Download Leaf orientation, photorespiration and xanthophyll cycle protect

Environmental and Experimental Botany 55 (2006) 87–96
Leaf orientation, photorespiration and xanthophyll cycle protect
young soybean leaves against high irradiance in field
Chuang-Dao Jiang a , Hui-Yuan Gao b,∗ , Qi Zou b , Gao-Ming Jiang a , Ling-Hao Li a
a
Laboratory of Quantitative Vegetation Ecology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, PR China
b Department of Plant Science, Shandong Agricultural University, Taian 271018, PR China
Accepted 6 October 2004
Abstract
In order to fully understand the adaptive strategies of young leaves in performing photosynthesis under high irradiance, leaf
orientation, chloroplast pigments, gas exchange, as well as chlorophyll a fluorescence kinetics were explored in soybean plants.
The chlorophyll content and photosynthesis in young leaves were much lower than that in fully expanded leaves. Both young and
fully expanded leaves exhibited down-regulation of the maximum quantum yield (FV /FM ) at noon in their natural position, no
more serious down-regulation being observed in young leaves. However, when restraining leaf movement and vertically exposing
the leaves to 1200 ␮mol m−2 s−1 irradiance, more pronounced down-regulation of FV /FM was observed in young leaves; and the
actual photosystem II (PS II) efficiency (ФPSII ) drastically decreased with the significant enhancement of non-photochemical
quenching (NPQ) and ‘High energy’ quenching (qE ) in young leaves. Under irradiance of 1200 ␮mol m−2 s−1 , photorespiration
(Pr ) in young leaves measured by gas exchange were obviously lower, whereas the ratio of photorespiration/gross photosynthetic
rate (Pr /Pg ) were higher than that in fully expanded leaves. Compared with fully expanded leaves, young leaves exhibited
higher xanthophyll pool and a much higher level of de-epoxidation components when exposure to high irradiance. During leaf
development, the petiole angle gradually increased all the way. Especially, the midrib angle decreased with the increasing of
irradiance in young leaves; however, no distinct changes were observed in mature leaves. The changes of leaf orientation greatly
reduced the irradiance on young leaf surface under natural positions. In this study, we suggested that the co-operation of leaf
angle, photorespiration and thermal dissipation depending on xanthophyll cycle could successfully prevent young leaves against
high irradiance in field.
© 2004 Elsevier B.V. All rights reserved.
Keywords: Photosynthetic rate; Chlorophyll a fluorescence; Photorespiration; Xanthophyll cycle; Leaf orientation; Soybean
Abbreviations: A, antheraxanthin; Chl, chlorophyll; F0 , minimal fluorescence in dark-adapted state; FM , maximum fluorescence in darkadapted state; FV , maximum variable fluorescence in dark-adapted state (=FM −F0 ); FV /FM , maximum quantum yield of photosystem II; FS ,
, maximum fluorescence in ligh-adapted state; F , maximum variable fluorescence in light-adapted
steady-state fluorescence under irradiance; FM
V
− F ); PFD, photon flux density; P , net photosynthetic rate; P , gross photosynthetic rate; P , photorespiration; PSII, photosystem
state (=FM
n
g
r
0
II; ФPSII , the actual PSII efficiency under irradiance; NPQ, non-photochemical quenching; qE , the fast relaxing component of non-photochemical
quenching; V, violaxanthin; Z, zeaxanthin
∗ Corresponding author. Tel.: +86 538 8241341; fax: +86 538 8249608.
E-mail address: [email protected] (H.-Y. Gao).
0098-8472/$ – see front matter © 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.envexpbot.2004.10.003
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C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
1. Introduction
During leaf development, the newly initiating leaves
are often exposed to full sunlight at the topmost canopy,
indicating that those young leaves have to endure extremely high irradiance. However, young leaves have
lower photosynthesis activity per unit area compared
with fully developed leaves (Krause et al., 1995; Choinski et al., 2003). These will inevitably result in more
excessive excited energy in young leaves. It is well
known that too much light can lead to largely increased
production of damaging reactive oxygen as byproducts
of photosynthesis, during which photosynthetic rate is
depressed (Osmond, 1994; Müller et al., 2001). In extreme cases, reactive oxygen can cause pigment bleaching and death. Such is the case well known to anyone
who tries to move a houseplant outdoors into full sunlight (Osmond, 1994; Müller et al., 2001). Therefore, it
is a great challenge for young leaves to be subjected to
strong irradiance. Nevertheless, plants have developed
a number of strategies to balance the captured light
energy, thereby protecting photosynthetic apparatus
against photodamage (Anderson et al., 1997).
