Plant Science 165 (2003) 1403–1410

Effects of abscisic acid on photoinhibition in maize plants

Husen Jia, Congming Lu∗
Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany,
Chinese Academy of Sciences, Xiangshan Nanxincum 20, Beijing 100093, PR China

Received 24 July 2003; received in revised form 24 July 2003; accepted 8 August 2003

Abstract

Effects of short- and long-term abscisic acid (ABA) treatments on CO2 assimilation, PSII photochemistry, and the xanthophyll cycle
were investigated in maize plants during exposure to high light (1500 ␮mol m−2 s−1 ). Under non-photoinhibitory condition, both short-
and long-term ABA treatments showed no effects on PSII photochemistry and carboxylation efficiency but induced a similar decrease in
CO2 assimilation and stomatal conductance. The pool size of the xanthophyll cycle was increased in long-term ABA-treated plants but
not in short-term ABA-treated plants. When exposed to high light, there was a significant decrease in the maximal efficiency of PSII
photochemistry (Fv/Fm). However, such a decrease was less in long-term ABA-treated plants but greater in short-term ABA-treated plants
than in control plants. There was no difference in Fv/Fm between control and short-term ABA-treated plants after exposure to high light
for longer time, e.g. 60 min. Similar results were observed in the actual PSII efficiency, photochemical quenching, CO2 assimilation and
carboxylation efficiency. The xanthophyll cycle pigment contents and non-photochemical quenching (NPQ) were significantly higher but
malondialdehyde content was lower in long-term ABA-treated plants than in control plants. However, there were no significant differences in
the xanthophyll cycle pigment contents, NPQ and malondialdehyde content between control and short-term ABA-treated plants. The results
suggest that short-term ABA treatment had no effect on photoinhibition or even induced aggravated photoinhibition, while long-term ABA
treatment led to increased resistance to photoinhibition, which was associated with higher CO2 assimilation capacity and enhanced xanthophyll
cycle.
© 2003 Elsevier Ireland Ltd. All rights reserved.

Keywords: Abscisic acid; Gas exchange; Chlorophyll fluorescence; Maize (Zea mays L.); Photosynthesis; Xanthophyll cycle

1. Introduction A major physiological effect induced by ABA on plants

is the closure of stomata, which inevitably leads to a de-
Abscisic acid (ABA) is a plant growth regulator that has crease in photosynthetic CO2 assimilation. Since CO2
been identified as a messenger in stress–perception–response assimilation is the main sink for leaf absorbed light en-
pathways [1,2], such as drought [3–5], high temperature [6], ergy, a decrease in CO2 assimilation can potentially ex-
low temperature [7,8] and salinity stress [9]. Many studies pose plants to excess excitation energy, which, if not
have shown that ABA can enhance the tolerance of plants to safely dissipated, may result in photodamage to PSII be-
environmental stresses [1,10]. ABA is also involved in many cause of an over-reduction of reaction centers [17]. In-
physiological processes, such as photosynthesis. It has been deed, it has been reported that ABA-induced stomatal
demonstrated that ABA plays important roles in stomatal closure results in increased susceptibility to photodam-
movements [11,12], the regulation of photosynthetic enzyme age, which is associated with the destacking of thylakoid
activities [9,13], the stability of photosynthetic apparatus membranes and rupturing of the chloroplast envelopes
[14,15] and the gene expressions involved in chloroplasts [18].
[10,16]. However, it has been reported that ABA may protect
photosynthetic apparatus against photodamage by enhanced
xanthophyll cycle [19] and an acceleration of the recovery
∗ Corresponding author. Tel.: +86-10-62595516; of the PSII complex from photo-inactivated state [20]. Thus,
fax: +86-10-82594105. the effects of ABA on photodamage and photoprotection re-
E-mail address: [email protected] (C. Lu). main controversial [21].

