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ORIGINAL PAPER
Photosynthetic regulation of C4 desert plant Haloxylonammodendron under drought stress
Peixi Su Æ Guodong Cheng Æ Qiaodi Yan ÆXinmin Liu
Received: 10 December 2005 / Accepted: 6 December 2006 / Published online: 16 January 2007� Springer Science+Business Media B.V. 2007
Abstract About 20-year-old desert plants of C4
species, Haloxylon ammodendron, growing at the
southern edge of the Badain Jaran Desert in
China, were selected to study the photosynthetic
characteristics and changes in chlorophyll fluo-
rescence when plants were subject to a normal
arid environment (AE), moist atmospheric con-
ditions during post-rain (PR), and the artificial
supplement of soil water (SW). Results showed
that under high radiation, in the AE, the species
down-regulated its net assimilation rate (A) and
maximum photochemical efficiency of PS II (Fv/
Fm), indicating photoinhibition. However, under
the PR and SW environments, A was up-regulated,
with a unimodal diurnal course of A and a small
diurnal change in Fv/Fm, suggesting no photoin-
hibition. When the air humidity or SW content
was increased, the light compensation points were
reduced; light saturation points were enhanced;
while light saturated rate of CO2 assimilation
(Amax) and apparent quantum yield of CO2
assimilation (FC) increased. FC was higher while
the Amax was reduced under PR relative to the
SW treatment. It was concluded that under high-
radiation conditions drought stress causes pho-
toinhibition of H. ammodendron. Increasing air
humidity or soil moisture content can reduce
photoinhibition and increase the efficiency of
solar energy use.
Keywords Desert plant � Photoinhibition �Photosynthesis down regulation � Photochemical
efficiency � Drought stress
Abbreviations
A Net assimilation rate
Amax Light saturated rate of CO2 assimilation
AE Arid environment
FC Apparent quantum yield of CO2
assimilation
Ca Ambient CO2 concentration
Ci Intercellular CO2 concentration
Fv/Fm Maximum photochemical efficiency
of PS II
Ic Light compensation point
Ik Light saturation point
PR Moist atmospheric conditions during
post-rain
PFD Photon flux density
RH Air relative humidity
SW Supplement of soil water
P. Su � Q. Yan � X. LiuLinze Inland River Basin Comprehensive ResearchStation, Cold and Arid Regions Environmentaland Engineering Research Institute, CAS,Lanzhou 730000, China
P. Su (&) � G. ChengState Key Laboratory of Frozen Soil Engineering,Cold and Arid Regions Environmentaland Engineering Research Institute, CAS,Lanzhou 730000, Chinae-mail: [email protected]
123
Plant Growth Regul (2007) 51:139–147
DOI 10.1007/s10725-006-9156-9
SW1 On day 1 after watering
SW2 On day 2 after watering
Ta Air temperature
Tl Leaf temperature
Introduction
Desert plants grow in a harsh environment with
high temperatures and radiation and are exposed
to drought often for much of the year. Their
specific morphological and physiological fea-
tures frequently reduce water loss and alleviate
high-radiation damage to the photosynthetic
apparatus. Morphologically, the true leaves of
Haloxylon ammodendron show a number of
degenerative features. It is the cortex of the
young annual shoots that provides the main
photosynthetic tissue. This adaptation reduces
the photoactive area and decreases plant water
loss. The physiological characteristics of H. am-
modendron photosynthetic organs (assimilating
shoots) conforms with Kranz anatomy; with
carbon isotopic ratio (d13C) values which are
around –15&, CO2 compensation point of less
than 5 lmol mol–1, light saturation point (Ik) of
higher than 1,600 lmol m–2 s–1, and elevated
photosynthetic capacity combined with high
water use efficiency (Su et al. 2004).
Plants adjust to changes in the harsh environ-
ment in an attempt to optimize and preserve the
functioning of the photosynthetic apparatus. Pho-
tosynthetic tissue adapts to high-external radia-
tion by protecting the assimilation process
by diurnal adjustments in photochemical and
non-photochemical processes (Franco and Luttge
2002). Photoinhibition occurs whenever the
absorbed light energy exceeds the capacity of
the plants to use the trapped energy through
photosynthetic electron transport (Jia and Lu
2003). Previously, the term photoinhibition was
used almost synonymously with damage to PS II.
