Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
1
2
3
Leaf Photosynthesis and Yield Components of Mung Bean under Fully Open-air
Elevated [CO2]1
4
5
Ji Gao 1,2*, Xue Han1*, Saman Seneweera3, Ping Li2, Yuzheng Zong2,Qi Dong2, Erda Lin1, Xingyu
6
Hao1,2
7
1
8
and Sustainable Development in Agriculture (IEDA), Chinese Academy of Agricultural Sciences, Beijing,100081,
9
P.R. China
Key Laboratory of Ministry of Agriculture on Agro-environment and Climate Change, Institute of Environment
10
2
College of Agriculture, Shanxi Agricultural University, Taigu, Shanxi, 030801, P.R. China
11
3
Centre for Systems Biology, University of Southern, Toowoomba, Queensland, QLD 4350, Australia
12
13
Abstract
14
Mung bean (Vigna radiata L.) has the potential to establish symbiosis with rhizobia, and
15
symbiotic association of soil micro flora may facilitate the photosynthesis and plant growth
16
response to elevated [CO2]. Mung bean was grown at either ambient CO2 400 mol mol–1 or [CO2]
17
(550  17 mol mol–1) under FACE (Free-Air Carbon dioxide Enrichment) experimental facility
18
in North China. Elevated [CO2] increased net photosynthetic rate (PN), water use efficiency (WUE)
19
and the non-photochemical quenching (NPQ) of upper most fully-expanded leaves, but decreased
20
stomatal conductance (gs), intrinsic efficiency of PSⅡ (Fv'/Fm'), quantum yield of PSⅡ(ΦPSⅡ)
21
and proportion of open PSⅡreaction centers (qP). At elevated [CO2], the decrease of Fv'/Fm',
22
ΦPSⅡ, qP at the bloom stage were smaller than that at the pod stage. On the other hand, PN was
23
increased at elevated [CO2] by 18.7%, 7.4% at bloom (R2) and pod maturity stage (R4),
24
respectively. From these findings, we concluded that as a legume despite greater nutrient supply to
25
the carbon assimilation at elevated [CO2], photosynthetic capacity of mung bean was still
26
suppressed under elevated [CO2] particularly at pod maturity stage but plant biomass and yields
27
was increased by 11.6 and 14.2%, respectively. Further, these findings suggest that even under
28
higher nutrient acquisition systems such as legumes, nutrient assimilation does not match carbon
29
assimilation under elevated [CO2] and leads photosynthesis down-regulation to elevated [CO2].
30
31
Key words: Free-air
Carbon Dioxide
Enrichment (FACE),
32
Photosynthesis, Chlorophyll fluorescence, Yield, mung bean
Photosynthetic pigment,
33
34
35
1
Correspondence: LIN Erda, E-mail: [email protected](EL); HAO xing-yu,
[email protected](XH))
*
Authors contributed equally to this work.
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
36
37
38
INTRODUCTION
Global atmospheric CO2 concentration ([CO2]) is predicted to reach 550 mol mol–1 by the
39
middle of this century (IPCC 2007). The increase in [CO2] may improve the photosynthetic
40
efficiency of plants, which leads to increasing the supply of photoassimilates, and thus the
41
biomass and yield (Ainsworth & long 2005; Long et al. 2004; Drake et al. 1997). In general, high
42
[CO2] increased the carboxylation rate of Rubisco while inhibits the oxygenation of Ribulose-1,
43
5-bisphosphate (RubP) (Bowes 1993). The response of plants to elevated [CO2] differs from one
44
species to another. The main reason for such variation in the photosynthetic response to elevated
45
[CO2] has been identified between the species and even with the species (Ainsworth & long 2005).
46
Variation in photosynthetic biochemistry and kinetic characteristics and sink strength and
47
molecular biology of Rubisco are identified as central to lower response to elevated [CO2] (Bowes
48
1993; Hao et al. 2012).
49
Mung bean (Vigna radiata L.) is an important conventional pulse crop in China and is
50
growing worldwide. It is an important crop not only due to its high nutritional value but also play
51
an important role in soil nitrogen enrichment via symbiotic fixation of atmospheric nitrogen. The
52
seeds of mung beans are commercially produced in China, Burma, India, Korea, Pakistan, Japan,
53
Thailand, and other parts of Southeast Asia. The beans are rich in protein and low in fat (Zhang et
54
al. 2013). Photosynthetic acclimation occurred in soybean plants exposed to long-term elevated
55
[CO2] and varied with cultivars, photosynthetic acclimation not occurred for the cultivar with
56
developed new sinks (Hao et al. 2012). N2-fixing pea exposed to elevated [CO2] were capable of
57
maintaining hexose levels (involved in Rubisco down regulation) at control levels with the
58
consequent avoidance of photosynthetic acclimation (Aranjuelo et al. 2014). However, there is a
59
limited understanding how mung bean will response to future climate.