0168-9452/$ – see front matter © 2003 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.plantsci.2003.08.004
1404 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410

In the present study, we investigated the effects of short- value. After photoinhibition, leaves were allowed to recover
and long-term ABA treatments on CO2 assimilation, PSII at 20 ␮mol m−2 s−1 .
photochemistry, photoinhibition and the xanthophyll cycle
in maize plants when exposed to high light. Our results
2.4. Gas exchange analysis
demonstrate that short-term ABA treatment showed no
effects on photoinhibition or even induced aggravated
An infrared gas analyzer (CIRAS-1, PP Systems, Hert-
photoinhibition, while long-term ABA treatment led to in-
fordshire, UK) was used to estimate net photosynthetic rate
creased resistance to photoinhibition when compared to
(Pn), stomatal conductance (Gs) and intercellular CO2 con-
control plants. Our results suggest that increased resistance
centration (Ci) at 800 ␮mol m−2 s−1 . External air was made
to photoinhibition induced by long-term ABA treatment
CO2 free and then pure CO2 was added to a reference con-
was associated with maintained CO2 assimilation capacity
centration of 360 ␮l l−1 . Flow rate was 200 ml min−1 and
and enhanced xanthophyll cycle.
external humidity 60–70% was used. The temperature inside
leaf chamber was maintained at 25 ◦ C. The slope of Pn–Ci
curve in the range of 0–200 ␮l l−1 was determined as the
2. Materials and methods
carboxylation efficiency of photosynthesis (CE).
2.1. Plant material
2.5. Chlorophyll fluorescence measurements
Seeds of maize (Zea mays L., Nongda 80) were
surface-sterilized by a 30 min soaking in freshly prepared Chlorophyll fluorescence measurements were made with a
solution of 3% (w/v) sodium hypochloride and then washed pulse-amplitude-modulation (PAM-2000) portable fluorom-
thoroughly with distilled water. After germinated on moist eter (Walz, Effeltrich, Germany) connected to a computer
filter paper, seeds were sown in pots containing quartz with data acquisition software (PAMWIN, Heinz, Walz).
sand and supplied with full-strength Hoagland’s solution. As described by Asada et al. [22], a multibranched fiberop-
Seedlings were grown in a greenhouse at 20–35 ◦ C under tic system connected to the PAM-2000 emitter-detector
natural daylight. unit was attached to the upper side of leaf on a leaf-clip
holder. Via the multibranched fiberoptic system, leaf in the
2.2. ABA treatments leaf-clip could be illuminated either by environmental light
or by light emitted from the PAM-2000 emitter-detector,
At the growth stage when the third leaf was fully ex- such as measuring light (MT), saturated pulse light (ST),
panded, one-third of the seedlings were used as long-term and far-red (FR) light, and in turns fluorescence signal
ABA treatment and watered once daily with Hoagland’s so- emitted from leaf could be detected simultaneously by the
lution plus 25 ␮M ABA, others were watered with normal PAM-2000 emitter-detector. The experimental protocol of
Hoagland’s solution. For short-term ABA treatment, half of fluorescence measurements was followed the description of
the seedlings watered with Hoagland’s solution only were Demmig-Adams and Adams III [23]. The minimal fluores-
surface sprayed once with 25 ␮M ABA in the evening just cence level (Fo) in dark-adapted state was measured by MT,
prior to carrying out all experiments and the rest of seedlings which was sufficiently low (<0.1 ␮mol m−2 s−1 ) not to in-
were used as control plants. In the course of experiments, duce any significant variable fluorescence. To determine the
the fourth fully expanded leaves were cut underwater and minimal fluorescence level during illumination (Fo ), a piece
their bases were immersed in water, thus water loss could be of black cloth was rapidly covered on the leaf-clip holder
avoided during photoinhibition, gas exchange and chloro- to avoid environmental light and simultaneously a 3 s FR
phyll fluorescence analyses. light (7 ␮mol m−2 s−1 ) illuminated via the multibranched
fiberoptic system to fully oxidize leaf PSII centers. The
2.3. Photoinhibitory treatments maximal fluorescence level in the dark-adapted state (Fm)
and the maximal fluorescence level during illumination
Photoinhibitory treatments were performed using a halo- (Fm ) were measured by 0.8 s ST at 3000 ␮mol m−2 s−1 .
gen lamp at 25 ◦ C. The photon flux density (PFD) reaching Steady-state fluorescence level during illumination (Fs) was
the surface of leaves was about 1500 ␮mol m−2 s−1 , which measured by MT. It should be pointed out that Fo , Fm and
was twice of photosynthesis-saturated irradiance of maize Fs were measured during illumination of 800 ␮mol m−2 s−1 .
plants, ca. 800 ␮mol m−2 s−1 . To avoid overheating and wa- The actual PSII photochemical efficiency (ΦPSII ) and
ter loss, a 5 cm deep circulating water bath was placed un- the maximal photochemical efficiency (Fv/Fm) were cal-
der the lamp and leaves were placed on the wet cheesecloth. culated as (Fm − Fs)/Fm and (Fm − Fo)/Fm, respec-
Photoinhibition was assessed by measuring the maximal effi- tively [24]. The photochemical quenching coefficient (qP)
ciency of PSII photochemistry (Fv/Fm) after high light treat- and non-photochemical quenching (NPQ) were calculated
ments. Fv/Fm was measured 30 min after the leaves were as (Fm − Fs)/(Fm − Fo ) [25] and Fm/Fm − 1 [26],
kept in the dark during which it usually reached a steady respectively.
 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410 1405