However, it has now been demonstrated that
photoinhibition can result not only from some
form of ‘‘damage’’ to PS II but also from an
increase in thermal energy dissipation, which is a
photoprotective process and does not represent
damage (Demmig-Adams and Adams 1992).
Short-term photoinhibition was not due to photo-
damage since this aggravated photoinhibition
could be rapidly and fully recovered and was
reversible, under long-term photoinhibition the
decreased maximum photochemical efficiency of
PS II (Fv/Fm) may be partly associated with
protective processes (Jia and Lu 2003).
The measurement of chlorophyll fluorescence
is a useful tool for quantification of the effect of
stress on photosynthesis (Krause and Weis 1991;
Schreiber et al. 1994). The Fv/Fm is frequently
used as a sensitive indicator of plant photosyn-
thetic performance, with many species showing
optimal values of around 0.83 (Bjorkman and
Demmig 1987; Johnson et al. 1993). Large
reversible decreases in Fv/Fm were compensated
by proportional increases in non-photochemical
processes related to photoprotection (Franco and
Luttge 2002).
This paper aims to describe the adaptive self-
regulation mechanisms of C4 desert plants,
H. ammodendron, and provide an improved
understanding of how key photosynthetic charac-
teristics and chlorophyll fluorescence change un-
der different atmospheric and soil water regimes.
Materials and methods
Environmental conditions of the study area
The study area in these experiments was located
at the southern edge of the Badain Jaran Desert,
China (39�19¢–39�21¢ N and 100�02¢–100�21¢ E), at
an altitude of 1,370 m. The climate in this region
is temperate continental, with an average annual
precipitation of 117 mm and a mean annual
evaporative demand of over 2,390 mm. Rainfall
mostly (70%) occurs between June and Septem-
ber. The average temperature is 7.6�C, while the
absolute maximum may reach 39�C and minimum
–27�C, with the frost-free period lasting around
165 days. Accumulated annual temperature of
‡10�C is around 3,088�C (Su et al. 2004).
Difference in environmental regimes
The classification of an arid environment (AE)
was used where plants were exposed to five
140 Plant Growth Regul (2007) 51:139–147
123
consecutive days or more without precipitation
and with day time air relative humidity (RH)
ranging from 9 to 35%, and a soil surface layer
(0–10 cm) volumetric moisture content of £0.7%,
at a soil water potential of £–29 kPa. This
situation is considered normal for the study
region.
Moist atmospheric conditions during post-rain
(PR), frequently occurs when rainfall exceeds
8 mm and with a day time RH ranging from 20 to
70%, and the soil surface layer (0–10 cm) volu-
metric moisture content exceeding 7% (soil water
potential >–13 kPa).
Soil water was supplemented (SW) by the
addition of 100 l of water at a depth of 25 cm. On
day 1 (SW1) and 2 (SW2) after watering soil
volumetric moisture content in the soil layer
(20–60 cm) increased by 329 and 236%, respec-
tively, without any effect on atmospheric humidity.
Soil moisture content and water potentials for the
three environmental regimes are presented in
Fig. 1.
To study the impact of maximal radiation,
combined with high temperature, measurements
were undertaken in late July (Su and Liu 2005).
This study also need effective rainfall (>8 mm)
immediately followed a high-radiation day, which
may not always occur in late July. To ensure this
comparison was possible, measurements were
taken over more than a single year. Experimental
plants were in a mature phase of growth (�20-
year-old), and showed little change from year-
to-year, and so the impact of plant growth
between years is expected to be minimal.
Photosynthesis measurements
Three 20-year-old plants H. ammodendron were
selected and their locations and site conditions
were recorded with repeated measurements on the
same plants. Daily dynamics of gas exchange and
response to photon flux density (PFD) were
measured under the three environmental regimes
on typical cloudless days during the high-temper-
ature period in late July (2001–2004) using LI-6400
Portable Photosynthetic System (LI-COR,
Lincoln, NE, USA). Under AE the diurnal mean
air temperature (Ta) (from 8:00 to 18:00) was
>32�C, the diurnal mean RH >15%; under PR the
diurnal mean Ta and RH were >29�C and >35%,
respectively, under SW2 corresponding values
were >33�C and >15%, respectively. Ambient
CO2 concentration (Ca) was 366 lmol mol–1. Four
assimilating shoots were selected for measurement
on each of the plants. Measurements were made in
the middle of the sunny side of the canopy. In
order to increase measuring area and keep the
consistent area of assimilating shoots closed in the
leaf chamber during measure, four assimilating
shoots were fastened to a plane side by side with
adhesive tape at both ends, then measured in vivo.