Photorespiration provides an effective electron sink
when CO2 assimilation is low (Kozaki and Takeba,
1996). It is well documented that photorespiration protects leaves against high irradiance through not only
acting as a sink for reducing equivalents but also preventing over-reduction of the electron carriers between
PS II and PS I (Kozaki and Takeba, 1996; Osmond
and Grace, 1995). However, there were few studies
focusing on changes of photorespiration during leaf
expansion.
Thermal dissipation of excess irradiance measured
as non-photochemical quenching (NPQ) is believed to
be of paramount importance in the protection of the
photosynthetic apparatus against the deleterious effects
of excess light. It has been known for many years that at
least two main components of NPQ can be resolved by
analyzing its dark relaxation kinetics, the rapidly relaxing component (qE ) and the slowly reversible component (often termed qI ). qE , the rapidly relaxing component of NPQ is considered to be an important photoprotective mechanism to cope with excessive irradiance
(Björkman and Demmig, 1987; Müller et al., 2001).
The value of qE is always associated with pH gradient
across the thylakoid membrane (Briantais et al., 1980)
and the formation of the xanthophyll cycle pigments,
zeaxanthin (Z) and antheraxanthin (A) (Björkman and
Demmig, 1987). All organisms that exhibit qE have a
xanthophyll cycle (Müller et al., 2001). For the last few
years, many investigators have paid special attentions
to the role of xanthophyll cycle under conditions of
cold-temperature stress (Verhoeven et al., 1999), water
stress (Munné-Bosch and Alegre, 2000), and nutrition
deficiency (Verhoeven et al., 1997; Jiang et al., 2001;
Jiang et al., 2002). Just recently, some people have further explored the characteristics of xanthophyll cycle
pigments and excited energy dissipation in senescence
leaves (Munné-Bosch et al., 2001; Lu et al., 2001; Lu
et al., 2003). Specifically, a few physiologists argued
that xanthophyll cycle pigments and excited energy dissipation were enhanced in young leaves so that the
photosynthetic apparatus could be protected (Krause
et al., 1995; Yoo et al., 2003). However, such question is still in debate (Ögren, 1991; Krause et al., 1995;
Bertamini and Nedunchezhian, EEB1511BIB312003).
In all these studies, we noticed that detached and almost
fully expanded leaves were chosen to explore xanthophyll cycle. Under field conditions, can these mechanisms successfully protect young leaves against high
irradiance at the early development stages?
Some authors also noticed that leaves, especially
some leguminous plants, can change their orientation
by inclining upwards and downwards under higher
irradiance, thereby minimizing the interception of
irradiance for avoiding photodestruction (Gamon and
Pearcy, 1989; Ögren and Evan, 1992; Björkman and
Demmig-Adams, 1995; James and Bell, 2000; Feng
et al., 2002). We wonder whether or not leaf orientations plays a more important role in newly initiating
leaves than that in fully developed ones when leguminous plants are subjected to strong irradiance.
The objective of this study is to explore how young
soybean leaves cope with high irradiance under field
conditions, and whether the co-operation of leaf orientation, photorespiration and xanthophyll cycle could
effectively protect young leaves against strong sunlight
in field.
2. Materials and methods
2.1. Plant materials
Soybean (Glycine max L.) plants were grown in ten
plastic pots (22 cm in diameter and 30 cm in height) at
C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
89
the beginning of May. The plants grown in pots were
placed in field subjected to natural solar radiation, with
a daily maximum photosynthetic photon flux density
(PPFD) of above 1600 ␮mol m−2 s−1 , and the maximum air temperature was about 33 ◦ C. The soybean
plants were thinned to one plant per pot 2 weeks after
sowing. Nutrients and water were supplied sufficiently
throughout, to avoid potential nutrients and drought
stresses. After growing for 5 weeks, newly expanding
leaves with an area of about 33% of fully expanded
leaves (33% A), near fully expanded leaves with an
area of about 78% of fully expanded leaves (78% A)
and fully expanded leaves (100% A) were studied in
the experiments. Generally, three leaves (33% A, 78%
A and 100% A) of each plant were used in the different measurements, and at least three replications were
made.