60
So far, only a few studies have been conducted on the responses of mung bean to elevated
61
[CO2] using enclosure system or growing plants in pots under FACE conditions (Yuan et al. 2007;
62
Hao et al. 2011; Hao 2014). It has been previously reported that when plants exposed to doubled
63
[CO2], Arbuscular mycorrhizal (AM) significantly increased the colonization capacity and hyphal
64
length (Yuan et al. 2007). Under enclosure conditions, Yuan et al reported significant increases in
65
the root/shoot ratio of mung bean when infected with AM fungi under doubled [CO2] when plant
66
were exposed for 28 days after sprouting (Yuan et al. 2007). Elevated [CO2] increased net
67
photosynthesis rate (PN) and water use efficiency (WUE) while decreased the stomatal
68
conductance (Gs) and transpiration rate (Tr) of mung bean. Further, plants were grown at elevated
69
[CO2] in pots decreased Maximum quantum efficiency (Fv/Fm) at pod filling stage (Hao et al.
70
2011). As most of the studies conducted in control conditions, the elevated [CO2] effects on plant
71
growth and development could have been not same as what experience under field conditions
72
(McLeod & Long 1999; Long et al. 2004). For example, restricted root growth limit the plant
73
response to elevated [CO2] (McLeod & Long 1999; Long et al. 2004).
Journal of Integrative Agriculture
Advanced Online Publication: 2015
74
Doi: 10.1016/S2095-3119(14)60941-2
In general, large amount of chlorophylls a and b absorbed energy from photosynthetically
75
active radiation (PAR) use in photosynthesis carbon reduction (PCR) reactions. In this process, the
76
carotenoids protect the reaction center from excess light and help them to intercept PAR into
77
auxiliary pigments of Chl a. Therefore, changes of pigment level in leaves strongly relate to the
78
physiological status and thus crop productivity (Strogonov 1973; Blaceburn 1998).
79
Plant species differ greatly in response to elevated [CO2] and among them, different functional
80
groups including legumes (Hao et al. 2012; Ainsworth & Long 2005). This is the first study that
81
reports the how elevated [CO2] influence the leaf photosynthetic physiology, chlorophyll
82
fluorescence and yield component in mung bean under open-air conditions. This study aims to
83
address the following questions: (1) Will the leaf photosynthetic physiology and chlorophyll
84
fluorescence properties varied under elevated [CO2] and whether there is any association between
85
these photosynthetic parameters? (2) Will elevated [CO2] improve photosynthetic capacity of
86
mung bean and whether there is any implication for the biomass and yield potential?
87
RESULTS
88
Photosynthetic pigment concentrations
89
At the bloom state, Chl a and total Chl concentrations were higher under elevated [CO2] than
90
under ambient [CO2] where Chl concentration increased at elevated [CO2] by 10.9 and 10.6%,
91
respectively (Fig.1). Despite total Chl concentration increased under elevated [CO2], no significant
92
differences in Chl b and carotenoid were observed. On other hand, at pod maturity (R4), the
93
concentration of Chl a, Chl b, carotenoid, total Chl, and Chl a/b were unchanged at elevated [CO2]
94
(Fig 1).
95
PN and gas exchange parameters
96
When photosynthesis and gas exchange parameters were measured under the growth [CO2]
97
(ambient conditions plant measured under 400μmol mol-1, FACE plant measured under 550 μmol
98
mol-1), it was found that PN of upper most fully-expended leaves in mung bean was stimulated by
99
18.7% and 7.4% at elevated [CO2] respectively at R2 and R4 growth stages. Simultaneous
100
measurement of gs was decreased under elevated [CO2] and the reduction was 19.2 and 13.7%,
101
respectively. Despite reduction of gs, Tr was not affected by elevated [CO2] (Table
102
1).Consequently, WUE was increased by 38.9 and 19.9% at elevated CO2 respectively at R2 and
103
R4 growth stages. The mechanistic analysis of gas change revealed that Jmax and Vc,max were not
104
significantly changed under elevated [CO2]. The interactive effect between [CO2] and growth
105
stage (R2 and R4) on PN, gs, Tr, WUE, Maximum velocity of carboxylation (Vc,max), Maximum
106
rate of electron transport (Jmax )was not significant (Table 1).