Each measurement was repeated three times.
Assimilation response to PFD was achieved using
different layers of neutral filters (Su et al. 2004).
Chlorophyll fluorescence measurements
The same material, as used for the A mea-
surements, was used to measure chlorophyll
-100
-80
-60
-40
-20
00 2 4 6 8 10 12 14 16
AE PR SW1 SW2
Soil volumetric moisture content (%)
)mc( htped lioS
-100
-80
-60
-40
-20
0-40 -35 -30 -25 -20 -15 -10 -5 0
AE PR SW1 SW2
Soil water potential (kPa)
)mc( htped lioS
(a) (b)
Fig. 1 Changes in soil moisture content (a) and waterpotential (b) at the three environmental regimes in growthsite of Haloxylon ammodendron. AE arid environment,
PR moist atmospheric conditions during post-rain, SW1 onday 1 after watering, SW2 on day 2 after watering. Errorbars are ±SE
Plant Growth Regul (2007) 51:139–147 141
123
fluorescence diurnally (8:00–18:00) with a FMS-2
Fluorescence Meter (Hansatech Company, Cam-
bridge, UK). Parameters measured included zero
fluorescence (Fo), variable fluorescence (Fv),
maximum fluorescence (Fm), and photochemical
efficiency of PS II (Fv/Fm). Before measurement,
the assimilating shoots were dark-adapted with
leaf-clips for 25 min (Seppanen and Coleman
2003), which was found to be sufficient to allow
complete reoxidation of the PS II reaction centers
and to ensure that all energy dependent quenching
was relaxed. All measurements were repeated five
times.
Statistical analysis
Differences in photosynthetic rates under the
different water regimes were analyzed by single
factor variance analysis. A multiple comparison
of various levels was made using Duncan’s new
multiple range test. The light compensation point
(Ic) was obtained from fitting a linear regression
of A against PFD (£200 lmol m–2 s–1), and
apparent quantum yield from dA/dPFD (Von
Caemmerer and Farquhar 1981). The Ik was
obtained by fitting a quadratic equation of A
against PFD (>200 lmol m–2 s–1) (Su et al. 2004).
Results
Daily changes in meteorological factors
under different environmental regimes
It can be seen from Fig. 2a that the PFD increased
antemeridian, and reached to the maximum at
13:00, then declined to sundown. Under the
environmental regimes used there was no signif-
icant difference in maximal PFD over most of the
photoperiod, which exceeded 2,000 lmol m–2 s–1
at mid-day (Fig. 2a). In generally RH declined
from 8:00 to 18:00 (Fig. 2b). RH was significantly
greater (P < 0.01) for the PR treatment compared
to AE and SW2 treatments. The mean value under
PR between 8:00 and 18:00 was 37%, while under
AE it was 18% and remained at a similar-value for
the SW2 treatment. No significant difference
existed between AE and SW2 treatments. The
minimum RH-values under PR, AE, and SW2
were 22, 9, and 11%, respectively (Fig. 2b).
Changes in Ta under different environmental
regimes are shown in Fig. 2c. The Ta increased
from sunrise to maximum during 15:00–16:00, and
then declined. The mean temperature values under
PR were 29.6�C with a maximum value of 35.0�C at
16:00. Temperature under AE and SW2 differed
little (33�C), with maximum values (37�C) occur-
ring at 15:00 (Fig. 2c). The diurnal pattern of the
leaf temperature (Tl) was the same as for Ta. The
mean values of Tl under PR, AE, and SW2 were 30,
33, and 34�C, with the maximum temperatures of
35, 37, and 38�C, respectively (Fig. 2d).
It can be seen from Fig. 2e that the diurnal
variations of intercellular CO2 concentration (Ci)
declined from 8:00 to mid-day and then increased,
which were caused mainly by the diurnal changes
in photosynthetic abilities.