In the experiments carried out in open field, all
leaves were kept in their natural positions. While in
the experiments performed in the laboratory, attached
leaves were restrained in horizontal positions using
flexible wire and vertically illuminated by a man-made
lamp (Philips HPLR 400 W). Between the lamp and
leaves, a water bath with flowing water was used to
keep temperature in steady.
ech, UK). The maximum quantum yield of photosystem II (FV /FM ) was determined in dark-adapted
(15 min) samples. After the initial Chl fluorescence
yield (F0 ) was determined in low modulated measuring light, a 0.7-s pulse of saturating white light
(>3000 ␮mol m−2 s−1 ) was applied to obtain the maximum Chl fluorescence yield (FM ) and the FV /FM
(FV , the variable Chl fluorescence yield, is defined as
FM −F0 ). The steady-state fluorescence level (FS ) and
) during expothe maximum Chl fluorescence level (FM
sure to illumination were also measured, respectively.
The fluorescence transient was induced by continuous light (1200 ␮mol m−2 s−1 ) for 2 h. While the photochemical fluorescence-quenching coefficient (qP )
and non-photochemical quenching (NPQ) were discriminated by applying saturating pulses after every
30 min of the continuous light treatment.
The actual PS II efficiency (ФPSII ) was calcu −F )/F (Genty et al., 1989), and nonlated as (FM
S
M
−1 (Bilger
photochemical quenching (NPQ) as FM /FM
and Björkman, 1990). NPQ was resolved into fast
relaxing (qE ) and slowly relaxing (qI ) components by
extrapolation in semi-logarithmic plots of the maximum fluorescence yield versus time as described by
Johnson et al. (1993).
2.2. Measurement of photosynthetic rate
2.4. Pigment analysis
Photosynthetic rate–Photosynthetic photon flux
density (Pn –PFD) response curves were made at leaf
chamber temperature of 30 ◦ C, and at 350 ␮mol mol−1
CO2 with a portable photosynthetic system (CIRAS1, PP systems, UK). PFD was fixed every 10 min in
a sequence of 2000, 1600, 1200, 800, 600, 400, 300,
200, 150, 100, 0 ␮mol m−2 s−1 . Light intensity, CO2
concentration and leaf chamber temperature were controlled by automatic control device of the CIRAS-1
photosynthetic system. Photosynthetic rate measured
at two O2 concentrations (21% O2 + 350 ␮mol mol−1
CO2 and 2% O2 + 350 ␮mol mol−1 CO2 ) under
1200 ␮mol m−2 s−1 PFD was used to calculate photorespiration.
The leaf chlorophyll and carotenoid were extracted
with 80% acetone, with the extracts being analyzed
with a UV-120 system (Shimadzu, Japan) according to Arnon (1949). Then the carotenoid components of xanthophyll cycle were determined, according
to the method developed by Thayer and Björkman
(1990). After dark adaptation for 12 h, leaves were
all horizontally exposed to a strong irradiance of
1200 ␮mol m−2 s−1 for 0, 1, 2 h, respectively. Afterwards, they were quickly frozen in liquid nitrogen.
Latter, leaf samples were extracted with 85% acetone.
Content of the pigments were estimated by applying
the conversion factors for peak area to nmol as determined for this solvent mixture by Thayer and Björkman
(1990).
2.3. Measurement of chlorophyll fluorescence
parameters
2.5. Measurement of leaf orientation
In vivo chlorophyll fluorescence was measured
using a pulse-modulated fluorimeter (FMS-2, Hansat-
A petiole angle is the angle of branch to which leaves
are attached and a midrib angle is defined as the devia-
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C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
tion of the midrib from vertical. Both leaf angles were
investigated using a clinometer (PM-5/360 PC, Suunto
Co., Finland). The midrib angle was measured at both
sunny and cloudy days to exclude the rhythmical movement.
and 3.59 ± 0.11 in 100% A, respectively. Such a result
indicates that the increase magnitude of Chl a was much
higher than that of Chl b during leaf development.