2.6. Malondialdehyde measurement 0. 9

a a a (A)

Malondialdehyde (MDA) content was determined by the c

thiobarbituric acid (TBA) reaction as described by Chen 0. 6 a
et al. [27]. Briefly, approximately 0.3 g leaf segments were
Fv/ F m

b
b
homogenized with 5 ml of 20% trichloroacetic acid (TCA) b
a a
and centrifuged at 10,000×g for 5 min. After centrifugation,
0. 3 a a
1 ml of supernatant was mixed with 4 ml 0.5% TBA and
incubated in boiling water for 30 min. Thereafter, it was
cooled to room temperature and centrifuged at 10,000 × g
0
for 5 min. Absorbance at 532 and 600 nm was determined, a (B)
a a
and MDA concentration was estimated by subtracting the 0. 6
non-specific absorption at 600 nm from the absorption at
c
532 nm using an absorbance coefficient of 156 mM−1 cm−1
at 532 nm. 0. 4 a
φ PS ΙΙ

b b

2.7. Pigment analysis a b

a
0. 2 a
a
Leaf segments were collected and frozen immediately in
liquid nitrogen. Samples were extracted in ice-cold 100%
0
acetone and the pigment extracts were filtered through a (C)
0.45 ␮m membrane filter. Pigments were separated and 0. 9 a a a

quantified by a HPLC as described by Thayer and Bjökman

[28]. c
0. 6 a
b b
qP

2.8. Statistical analysis b

a a
0. 3 a a
Statistical analysis was performed using the data obtained
from three to five independent measurements and t-test was
used to examine significant differences between control and
0
ABA-treated plants. Differences were considered significant (D)
at a probability level of P ≤ 0.05. 4
b

3 b
a a
3. Results
NPQ

a a
2 b
3.1. Effect of ABA on chlorophyll fluorescence
a a
parameters under high light 1
a a a
Fig. 1 shows the changes in fluorescence parameters in
0
control and ABA-treated plants after exposure to high light 0 30 60 90
(1500 ␮mol m−2 s−1 ) up to 90 min. High light led to a signif- Photoinhibition treatment (min)

icant decrease in the maximal efficiency of PSII photochem- Fig. 1. Changes in the maximal efficiency of PSII photochemistry (Fv/Fm,
istry (Fv/Fm) in both control and ABA-treated plants. How- A), the actual PSII efficiency (ΦPSII , B), the photochemical quenching co-
ever, Fv/Fm values were significantly higher in long-term efficient (qP, C) and non-photochemical quenching (NPQ, D) during expo-
ABA-treated plants than in control plants. In contrast, Fv/Fm sure to high light (1500 ␮mol m−2 s−1 ) in control plants (white columns),
short-term ABA-treated plants (gray columns) and long-term ABA-treated
was significantly lower in short-term ABA-treated plants
plants (black columns). Data are mean±S.E. of five independent measure-
than in control plants after exposure to high light for 30 min. ments. Values indicated with different letters were significantly different
No significant differences in Fv/Fm between control and at P = 0.05.
short-term ABA-treated plants were observed after exposure
to high light for longer time, e.g. 60 and 90 min (Fig. 1A).
Similar results were observed in the actual PSII efficiency control and short-term ABA-treated plants while NPQ was
(ΦPSII ) and the photochemical quenching coefficient (qP) significantly higher in long-term ABA-treated plants than in
(Fig. 1B and C). On the other hand, non-photochemical control plants.
quenching (NPQ) increased significantly during photoinhi- Fig. 2 shows the time courses of recovery of Fv/Fm
bition (Fig. 1D). There was no difference between NPQ in in control and ABA-treated plants after exposure to high
1406 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410