107
Chlorophyll fluorescence
108
Fv/Fm ranged from 0.78 to 0.83 and was not affected by elevated [CO2]. However, elevated
109
[CO2] significantly decreased Fv'/Fm' which was 2.8 and 13.8%, at 40 and 58 DAS, respectively.
110
Simultaneously, elevated [CO2] reduced ΦPSⅡ by 2.3 and 34.5%, at R2 and R4 growth stages,
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
111
respectively. In the same time, the degree of opening of PSⅡreaction centers (qP) was decreased
112
at elevated [CO2] by 0.4 and 23.2%, in R2 and R4 growth stages respectively. On other hand,
113
non-photochemical quenching (NPQ) in leaves was increased by 12.8 and 28.2%, at R2 and R4
114
growth stages, respectively. The decrease of Fv'/Fm', ΦPSⅡ, qP between ambient and FACE at
115
R2 stages were much lower than that at R4 stages (Table 2).
116
117
Biomass, yield and yield composition
118
The total biomass and grain yield per square meter was significantly increased at elevated
119
[CO2] by 11.6% and 14.2% respectively (Fig.2). The increase in grain yield at elevated [CO2]
120
was largely associated with increased seed number where seed number per pod was increased
121
by 11.8% at elevated [CO2] (Table 3). However, elevated [CO2] had no significant effect on
122
the number of pods per plant or the weight of 100 seeds.
123
DISCUSSION
124
The changes of pigment concentrations in leaf are well associated with physiological status
125
and thus productivity of a plant (Strogonov 1973; Blaceburn 1998). In recent past, Jiang et al.
126
(2006) and Zhao et al. (2003) investigated the biosynthesis of photosynthetic pigments of soybean
127
(Glycine max L. Merr.) leaf during leaf development under elevated [CO2] in OTC (Open topped
128
chambers) and demonstrated that elevated [CO2] increased the contents of Chl a, Chl b, total
129
chlorophyll and carotenoid in leaves. On the contrary, the content of Chl a, Chl b, carotenoid, total
130
Chl, and Chl a/b were not affected for soybean by elevated [CO2] in a previous FACE study (Hao
131
et al. 2012). The reduction of total chlorophyll (a + b) concentration at elevated [CO2] were
132
documented for black spruce (Picea mariana (Mill.) B.S.P.) and red spruce (Picea rubens Sarg.)
133
(Major et al. 2007). However, our results clearly demonstrated that elevated [CO2] increased the
134
chlorophyll concentration of mung bean at the bloom stage, but no effect was found at the pod
135
maturity stage (Fig 1). These findings suggest that pigment turnover in response to elevated [CO2]
136
varied with growth stage of the plant. These findings are quite different to other species as
137
chlorophyll content mostly decreased in most of non-legume C3 plants (Seneweera et al. 2005). In
138
our experiment, the measurement of PN was highest at elevated [CO2] when measurements were
139
made at bloom stage. This was supported by the increase of chlorophyll concentration and gas
140
exchange properties of the plants. The concentration of chlorophyll was increased at elevated
141
[CO2] by 18.7% at bloom stage compared to (7.4%) pod maturity stage.
142
In general, elevated [CO2] stimulated light-saturated photosynthesis (Asat) for C3 plants by an
143
average of 31% in FACE but the magnitude of the stimulation of
photosynthesis to elevated
144
[CO2] varied between functional groups and environment (Ainsworth & Rogers 2007). It has been
145
demonstrated that photosynthetic response to elevated CO2 was greater for functional groups that
146
shows the ribulose- 1,5 - bisphosphate carboxylase/oxygenase (Rubisco) is the major limiting
147
factor for the photosynthesis than those where photosynthesis became limited by
148
ribulose-1,5-bisphosphate (RubP) (Ainsworth & Rogers 2007). Our results showed that Jmax and
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
149
Vc,max in leaves were not significantly changed under elevated [CO2], despite an increase in PN at
150
elevated [CO2] .
151
ΦPSⅡ is related to the photochemical efficiency of PSⅡ(Tausz-Posch et al. 2013). The
152
parameter qN reflected activation state of the non-photochemical processes during the light period,
153
which mostly leading to the non-radiative energy dissipation (NRD) (Rohacek 2002). The intrinsic
154
efficiency of PSⅡ (Fv'/Fm') was called the efficiency of excitation energy capture by open (qP =
155
1) reaction centers of PSⅡ(Rohacek 2002). NPQ potential indicates that plant’s capacity to
156
dissipate energy by the means of thermal energy rather than linear electron transport (Myers et al.