3.2. Changes of photosynthesis and
photorespiration
2.6. Statistical analysis
Data of measurements were inputted into Microsoft
Excel 2000 spreadsheet, and each value of mean and
S.E. in the figures represents 3–6 replications of measurements. And data were subjected to analysis of
variance using SPSS (10.0 for Windows). The least
significant differences between the means were estimated at 95% confidence level. Plots and fit curves were
performed using SigmaPlot 2000 and Microsoft Excel
2000. Unless otherwise indicated, significant differences among different leaf types are given at P < 0.05.
3. Results
Fig. 2 shows the photosynthesis–photosynthetic
photon flux density (Pn –PFD) response curves during leaf development. The maximum assimilation
rates under saturation photon flux density were
5.1 ± 0.43 ␮mol m−2 s−1 , 10.2 ± 0.5 ␮mol m−2 s−1
and 16.7 ± 0.46 ␮mol m−2 s−1 in 33% A, 78% A,
100% A leaves, respectively. Obviously, young leaves
exhibited lower CO2 assimilation capacity than that of
fully expanded ones. Young leaves also showed lower
saturation light of photosynthetic rate (SLP) (Fig. 2). In
parallel with the lower CO2 assimilation capacity, the
photorespiration (Pr ) in young leaves was also lower
(Fig. 3), whereas the ratio of photorespiration/gross
photosynthetic rate (Pr /Pg ) in young leaves was higher
than that in fully expanded leaves (Fig. 3).
3.1. Changes in chlorophyll content
Chlorophyll (Chl) contents per unit area in young
leaves (33 and 78% expanded) were significantly lower
than that in fully expanded ones (Fig. 1). Chl a/Chl b
ratios were 2.20 ± 0.07 in 33% A, 3.06 ± 0.12 in 78% A
Fig. 1. Changes of chlorophyll pigments during the development of
soybean leaves. The newly expanding leaves with an areas of about
33% of fully expanded leaves (33% A), near fully expanded leaves
with an areas of about 78% of fully expanded leaves (78% A) and
fully expanded leaves (100% A) were studied in the experiment.
Values are means ± S.E., n = 3.
3.3. Changes of the maximum PS II quantum yield
under high irradiance
The maximum PS II quantum yield (FV /FM ) after
full dark-adaptation were 0.78 ± 0.01, 0.81 ± 0.01
Fig. 2. Typical light response curves of different expanding soybean
leaves measured in ambient CO2 (about 350 ␮mol/mol) at leaf chamber temperature of 30 ◦ C. (䊉), () and () represent fully expanded
leaves (100% A), almost fully expanded leaves (78% A) and just initiated leaves (33% A), respectively. Values are means ± S.E., n = 3–5.
C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
91
Fig. 3. Changes of photorespiration (Pr ) and the ratio of photorespiration to gross photosynthetic rate (Pr /Pg ) during expansion of
soybean leaves under 1200 ␮mol m−2 s−1 irradiance measured at leaf
chamber temperature of 30 ◦ C. Values are means ± S.E., n = 4.
and 0.84 ± 0.01 in 33% A, 78% A and 100% A
leaves, respectively (Fig. 4A). When leaf movements
were restrained and vertically subjecting leaves to
1200 ␮mol m−2 s−1 irradiance, young leaves were
more susceptible to strong light than mature ones, as
indicated by the more pronounced decrease in FV /FM
ratios in young leaves; when the light was turned off,
the values of FV /FM were almost completely restored
in 1 h in the three leaf types (Fig. 4A). However, there
were no appreciable differences in FV /FM (P > 0.05)
at noon when all leaves in their natural positions
were exposed to full sun light in field condition
(Fig. 4B).
3.4. Regulation of PS II photochemistry under
high irradiance
As shown in Fig. 5A, a general decline in ФPSII was
observed upon exposure to high irradiance, but the fully
expanded leaves remained substantially higher ФPSII
than others. In young leaves, a significant decrease
of ФPSII together with a marked increase in nonphotochemical quenching (NPQ) occurred (Fig. 5B).
Meanwhile, NPQ in young leaves was dramatically
higher compared with mature ones (Fig. 5B). To estimate the contribution of qE , the dark relaxation kinetics
of fluorescence in the three leaf types were analyzed.
Clearly, qE was significantly greater in young leaves
than that in mature ones (Fig. 5C).
Fig. 4. (A) Changes of the maximum efficiency of PS II photochemistry (FV /FM ) in different expanding soybean leaves under
1200 ␮mol m−2 s−1 irradiance and the dark recovery courses measured in ambient CO2 (about 350 ␮mol/mol) at room temperature
(25–30 ◦ C). Attached leaves were kept vertically to the irradiance.