light for 30, 60 and 90 min, respectively. After 30 min pho- plants. There was no significant difference in the recovery
toinhibitory treatment, the decrease in Fv/Fm was fully rate of Fv/Fm between control and short-term ABA-treated
recovered in 60 min either in control and ABA-treated plants. However, the recovery rate of Fv/Fm in long-term
plants. Long-term ABA-treated plants showed a fast recov- ABA-treated plants was faster than in control plants (Fig. 2B
ery in Fv/Fm, followed by control plants and short-term and C).
ABA-treated plants (Fig. 2A). After exposure to high light
for longer time, e.g. 60 and 90 min, the recovery of Fv/Fm 3.2. Effect of ABA on gas exchange parameters
was slow and small either in control plants or in ABA-treated under high light

Fig. 3 shows the changes in gas exchange parameters

0.9 in control and ABA-treated plants during photoinhibi-
(A)
tion. Under non-photoinhibitory condition, both short- and
long-term ABA treatments resulted in a similar decrease in
photosynthetic rate (Pn) and stomatal conductance (Gs) but
0.6 had no effects on intercellular CO2 concentration (Ci) and
carboxylation efficiency (CE), suggesting that the decreased
Fv/Fm

Pn induced by ABA treatments was associated with the

decreased Gs. Pn decreased significantly during photoinhi-
0.3 bition (Fig. 3A). However, the decrease in Pn was much less
in long-term ABA-treated plants than in control plants. After
exposure to high light for 60 and 90 min, there was no dif-
ference in Pn between control and short-term ABA-treated
0 plants while the decrease in Pn was greater in short-term
0 30 60 90 120 150
0.9
ABA-treated plants than in control plants after exposure to
(B) high light for 30 min (Fig. 3A). Similar results were observed
in the changes in CE during high light treatment (Fig. 3D).
Gs increased during high light treatment (Fig. 3B). Gs was
0.6
lower in ABA-treated plants than in control plants. There
was no difference in Gs between long-term and short-term
ABA-treated plants after exposure to high light for 60 and
Fv/Fm

90 min while Gs was higher in long-term ABA-treated

plants than in short-term ABA-treated plants after exposure
0.3
to high light for 30 min (Fig. 3C). Ci increased during high
light treatment and such an increase was greater in control
plants than in long-term ABA-treated plants. After expo-
sure to high light for 60 and 90 min, no difference in Ci
0
0 30 60 90 120 150 180 was observed between control and short-term ABA-treated
0.9
(C) plants. However, after exposure to high light for 30 min, Ci
was higher in short-term ABA-treated plants than in control
plants.
0.6
3.3. Effect of ABA on photoinhibition in the presence
of sodium bicarbonate
Fv/Fm

In order to examine whether photoinhibition occurred

0.3
in short- and long-term ABA-treated plants was due to
stomatal closure induced by ABA treatment or not, the
effect of ABA on photoinhibition was investigated in the
presence of sodium bicarbonate (Fig. 4). When leaves were
0
0 30 60 90 120 150 180 210
floated on 10 mM NaHCO3 solution after vacuum infil-
Photoinhibition/recovery time (min) trated, CO2 supply was sufficient to overcome the stomatal
closure [29]. Thus, the difference in stomatal closure be-
Fig. 2. Changes in the maximal efficiency of PSII photochemistry (Fv/Fm)
tween control and ABA-treated plants could disappear.
in control plants (䊉), short-term ABA-treated plants (䊊) and long-term
ABA-treated plants (䉲) during exposure to 1500 ␮mol m−2 s−1 for 30 min After exposure to high light for 30 min, Fv/Fm was higher
(A), 60 min (B) and 90 min (C) and recovery. Arrows indicate starting in long-term ABA-treated plants but lower in short-term
point for recovery. Data are mean±S.E. of five independent measurements. ABA-treated plants than in control plants when leaves were
 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410 1407

25 0.9
(A)
a
20 b b
Pn (µmol CO2 m-2 s-1)

b
c
0.6
a a a
15
Fv/Fm

c b

10 a

b 0.3
b
5 a b
a
a a
0
(B) 0
200 (A) (B)
a a
a
b Fig. 4. Changes in the maximal efficiency of PSII photochemistry (Fv/Fm)
Gs (mmol m-2 s-1)