157
1999). It has been previously demonstrated that NPQ dramatically increased when sink
158
development is limited (no development of new sinks) (Myers et al. 1999). In this experiment,
159
when plant exposed to elevated [CO2], Fv'/Fm', ΦPSⅡ and qP was significantly decreased, and
160
the reduction was greater at R4 stages than that at R2 stages. These findings further confirm that
161
the photosynthetic capacity of mung bean leaves was down-regulated when the development of
162
new sinks was restricted under elevated [CO2], and this response was predominant at R4 stage
163
(Table 2). In our experiment, NPQ was significantly increased at elevated [CO2] and consequently,
164
more energy was dissipated as a thermal energy (Table 2). However, it is still not known whether
165
this increase in thermal dissipation at elevated [CO2] have role in leaf senescence or initiation of
166
some of important catabolic reaction in the plants. PN was always greater at elevated [CO2] when
167
PN was measured at growth CO2 concentration (Table 1). Further, PN was always lower at the R4
168
compared to the R2 stage (Table 1) which was consistent with the change of chlorophyll
169
fluorescence parameters and gas exchange properties (Table 2). It has been well documented that
170
the source-sink relationship affects plant photosynthesis under elevated [CO2] (Ainsworth &
171
Rogers 2007; Hao et al. 2012). Our data suggest that mung bean have potential to respond to
172
elevated [CO2] for a great plasticity of sink development. [CO2]-induced increased in plant
173
biomass and yields by11.6% and 14.2%, respectively. The increase of yields at elevated [CO2] was
174
mainly due to the increased in seed number per pod at elevated [CO2]. Pod number and/or single
175
grain weight was not changed at elevated CO2.
176
Gs was significantly reduced under elevated [CO2] but no long-term stomatal acclimation to
177
elevated [CO2] was found in soybean (Leakey et al. 2006). The decrease in gs under elevated [CO2]
178
was associated with increased water use efficiency (Leakey et al. 2006). Gs was decreased in
179
mung bean under elevated [CO2], but Tr was not affected (Table 1). The water use efficiency in
180
mung bean was increased largely because of the increase in PN. These findings suggest that the
181
drought resistance of mung beam will be enhanced under high [CO2].
182
CONCLUSION
183
Elevated [CO2] increased the chlorophyll concentration of mung bean at the bloom stage. PN,
184
WUE and NPQ of upper most fully-expanded leaves in mung bean were increased under elevated
185
[CO2], but Fv'/Fm', ΦPSⅡ and qP was decreased. We concluded that photosynthetic capacity of
186
mung bean was restrained through the changes in chlorophyll fluorescence characteristics under
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
187
elevated [CO2].
Despite these changes, PN was greater at elevated [CO2] and consequently the
188
biomass and yields was increased under elevated [CO2]. The increase in yield was attributed to
189
increased grain number per pod rather than single grain weight or pod number. These findings
190
suggest that future mung bean yield can be improved if plants are bred for a great plasticity of sink
191
development.
192
193
MATERIALS AND METHODS
194
Site description
195
The study was conducted at the Mini-FACE facility developed by IEDA (Institute of
196
Environment and Sustainable Development in Agriculture) located at an experimental station of
197
the Chinese Academy of Agricultural Sciences at Changping, Beijing, China (40.13°N, 116.14°E).
198
The operational procedures of the facility were as described in a previous experiment (Hao et al.
199
2012, 2013). The soil is a clay loam and had a pH (1:5 soil:water) of 8.3,1.12% organic carbon (C),
200
and 0.10% total N before sowing. The rainfall and the average temperature during the mung bean
201
growing season in 2011 were 517.9 mm and 26.8℃, respectively (Hao et al. 2014).
202
203
Mung bean cultivation, fertilization and irrigation
Mung bean cv. Zhonglv 1, developed by the Institute of Crop Sciences, Chinese Academy
204
of Agricultural Sciences, was sown on 24 June 2011 on plots (4-m diameter octagonal plot) at 0.45
205
m row spacing and at a sowing density of 20 plants per m2. The experimental design was
206
randomized complete block with [CO2] as main effect and three replicates level (six plots, three
207
for FACE plots and three for ambient plots). Plots were neither irrigated nor fertilized during the
208
growing season.
209
Measurement of photosynthetic pigment concentration
210
Chl a, Chl b and Carotenoid concentration per fresh weight from the upper most
211
fully-expanded leaves at 40, 58 days after sowing (DAS) (equivalent to bloom and pod maturity
212
stage, respectively) were determined according to the methods of Arnon (Arnon 1949).