(B) Changes of the maximal efficiency of PS II photochemistry
(FV /FM ) in different expanding soybean leaves in field. Attached
leaves were all kept in natural positions and measured in ambient
CO2 (about 350 ␮mol/mol). Values are means ± S.E., n = 4–6.
Xanthophyll cycle pigments, which are closely correlated with energy dissipation, were also analyzed. On
chlorophyll basis, the xanthophyll cycle pool size was
significantly higher in young leaves than that in fully
expanded leaves (Fig. 6A). And the de-epoxidation
components of the xanthophyll cycle pigments were
much more enhanced in young leaves than that in
fully expanded leaves when vertically exposed to
1200 ␮mol m−2 s−1 irradiance for 1 and 2 h, respectively (Fig. 6B and C).
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C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
Fig. 6. (A) Changes of xanthophyll cycle pigment pool size, (B)
the de-epoxidation components per Chl, and (C) the de-epoxidation
level at various developmental stages of soybean leaves in dark and
vertically exposed to 1200 ␮mol m−2 s−1 irradiance for 1 and 2 h,
respectively. Values are means ± S.E., n = 4.
Fig. 5. Changes of (A) actual photosystem II efficiency (ФPSII ), (B)
non-photochemical quenching (NPQ) and (C) ‘high-energy’ fluorescence quenching (qE ) in different expanding soybean leaves under
1200 ␮mol m−2 s−1 irradiance measured in ambient CO2 (about
350 ␮mol/mol) at room temperature (25–30 ◦ C). Attached leaves
were kept vertically to the irradiance. Values are means ± S.E.,
n = 3–4.
3.5. Changes in leaf angle and irradiance on leaf
surface
Fig. 7 showed that petiole angles were smaller in
young leaves than that in mature ones. At dawn or
sunset, the midrib angles of all the three leaf types
were almost the same. However, the angles in young
leaves were significantly reduced at noon on clear days
(Fig. 8A). Noticeably, no appreciable diurnal variation
C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
Fig. 7. Changes of petiole angle during various developmental stages
of soybean leaves in field. Values are means ± S.E., n = 6.
93
Fig. 9. Typical daily changes of irradiance on leaf surface at various
developmental stages of soybean leaves on clear day in field. Values
are means ± S.E., n = 6.
(P > 0.05) was noted on cloudy day (Fig. 8B). Obviously, it is the light rather than rhythmical movement
that induced the change of midrib angle. We also noted
that the changes of leaf orientation under high irradiance in young leaves were steeper than that in fully
expanded ones (Figs. 7 and 8). Among the three leaf
types, mature leaves received the greatest amount of
daily irradiance on leaf surface, and had a large peak
of irradiance at noon (Fig. 9). Along with the development of soybean leaves, it was the changes in leaf angle
that resulted in the increase of intercepted photon flux
density.
4. Discussion
4.1. Development of photosynthetic apparatus and
changes of leaf orientation
Fig. 8. Changes of midrib angle in different expanding soybean
leaves on clear day (A) and cloudy day (B) in field. Values are
means ± S.E., n = 6.
The increase of chlorophyll content and Chl a/Chl
b ratio with the process of leaf expansion indicated
a gradual development of photosynthetic apparatus
(Fig. 1), which was supported by the increase of photosynthetic rate with the leaf expansion (Fig. 2), so that
more excited energy would be utilized in CO2 assimilation rather than dissipated with the process of leaf
expansion.
It was reported that FV /FM could represent original
activity of PS II (Hulsebosch et al., 1996). However,
high FV /FM was observed among the three leaf types
(Fig. 4A) indicating that young leaves had almost the
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C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
same activity of primary charge separation as that in
mature leaves. It is thus deduced that the activity of PS
II might not be the limiting step of the photosynthesis
in young leaves.
Young leaves had a more vertical leaf orientation
than mature leaves (Figs. 7 and 8) indicating that the
mature leaves can effectively intercept more irradiance
than young leaves under filed conditions. Considering
that with the development of photosynthetic apparatus
and increase of CO2 assimilation capacity, more and
more irradiance capture is needed to promote photosynthesis, the change of leaf angle is an adaptation to
intercept irradiance during leaf expansion.
4.2. Development of photoprotective mechanisms
during leaf expansion
It has been widely known that leaves developed
several regulation mechanisms to protect themselves
against high irradiance, thus can efficiently balance the
light capture and utilization (Osmond, 1994). Data in
this study revealed that young leaves that did not have
accomplished photosynthetic apparatus ad already had
efficient mechanisms to consume excited energy captured by light harvesting complexes (Figs. 3 and 5)
except carbon assimilation.