150 after exposure to high light (1500 ␮mol m−2 s−1 ) for 30 min in control
b b b
c plants (white columns), short-term ABA-treated plants (gray columns) and
a
b
long-term ABA-treated plants (black columns): (A) leaves were placed
100 b b on wet cheesecloth; (B) leaves were floated on 10 mM NaHCO3 solu-
tion after vacuum infiltrated. Data are mean ± S.E. of five independent
measurements. Values indicated with different letters were significantly
different at P = 0.05.
50

0
(C) placed on wet cheesecloth. However, when leaves were
floated in 10 mM NaHCO3 , no decrease in Fv/Fm was
450 a a
a a
observed in short-term ABA-treated plants but the higher
b b Fv/Fm still maintained in long-term ABA-treated plants.
b
These results suggest that aggravated photoinhibition in
Ci (µl l-1)

a ac
300 a short-term ABA-treated plants was mainly resulted from
a a
ABA-induced stomatal limitation, while increased resis-
tance to photoinhibition in long-term ABA-treated plants
150 was not due to ABA-induced stomatal limitation but due to
other non-stomatal processes induced by long-term ABA
treatment.
0
(D)
0.3 3.4. Effect of ABA on the xanthophyll cycle pigments
a under high light
a a

b Effect of ABA treatments on the pigment composition

0.2 a a of the xanthophyll cycle during photoinhibition is shown
CE

in Fig. 5. Under non-photoinhibitory condition, short-term

ABA treatment had no effect on the pool size of the xan-
0.1 b thophyll cycle while long-term ABA treatment resulted
a
a
b in an increase in the pool size of the xanthophyll cycle,
a which was due to an increase in the content of violaxan-
a
thin. Under high light condition, the content of zeaxanthin
0
0 30 60 90 increased significantly while that of violaxanthin decreased
Photoinhibition treatment (min) significantly. However, the pool size of the xanthophyll
cycle was significantly greater in long-term ABA-treated
Fig. 3. Changes in CO2 assimilation (Pn, A), stomatal conductance (Gs, plants than in control and such a greater increase was
B), intercellular CO2 concentration (Ci, C) and carboxylation efficiency
due to higher contents of violaxanthin, antheraxanthin and
(CE, D) during exposure to high light (1500 ␮mol m−2 s−1 ) in control
plants (white columns), short-term ABA-treated plants (gray columns) zeaxanthin. There was no significant difference in the pool
and long-term ABA-treated plants (black columns). Data are mean ± S.E. size of the xanthophyll cycle and the pigment composi-
of five independent measurements. Values indicated with different letters tion between control plants and short-term ABA-treated
were significantly different at P = 0.05. plants.
1408 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410

80 9
b (A)
b
b a a
a a a a
V+A+Z (mmol mol-1Chl)

60 b
MDA (µmol g-1FW)

a
a 6
b
aa
a
40 a
b

3
20 a a
a a a a

0 0
(B) 0 30 60 90
60 b
Photoinhibition treatment (min)
a a
Fig. 6. Changes in the content of malondialdehyde (MDA) during expo-
V (mmol mol-1Chl)

45 sure to high light (1500 ␮mol m−2 s−1 ) in control plants (white columns),
short-term ABA-treated plants (gray columns) and long-term ABA-treated
plants (black columns). Data are mean±S.E. of five independent measure-
30 ments. Values indicated with different letters were significantly different
b at P = 0.05.
a a b
15 b
a a 3.5. Effect of ABA on lipid peroxidation
a a under high light
0
(C) Fig. 6 shows the changes in the content of MDA in con-
8
trol and ABA-treated plants during high light treatment.
There were no significant changes in MDA contents after
b
A (mmol mol-1Chl)

6 a a a b
30 min photoinhibition. However, a significant increase in
a
a b MDA levels was observed after exposure to high light for
a a 60 and 90 min. Such an increase was much less in long-term
4 a ABA-treated plants than in control plants. There were no
a
significant differences in the content of MDA between con-
trol and short-term ABA-treated plants.
2