213
Gas exchange measurements
214
Measurements of PN vs Ci were conducted at 40 (bloom stage, R2) and 58 DAS (pod
215
maturity stage, R4). On an average, mung bean plants height were 41 and 65 cm tall at their
216
respective sampling time. The leaf number was 8th and 10th, respectively. Gas exchange
217
measurements were conducted using portable gas exchange systems (LI-COR 6400; LI-COR,
218
Lincoln, Neb.). The operational procedures of the systems were as described in a previous
219
experiment (Hao et al. 2012). The [CO2] in the leaf chamber was controlled by the LI-COR CO2
220
injection system, and an irradiance of 1600 μmol photons m-2 s-1 was supplied using an built-in
221
LED lamp (red/blue). Values of PN and Ci were used to calculate Vc,max and Jmax using the model
222
described by Sharkey et al (2007). PN and gs were also measured at the same irradiance,
223
temperature and the vapour pressure when measurements. [CO2] in the leaf chamber was set to
224
400 μmol mol-1and 550 μmol mol-1 for each treatment, and three upper most fully-expanded
Journal of Integrative Agriculture
Advanced Online Publication: 2015
225
leaves were measured per plot.
226
Chlorophyll fluorescence
227
Doi: 10.1016/S2095-3119(14)60941-2
The photosynthetic performance of upper most fully-expanded leaves was assessed in terms of
228
the chlorophyll a fluorescence parameter Fv/Fm, Fv'/Fm' , ΦPSⅡ, qP, NPQ using a miniaturized
229
pulse-amplitude modulated fluorescence analyzer (Mini-PAM, Walz, Effeltrich, Germany) with a
230
leaf clip holder as described by Bilger et al. (1995) and Hao et al. (2013), nine upper most
231
fully-expanded leaves were measured per plot. All chlorophyll fluorescence parameters were
232
calculated as described (Rascher et al. 2004).
233
Harvesting
234
At maturity, mung bean plants were hand-harvested on 2nd September 2011 (71 DAS) from
235
an area of 3 m2 within each plot. After drying, random subsamples of 10 plants from each subplot
236
were taken to assess the number of pods per plant, the number of seeds per pod and the weight of
237
100 seeds. Other plants were also threshed mechanically to separate seed from all other shoot
238
components. Yield was determined for all the plants from the 3 m2 patch in each plot.
239
Statistical analysis
240
All the experiment data presented was examined statistically by analysis of variance. Means
241
of three replicates were subjected to the analysis of variance at 0.05 probability level using SAS
242
243
244
245
246
247
248
249
System 8.1 (SAS Institute Inc., Cary, NC, USA).
Acknowledgement
This work was supported by The National Key Technology R&D Program in the 12th Five year
Plan of China (No.2013BAD11B03-8), National Basic Research Program of China (973 Program)
(No.2012 CB955904), Natural science fund projects of Shanxi Province(No.2013011039-3),
the Agricultural Science and Technology Innovation Program of CAAS, the earmarked fund for
Modern Agro-industry Technology Research System (CARS-3-1-24) and Shanxi Agricultural
University Doctoral Scientific Research fund.
250
251
Reference
252
Ainsworth E A, Long S P. 2005. What have we learned from 15 years of free-air CO2 enrichment
253
(FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and
254
plant production to rising CO2. New Phytologist, 165, 351-372.
255
Ainsworth E A, Rogers A. 2007. The response of photosynthesis and stomatal conductance to
256
rising [CO2]: mechanisms and environmental interactions. Plant Cell and Environment, 30,
257
258-270.
258
Aranjuelo I, Cabrerizo P M, Aparicio-Tejo P M, Arrese-Igor C. 2014, Unravelling the
259
mechanisms that improve photosynthetic performance of N2-fixing pea plants exposed to
260
elevated [CO2]. Environmental and Experimental Botany, 99, 167-174.
261
262
263
Arnon D I. 1949, Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.
Plant physiology, 24, 1-15.
Bilger W, Schreiber U, Bock M. 1995, Determination of the quantum efficiency of photosystem II
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
264
and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia, 102,
265
425-432.
266
267
268
269
Blaceburn G A. 1998, Spectral indices for estimating photosynthetic pigment concentrations: a
test using senescent tree leaves. Remote Sensing of Environment, 19, 657-675.
Bowes G. 1993, Facing the inevitable: plants and increasing atmospheric CO2. Annual Review of
Plant Physiology and Plant Molecular Biology, 44, 309-332.