Diurnal changes of assimilation rate
under different environmental regimes
It can be seen from Fig. 3a that the diurnal course
of net assimilation rate (A) of H. ammodendron
under PR showed a unimodal pattern, with a
maximum value at 15:00. The daily mean A (from
8:00 to 18:00) was 21 ± 4 lmol m–2 s–1, with a
maximum value of 39 lmol m–2 s–1. The diurnal
course under AE was however bimodal with a
depression in A around 15:00. Daily mean A
under AE was 18 ± 4 lmol m–2 s–1, with a max-
imum value of 36 lmol m–2 s–1. A similar depres-
sion was observed on other sunny days in July
under AE with no significant difference between
days (July 20, 2001 and July 21, 2002); the values
for the first and second peak are 34.8 and
16.7 lmol m–2 s–1 on 20 July and 35.5 and
17.3 lmol m–2 s–1 on 21 July, respectively. Assim-
ilation rate under SW showed no mid-day depres-
sion (Fig. 3b). Daily mean A under SW1, and
SW2 were 28 ± 4 and 25 ± 4 lmol m–2 s–1 with
maximum values of 42 and 39 lmol m–2 s–1,
respectively.
Diurnal changes in chlorophyll fluorescence
under different environmental regimes
It can be seen from the photochemical efficiency
of PS II that the Fv/Fm ratio for H. ammoden-
dron was lowest between 14:00 and 16:00 under
142 Plant Growth Regul (2007) 51:139–147
123
(e)
8 10 12 14 16 18100
150
200
250
300
350
AE PR SW2
Time of day (h)
( iC
µlo
m lom
1-)
(c)
8 10 12 14 16 18
18
21
24
27
30
33
36
39
Time of day (h)
AE PR SW2
(d)
8 10 12 14 16 18
18
21
24
27
30
33
36
39
AE PR SW2
Time of day (h)
(a)
8 10 12 14 16 18300
600
900
1200
1500
1800
2100
AE PR SW2
( DFP
µm lo
m2-
s 1-)
(b)
8 10 12 14 16 18
10
20
30
40
50
60
70
**
AEPRSW2
)%(
HR
Ta (
0C
)
Tl (
0C
)
Fig. 2 Diurnal pattern of photon flux density (PFD) (a),air relative humidity (RH) (b), air temperature (Ta) (c),leaf temperature (Tl) (d), and intercellular CO2 concen-tration (Ci) (e) under three environmental regimes. AEarid environment, measured on July 23, 2002, PR moist
atmospheric conditions during post-rain, measured on July24, 2001, SW2 on day 2 after watering, measured on July21, 2004. Asterisks indicates significant differences(P < 0.01) for the PR compared to AE and SW2 (b)
(a)
8 10 12 14 16 180
10
20
30
40
50
AE PR
A( µ
OC lo
m2
m 2-
s 1-)
Time of day (h)
(b)
8 10 12 14 16 180
10
20
30
40
50
SW1 SW2
Time of day (h)
A( µ
OC lo
m2
m 2-s
1-)
Fig. 3 Diurnal course of net assimilation rate (A) ofHaloxylon ammodendron at the three environmentalregimes. AE arid environment, measured on July 23,2002, PR moist atmospheric conditions during post-rain,
measured on July 24, 2001, SW1 on day 1 after water-ing, measured on July 20, 2004, SW2 on day 2 afterwatering, measured on July 21, 2004. Error bars are ±SE
Plant Growth Regul (2007) 51:139–147 143
123
the AE. Fv/Fm under AE was 0.86 at 8:00 and
declined to 0.73 at 16:00 (Fig. 4). Statistical
analyses shows that there was no significant
difference in Fv/Fm during 8:00–12:00 among
three environmental regimes, but there was sig-
nificant differences (P < 0.01) between the AE
compared to PR and SW2 treatments during
14:00–18:00. Minimum values of Fv/Fm recorded
on the SW2 and PR were similar; these values
were higher than 0.81 (Fig. 4). Healthy plants have
Fv/Fm of 0.8–0.9 in general (Odasz-Albrigtsen
et al. 2000).
The responses of A to PFD under different
environmental regimes
The responses of A of H. ammodendron to PFD
(Ic, Ik, apparent quantum yield of CO2 assimila-
tion (FC) and light saturated rate of CO2 assim-
ilation (Amax)) under different environmental
regimes are shown in Fig. 5 and Table 1. Com-
pared with that under AE, the FC, Amax, and Ik
under PR and SW2 treatments were higher, but
the Ic were lower. The Amax for treatments PR and
SW2 were 27 and 35% greater than that under
AE. The values of Ic, Ik, and Amax under SW2 were
higher than those under PR, but the value of FC
under SW2 was lower than that under PR.