Foyer and Noctor (2000) reported that photorespiration acts as a route for energy consumption in C3
plant; Kozaki and Takeba (1996) also demonstrated
that photorespiration plays a key role in the protection
of leaves against over reduction and uses energy when
CO2 assimilation is restricted. The pronounced higher
ratio of Pr /Pg in young leaves (Fig. 3) implies that relative more excited energy captured by light harvesting
complexes was allocated to photorespiration in young
leaves. Increased allocation of excited energy to photorespiration can effectively maintain linear electron
transport and utilization of excited energy by allowing
metabolism to continue using the products of photosynthetic electron transport (Osmond and Grace, 1995;
Foyer and Noctor, 2000), mitigating deleterious effects,
such as photodestruction during the initial stages of leaf
expansion.
The lower ФPSII in young leaves under controlled
conditions indicates that less light energy was utilized
in photochemical reaction than that in mature ones
(Fig. 5A) so that much more excessive energy was produced in young leaves. In fact, much more excessive
energy was dissipated in young leaves (Fig. 5B), which
was also supported by the fact that young leaves had
larger qE , one of the major components of NPQ, than
the mature leaves under the same irradiance (Fig. 5C).
Some authors reported that qE is promoted by the formation of the xanthophyll pigments zeaxanthin (Z) and
antheraxanthin (A) (Demmig-Adams, 1990; Gilmore,
1997). We noticed that much more de-epoxidation
components were produced in young leaves than that
in fully expanded ones when exposed to irradiance
(Fig. 6B and C), which was in accordance with the
change of qE . Additionally, it is believed that Z might
act as an important antioxidant, which can directly
deactivate 1 O2 and also quench the excited triplet state
of chlorophyll in the thylakoid membrane under high
irradiance (Havaux and Niyogi, 1999; Havaux et al.,
2000). The higher content of xanthophyll cycle pigments per Chl and the higher de-epoxidation state of
xanthophylls [(A + Z)/(V + A + Z)]% in young leaves
might be a strengthened acclimation to cope with
excess irradiance during the initial stages of leaf expansion to excess irradiance (Fig. 6B and C). The reversible
changes of FV /FM in young leaves revealed that photoprotective mechanisms in young leaves worked well to
avoid photodestruction to the photosynthetic apparatus
under excessive irradiance (Fig. 4A and B).
4.3. Changes of leaf orientation alleviate high
light stress in young leaves
Data in the present study demonstrated that young
leaves have timely developed photoprotective mechanisms, such as: photorespiration, xanthophylls cycle, to
cope with high irradiance. Significant down-regulation
in FV /FM in young leaves when vertically exposed to
high irradiance reflected that young leaves were more
susceptible to high irradiance (Fig. 4A). Additionally,
when FV /FM measured during daily courses were plotted as a function of irradiance (Fig. 10), it was also
noticed that young leaves were more susceptible to high
irradiance than mature ones in field.
Theoretically, horizontal leaves receive more irradiance on leaf surface than steep ones (Ögren and Evan,
1992; James and Bell, 2000). Obviously, the changes
in petiole angle and midrib angle kept young leaves
in more vertical positions than fully expanded leaves
(Figs. 7 and 8), enabling the young leaves to reduce
light intensity on the leaf surface (Fig. 9). Therefore,
C.-D. Jiang et al. / Environmental and Experimental Botany 55 (2006) 87–96
Fig. 10. Changes of FV /FM plotted as a function of irradiance for
three types of leaf. Data were obtained in Fig. 4B.
no more decrease of FV /FM occurred in young leaves
than that in mature ones under the field conditions
(Fig. 5B) with the daily maximum photon flux density
being larger than 1500 ␮mol m−2 s−1 at noon.
5. Conclusion
The changes of petiole angle and the midrib angle
kept the young leaves more vertical in positions, which
reduced light intensity on the leaf surface; and the collaboration of leaf angle, photorespiration and thermal
dissipation depending on xanthophyll cycle successfully protected young leaves against high irradiance in
field.
Acknowledgements
The authors gratefully acknowledge the support of
K.C. Wang Education Foundation (Hong Kong) and
China Postdoctoral Science Foundation.
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