270
Drake B G, Gonzalez-Meler M A, Long S P. 1997, More efficient plants: a consequence of rising
271
atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology, 48,
272
609-639.
273
Hao X Y. 2014, Effects of elevated [CO2] on major crops of china, Meteorological press, Beijing.
274
Hao X Y, Gao J, Han X, Ma Z Y, Merchant A, Ju H, Li P, Yang W S, Gao Z Q, Lin E D. 2014,
275
Effects of open-air elevated atmospheric CO2 concentration on yield quality of soybean
276
(Glycine max (L.) Merr). Agriculture Ecosystems & Environment, 192, 80-84.
277
Hao X Y, Han X, Lam S K, Wheeler T, Ju H, Li P, Lin E D. 2012, Effects of fully open-air [CO2]
278
elevation on leaf ultrastructure, photosynthesis, and yield of two soybean cultivars.
279
Photosynthetica, 50, 362-370.
280
Hao X Y, Han X, Li P, Yang H B, Lin E D. 2011, Effects of elevated atmospheric CO2
281
concentration on mung bean leaf photosynthesis and chlorophyll fluorescence parameters.
282
Chinese Journal of Applied Ecology, 22, 2776-2780 (in Chinese).
283
Hao X Y, Li P, Feng Y X, Han X, Gao J, Lin E D, Han Y H. 2013, Effects of fully open-air [CO2]
284
elevation on leaf photosynthesis and ultrastructure of Isatis indigotica Fort. Plos ONE, 8, 1-7.
285
IPCC. 2007, Climate Change 2007: the Physical Science Basis. Contribution of Panel on Climate
286
Change. Cambridge University Press, Cambridge and New Working Group I to the Fourth
287
Assessment Report of the Intergovernmental
288
York.
289
Jiang Y L, Yao Y G, Zhang Q G, Yue W, Chen T F, Fan L L. 2006, Changes of photosynthetic
290
pigment contents in soybean under elevated atmospheric CO2 concentrations. Crop Research,
291
2, 144-146 (in Chinese).
292
Leakey A D B, Bernacchi C J, Ort D R, Long S P. 2006, Long-term growth of soybean at elevated
293
[CO2] does not cause acclimation of stomatal conductance under fully open-air conditions.
294
Plant Cell and Environment, 29, 1794-1800.
295
296
Long S P, Ainsworth E A, Rogers A, Ort D R. 2004, Rising atmospheric carbon dioxide: plants
FACE the future. Annual Review of Plant Biology, 55, 591-628.
297
Major J E, Barsi DY, Mosseler A, Campbell M. 2007, Genetic variation and control of chloroplast
298
pigment concentrations in Picea rubens, Picea mariana and their hybrids. I. Ambient and
299
elevated [CO2] environments. Tree Physiology, 27, 353-364.
300
301
McLeod A R, Long S P. 1999, Free-air carbon dioxide enrichment (FACE) in global change
research: A review. Advances in Ecological Research, 28, 1-56.
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
302
Myers D A, Thomas R B, Delucia E H. 1999, Photosynthetic capacity of loblolly pine (Pinus
303
taeda L) trees during the first year of carbon dioxide enrichment in a forest ecosystem. Plant
304
Cell and Environment, 22, 473-481.
305
Rascher U, Bobich E G, Lin G H, Walter A, Morris T. 2004, Functional diversity of
306
photosynthesis during drought in a model tropical rainforest-the contributions of leaf area,
307
photosynthetic electron transport and stomatal conductance to reduction in net ecosystem
308
carbon exchange. Plant Cell and Environment, 27, 1239-1256.
309
310
311
Rohacek K. 2002, Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning,
and mutual relationships. Photosynthetica, 40, 13-29.
Seneweera S, Makino A, Mae T. Basra S A. 2005, Response of rice to p(CO2) enrichment: the
312
relationship between photosynthesis and nigrogen metabolism. Journal of Crop Improvement,
313
13,31-53.
314
Sharkey T D, Bernacchi T D, Farquhar G D, Singsaas E L. 2007, Fitting photosynthetic carbon
315
dioxide response curves for C3 leaves. Plant Cell and Environment, 30, 1035–1040.
316
Strogonov B P. 1973, Structure and function of plant cell in saline habitats. Halsted Press, New
317
York.
318
Tausz-Posch S, Borowiak K, Dempsey R W, Norton R M, Seneweera S. 2013, The effect of
319
elevated CO2 on photochemistry and antioxidative defence capacity in wheat depends on
320
environmental growing conditions- A FACE study. Environmental and Experimental Botany,
321
88, 81-92.