Discussion
Drought is considered to be a predominant factor
both for determining the global geographic dis-
tribution of vegetation and restricting crop yields
in agriculture (Schulze 1986). Water is the limit-
ing factor for plant growing in arid to semiarid
8 10 12 14 16 18
0.72
0.75
0.78
0.81
0.84
0.87
0.90
**
AE PR SW2
mF/vF
Time of day (h)
Fig. 4 Diurnal changes of maximum photochemical effi-ciency of PS II (Fv/Fm) of Haloxylon ammodendron underthree environmental regimes. AE arid environment,measured on July 23, 2002, PR moist atmosphericconditions during post-rain, measured on July 24, 2001,SW2 on day 2 after watering, measured on July 21, 2004.Error bars are ±SE. Asterisks indicates significant differ-ences (P < 0.01) for the AE compared to PR and SW2between 14:00 and 18:00
(a)
0 40 80 120 160 200-4
0
4
8
12
16 AE PR SW2 Fitted of AE Fitted of PR Fitted of SW2
A( µ
OC l o
m2
m 2-
s 1 -)
PFD (µmol m-2 s-1)
(b)
400 800 1200 1600 20000
10
20
30
40
50
AE PR SW2 Fitted of AE Fitted of PR Fitted of SW2
A( µ
OC lo
m2
m 2-
s 1-)
PFD (µmol m-2 s-1)
Fig. 5 Responses of net assimilation rate (A) to differentphoton flux density (PFD) of Haloxylon ammodendronunder three environmental regimes. AE arid environment,measured on July 23, 2002, PR moist atmosphericconditions during post-rain, measured on July 24, 2001,SW2 on day 2 after watering, measured on July 21, 2004.During the measurement, Ca was 360.0 ± 1.0 lmol mol–1,and Tl was 30.0 ± 0.3�C. Error bars are ±SE. (a) Fitted asa linear equation under low PFD (£200 lmol m–2 s–1), AE:
A = –3.4591 + 0.0436PFD, r2 = 0.995, P < 0.001; PR: A =–1.1454 + 0.0876PFD, r2 = 0.997, P < 0.0001; SW2:A = –3.5435 + 0.0553PFD, r2 = 0.956, P = 0.006. (b) Fit-ted as a quadratic equation under high PFD(>200 lmol m–2 s–1), AE: A = –0.3378 + 0.0331PFD –0.00001PFD2, r2 = 0.997, P = 0.0002; PR:A = 11.053 + 0.0237PFD – 0.000006PFD2, r2 = 0.975,P = 0.003; SW2: A = 1.1756 + 0.0358PFD –0.000009PFD2, r2 = 0.997, P < 0.0001
144 Plant Growth Regul (2007) 51:139–147
123
regions. For desert plants the exact compromise
that occurs in nature between restricting water
loss through stomata versus maintaining a high-
carbon gain depends on stomatal and non-stoma-
tal regulations. In the present study, the change of
the A of H. ammodendron under AE at 15:00 was
in the opposite direction to Ci (Figs. 2e, 3a). The
criterion for establishing that stomatal responses
are dominant in the response of assimilation rate
to some perturbation is that Ci should change in
the same direction as A. If the changes are
opposite, the most important change must have
been in the mesophyll cells (Farquhar and Shar-
key 1982), caused by non-stomatal factors, such as
limiting of RuBP production, ribulose–1,5-bis-
phosphate carboxylase/oxygenase (RuBPCO)
activity, ATP production (Lawlor and Cornic
2002), photosystem II activity and electron trans-
port (Tezara et al. 2005). In our study, diurnal
course of Ci associated with diurnal course of A
under AE suggested that a non-stomatal factor
was the main cause of the reduction of A. Under
non-stressed conditions (PR and SW), A showed
no depression despite high radiation (Fig. 3).