0 4. Discussion
60 (D)
b
b The results in this study clearly show that the effects
of short- and long-term ABA treatments on photoinhibition
Z (mmol mol-1Chl)

45 b
a a were different. Short-term ABA treatment led to aggravated
photoinhibition after exposure to high light for 30 min and
a a
30
this negative effect disappeared when exposed to high light
a
a
for longer time, e.g. 60 and 90 min (Fig. 1A). Our results
suggest that this photoinhibition was not due to photodam-
15 age since this aggravated photoinhibition could be rapidly
a
a a and fully recovered and was reversible (Fig. 2A) and there
was no change in MDA level (Fig. 6). A significant increase
0
0 30 60 90
in NPQ and the content of zeaxanthin after exposure to high
Photoinhibition treatment (min) light for 30 min indicate that this aggravated photoinhibition
was associated with the photoprotective processes (Figs. 1D
Fig. 5. Changes in the pool size of the xanthophyll cycle pigment and 5D) [17,30,31]. Our results further indicate that this ag-
(V+A+Z, A), the contents of violaxanthin (V, B), antheraxanthin (A, C),
and zeaxanthin (Z, D) during exposure to high light (1500 ␮mol m−2 s−1 )
gravated photoinhibition was associated with the stomatal
in control plants (white columns), short-term ABA-treated plants (gray closure induced by ABA treatment (Fig. 4).
columns) and long-term ABA-treated plants (black columns). Data are On the other hand, our results show that long-term ABA
mean ± S.E. of five independent measurements. Values indicated with treatment induced higher resistance to photoinhibition
different letters were significantly different at P = 0.05. (Fig. 1). When exposed to short-term photoinhibition, i.e.
 H. Jia, C. Lu / Plant Science 165 (2003) 1403–1410 1409

30 min, this kind of photoinhibition was due to photoprotec- long-term ABA-treated plants than in control plants suggest
tive processes but not to photodamage, since the decrease that xanthophyll cycle-dependent energy dissipation induced
in Fv/Fm was fully recovered (Fig. 2A) and there were no by long-term ABA treatment may also play an important role
changes in MDA level (Fig. 6) but there were significant in- in protecting photosynthetic apparatus against photodamage
creases in NPQ and the content of zeaxanthin (Figs. 1D and under high light.
5D) [17,30,31]. When exposed to long-term photoinhibi- It has been shown that the antioxidant systems can
tion, e.g. 60 and 90 min, the facts that the recovery rate scavenge the reactive species of oxygen that is produced
of Fv/Fm was slow and small and there was a significant during photoinhibition and protect photosynthetic appara-
increase in MDA level (Figs. 2B and C, and 6) suggest that tus against photodamage [40]. It has been reported that the
photoinhibition indicated by the decrease in Fv/Fm was activities of antioxidant enzymes, such as superoxide dis-
associated with photodamage. However, we also observed mutase, ascorbate peroxidase and glutathione redutase, are
that NPQ and the content of zeaxanthin increased signifi- enhanced by ABA treatment [41–44]. Therefore, it is also
cantly (Figs. 1D and 5D). Since the slowly recovering NPQ possible that the increased resistance to photodamage in
and the sustained zeaxanthin can make contributions to the long-term ABA-treated plants was associated with increased
decreased Fv/Fm [32], our results suggest that the decreased antioxidant metabolism induced by ABA, which scavenges
Fv/Fm under long-term photoinhibition may also be partly the reactive species of oxygen and protects photosynthetic
associated with protective processes. apparatus from photodamage.
How does long-term ABA treatment induce increased
resistance to photoinhibition in maize plants? It is well
known that photoinhibition occurs whenever the absorbed Acknowledgements
light energy exceeds the capacity of the plants to use the
trapped energy through photosynthetic electron transport. We are grateful for the financial support by the Program
When excess light energy is not dissipated, PSII will be of 100 Distinguished Young Scientists of Chinese Academy
over-reduced and reactive species of oxygen, such as sin- of Sciences, the State Key Basic Research and Development
glet oxygen (1 O2 ) and superoxide anion (O2 − ), will be pro- Plan of China (G1998010100) to C. Lu.
duced, which causes photodamage on photosynthetic appa-
ratus [33]. Since CO2 assimilation is the main sink to utilize
absorbed light and is the primary means of protection against
photoinhibition [34,35], obviously high CO2 assimilation References
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