322
Yuan X X, Lin X G, Ghu H Y, Yin R, Wang J H. 2007, Effects of double CO2 on AM fungi and
323
inoculation effects on Green gram. Journal Agro-Environmental Science, 26, 211-215(in
324
Chinese).
325
Zhang X W, Shang P P, Qin F, Zhou Q, Gao B Y. 2013, Chemical composition and antioxidative
326
and anti-inflammatory properties of ten commercial mung bean samples. LWT-Food Science
327
and Technology, 54, 171-178.
328
Zhao T H, Shi Y, Huang G H. 2003, Effect of doubled CO2 and O3 concentration and their
329
interactions on ultrastructure of soybean chloroplast. Chinese Journal of Applied Ecology, 14,
330
2229-2232 (in Chinese).
331
332
333
334
335
336
337
338
339
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
340
341
自由大气CO2浓度升高对绿豆光合生理及产量的影响
342
343
344
高霁 1,2*, 韩 1*, Saman Seneweera3, 李萍 2, 宗毓铮 2, 董琪 2, 林而达 1, 郝兴宇 1,2
345
1. 中国农业科学院农业环境与可持续发展研究所，北京 100081
346
2. 山西农业大学农学院，山西太谷 030801
347
3. Centre for Systems Biology, University of Southern, Toowoomba, Queensland, QLD
348
4350, Australia
349
350
351
中文摘要：
352
绿豆根系可以与根瘤菌建立共生体，共生体可能会影响绿豆光合作用和生长对大气 CO2
353
浓度升高响应。本研究在中国北方 FACE 系统（自由大气 CO2 富集系统）平台开展大气 CO2
354
浓度升高对绿豆影响试验研究，大气 CO2 浓度设对照浓度（400 mol mol–1）和高 CO2 浓度
355
(550  17 mol mol–1)。分别对绿豆叶片光合色素含量、光合作用、叶绿素荧光参数、生物量
356
和产量进行了测定。大气 CO2 浓度升高使绿豆生物量提高 11.6%，产量提高 14.2%。大气
357
CO2 浓度升高后，绿豆叶片叶绿素 a 和总叶绿素含量分别增加 10.9% 和 10.6%，而叶绿素 b
358
和类胡萝卜素含量无显著变化。大气 CO2 浓度升高使绿豆叶片净光合速率(PN)、水分利用率
359
(WUE)、非光化学猝灭系数(NPQ)增加，使叶片气孔导度(gs)、光下光系统Ⅱ的捕获效率
360
(Fv'/Fm')、光系统Ⅱ的实际量子效率(ΦPSⅡ)、光化学猝灭系数(qP)下降。大气 CO2 浓度升
361
高后，开花期光下光系统Ⅱ的捕获效率(Fv'/Fm')、光系统Ⅱ的实际量子效率(ΦPSⅡ)、光化
362
学猝灭系数(qP)的降幅要小于荚期。与之对应的是净光合作用在开花期(R2)增加 18.7%，荚
363
期(R4)仅增加 7.4%。绿豆作为豆科作物可以通过根瘤固氮提高氮素营养，但氮同化任然不
364
能满足高 CO2 浓度条件下的植物碳同化需求，导致光合能力下调，且在生长后期更明显。
365
366
367
368
369
370
371
372
373
关键词：自由大气 CO2 富集(FACE)，光合色素，光合作用，叶绿素荧光，产量，绿豆
Journal of Integrative Agriculture
Advanced Online Publication: 2015
*
g -1)
Chl b(mg·
Chl a (mg·g-1)
2
Doi: 10.1016/S2095-3119(14)60941-2
1.5
1
0.5
2.5
*
Carotenoid(μg·g-1)
Total Chl(mg·g-1)
0
2
1.5
1
0.5
0
40
58
ambient
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0.6
0.5
0.4
0.3
0.2
0.1
0
40
Days after sowing ( day )
Fig. 1
376
Weight per square meter（g）
Fig. 1 Photosynthetic pigment contents of per fresh weight mung bean leaf grown in ambient and
FACE plots. Each bar represents the standard error of the difference between treatments (n=3). *, P
≤0.05. The same as below.
1200
*
ambient
FACE
1000
800
600
*
400
200
0
Biomass
Yield
382
383
Fig. 2
384
385
386
387
388
389
58
Days after sowing ( day )
374
375
377
378
379
380
381
FACE
Fig. 2. Effects of elevated [CO2] on biomass and yield per square meter.