At the same time as the decrease of A under
high radiation in the AE was (Fig. 3a), Fv/Fm
decreased (Fig. 4). Fv/Fm is one of the fluores-
cence parameters most widely used to estimate the
degree of photoinhibition (Osmond and Grace
1995; Solhaug and Haugen 1998). Photoinhibition
is characterized by parallel decreases in A and Fc,
accompanied by a decline in Fv/Fm (Osmond and
Grace 1995). In addition, reduction of Amax is also
one of the characteristics of photoinhibition
(Sassenrath and Ort 1990). In our study when air
humidity and soil moisture increased under PR and
SW, the FC and Amax were increased, compared to
under AE (Fig. 5, Table 1). It was concluded that
photoinhibition of H. ammodendron occurred
under AE, but not under PR and SW. Zhao et al.
(2005) also observed that photoinhibition of
H. ammodendron occurred in an AE.
CO2 assimilation rates of H. ammodendron
were high under PR and SW treatments without
depression under high radiation. Under AE,
when A decreased at 15:00, Fv/Fm was at a
minimum. Fv/Fm recovered by the next morning
(data not shown), indicating that photoinhibition
was reversible. This can be associated with limited
susceptibility to photoinhibition (Werner et al.
1999). Reduced susceptibility to photoinhibition
is sometimes associated with a high CO2 assim-
ilation capacity (Edwards and Baker 1993; Jia and
Lu 2003). As shown in our study and previously
reported by Su et al. (2004) and Ju et al. (2005),
assimilation rates of H. ammodendron are very
high. It has been suggested that CO2 assimilation
is the main sink to utilize absorbed light and is the
primary means of protection against photoinhibi-
tion (Powles 1984). Photoinhibition of PS II in
vivo is often a photoprotective strategy, protect-
ing against excess excitation energy, rather than a
damaging process (Demmig-Adams and Adams
1992; Anderson et al. 1997; Choudhury and
Behera 2001). A diurnal decline in Fv/Fm that is
fully reversible overnight is often associated with
photoprotection rather than damage to PS II
(Werner et al. 1999). Further study is required to
confirm whether the photoinhibition response of
H. ammodendron under arid conditions is a
protective mechanism.
Many factors such as high light, high temper-
ature, low-soil moisture, and nitrogen deficiency,
etc. may lead to photoinhibition (Long et al. 1994;
Figueroa et al. 1997; Flexas et al. 1999). Even
under low light, other adverse environment
Table 1 Light compensation point (Ic), light saturation point (Ik), apparent quantum yield of CO2 assimilation (FC), andlight saturated rate of CO2 assimilation (Amax) of Haloxylon ammodendron at the three environmental regimes
Environmental regimes Ic (lmol m–2 s–1) Ik (lmol m–2 s–1) FC (mol mol–1) Amax (lmol m–2 s–1)
AE 79a 1,655a 0.044a 27a
PR 13b 1,975b 0.088b 35b
SW2 64c 1,989b 0.055c 37b
AE arid environment, PR moist atmospheric conditions during post-rain, SW2 on day 2 after watering. The data here are thefitted results of repeated three times in Fig. 5. In the same column, the same small letter means no significant difference atthe 0.05 P-level
Plant Growth Regul (2007) 51:139–147 145
123
stresses may cause photoinhibition (Demmig-
Adams and Adams 1992; Oquist et al. 1992).
Under the three environmental regimes, there
was no significant difference in the maximal PFD,
which shows that the high radiation was not the
predominant factor to photoinhibition. Neither
Ta nor Tl exceeded the maximum temperature
for photosynthesis in C4 plants (45�C; Ludlow
1976) in any of the environmental regimes,
additionally temperatures in AE, under which
photoinhibition occurred, were lower than SW2
(Fig. 2c, d). This suggests that temperature was
not the predominant factor causing photoinhibi-
tion in arid desert environment. Our results
indicate that photoinhibition of H. ammodendron
occurs under drought conditions. Increasing
either air humidity or soil moisture content can
reduce photoinhibition.
The root system of H. ammodendron devel-
oped 20 cm below the ground surface. It is
interesting that an increase in air humidity
showed a similar effect to soil wetting in prevent-
ing photoinhibition. The interior mechanism
remains to be further studied to identify the
contribution of increased air humidity to avoid
the photoinhibition.
Acknowledgements We are grateful for the financialsupport by the National Natural Sciences Foundation ofChina (No. 40471046) and the key project of the ChineseAcademy of Sciences (KZCX1-09). The authors also wantto express thanks to the editor and the anonymousreviewers for their valuable comments to the manuscript.
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