Received July 7, 1997;
accepted November 6, 1997.
2
In accordance with the Commission on Plant Gene
Nomenclature's guidelines, we have decided to change the names of the
genes encoding the mtCA from  -CA1 and
-CA2 to Mca1 and
Mca2.
| |
ABBREVIATIONS |
Abbreviations:
CA, carbonic anhydrase.
CCM, CO2-concentrating mechanism.
mtCA, mitochondrial CA.
pCA, periplasmic CA.
| |
ACKNOWLEDGMENT |
The authors thank Dr. Youn-Il Park for assistance with
experiments on light quality.
| |
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Top
Abstract
Introduction