Journal of Integrative Agriculture
Advanced Online Publication: 2015
Doi: 10.1016/S2095-3119(14)60941-2
390
391
392
393
394
Table 1. Effects of elevated [CO2] on gas exchange parameters in the last fully-expanded leaves of
mung bean at 40 and 58 days after sowing.
Days after
Growth
sowing（d） [CO2]
40
58
P values
[mol(CO2)
–2 –1
m s ]
gs
[mol(H2
O)m–2
s–1]
Tr
WUE
–2
[mol m
–1
[mol
–1
s ]
mmol ]
Jmax
Vcmax
[molm–2 s–1]
[molm–2
–1
s ]
ambient
21.67±0.79
1.33±0.10
11.15±1.02
2.02±0.25
84.61±3.31
107.79±3.59
FACE
25.72±0.02
1.08±0.03
9.41±1.10
2.80±0.30
90.79±2.93
117.37±1.62
ambient
30.63±0.52
1.22±0.08
9.29±0.46
3.32±0.21
112.40±4.23
142.27±14.12
FACE
32.90±0.65
1.05±0.04
8.30±0.36
3.98±0.16
110.90±4.02
142.12±8.84
0.00
0.35
0.10
0.00
0.00
0.05
0.00
0.02
0.13
0.01
0.26
0.24
0.16
0.54
0.66
0.75
0.17
0.23
Growth
stage
CO2
Growth
stage*CO2
395
396
397
398
399
400
401
402
403
404
405
406
407
408
409
410
411
412
413
414
415
416
417
418
419
420
PN
Measurement was taken on their growth [CO2] concentration. Values are means ±standard error of
variables across the three replicates; three plants were tested in each plot (three FACE plots and
three ambient plots). The statistical significance level for the effects of [CO2] treatment, growth
stage and their interaction was tested. PN - net photosynthetic rate; gs- stomatal conductance; Tr transpiration ratio; WUE- water use efficiency.
Journal of Integrative Agriculture
Advanced Online Publication: 2015
421
422
423
424
Doi: 10.1016/S2095-3119(14)60941-2
Journal of Integrative Agriculture
Advanced Online Publication: 2015
425
426
427
Table 2. Effects of elevated [CO2] on chlorophyll fluorescence parameters in the last
fully-expanded leaves of mung bean at 40 and 58 days after sowing.
Days after
Growth
Sowing（d）
[CO2]
40
58
P values
Fv/Fm
Fv'/Fm'
ΦPSⅡ
qP
NPQ
ambient
0.83±0.00
0.58±0.01
0.38±0.01
0.65±0.02
1.26±0.07
FACE
0.83±0.01
0.56±0.02
0.37±0.02
0.65±0.01
1.42±0.10
ambient
0.80±0.01
0.55±0.03
0.36±0.04
0.64±0.03
1.11±0.18
FACE
0.78±0.04
0.47±0.02
0.23±0.02
0.49±0.02
1.42±0.07
growth stage
0.07
0.02
0.00
0.00
0.97
CO2
0.46
0.05
0.01
0.00
0.03
0.57
0.20
0.02
0.00
0.21
Growth
stage*CO2
428
429
430
431
432
433
434
435
436
437
438
439
440
441
442
443
444
445
446
447
448
449
450
451
452
453
454
455
456
457
458
459
Doi: 10.1016/S2095-3119(14)60941-2
Values are means ± standard error of variables across the three replicates; nine plants were taken
in each plot (three FACE plots and three ambient plots). The statistical significance level for the
effects of [CO2] treatment, growth stage and their interaction was tested. Fv/Fm- maximum
quantum efficiency of PSⅡ; Fv'/Fm'- intrinsic efficiency of PSⅡ; ΦPSⅡ- quantum yield of PSⅡ;
NPQ- non-photochemical quenching; qp- proportion of open PSⅡ reaction centers.
Journal of Integrative Agriculture
Advanced Online Publication: 2015
460
461
462
463
464
465
466
Doi: 10.1016/S2095-3119(14)60941-2
Table 3.Yield components of mung bean grown under ambient and FACE conditions.
the number of pods
the number of seeds
the weight of 100 seeds
Growth [CO2]
per plant
per pod
[g]
Ambient
15.93±1.31
7.63±0.16
6.57±0.26
FACE
18.13±0.48
8.53±0.15
6.50±0.19
P values
0.19
0.02
0.86
Measurements were taken under ambient and elevated [CO2]. Values are means ± standard error
of variables across the three replicates.