Plant Science 181 (2011) 428–438
Contents lists available at ScienceDirect
Plant Science journal homepage: www.elsevier.com/locate/plantsci
Responses of Gmelina arborea, a tropical deciduous tree species, to elevated atmospheric CO2 : Growth, biomass productivity and carbon sequestration efﬁcacy Girish K. Rasineni, Anirban Guha, Attipalli R. Reddy ∗ Photosynthesis and Plant Stress Biology Laboratory, Department of Plant Sciences, University of Hyderabad, Hyderabad 500 046, India
a r t i c l e
i n f o
Article history: Received 24 March 2011 Received in revised form 2 July 2011 Accepted 11 July 2011 Available online 26 July 2011 Keywords: Biomass yields Carbon sequestration Elevated CO2 Gmelina arborea Productivity
a b s t r a c t The photosynthetic response of trees to rising CO2 concentrations largely depends on source–sink relations, in addition to differences in responsiveness by species, genotype, and functional group. Previous studies on elevated CO2 responses in trees have either doubled the gas concentration (>700 mol mol−1 ) or used single large addition of CO2 (500–600 mol mol−1 ). In this study, Gmelina arborea, a fast growing tropical deciduous tree species, was selected to determine the photosynthetic efﬁciency, growth response and overall source–sink relations under near elevated atmospheric CO2 concentration (460 mol mol−1 ). Net photosynthetic rate of Gmelina was ∼30% higher in plants grown in elevated CO2 compared with ambient CO2 -grown plants. The elevated CO2 concentration also had signiﬁcant effect on photochemical and biochemical capacities evidenced by changes in FV /FM , ABS/CSm, ET0 /CSm and RuBPcase activity. The study also revealed that elevated CO2 conditions signiﬁcantly increased absolute growth rate, above ground biomass and carbon sequestration potential in Gmelina which sequestered ∼2100 g tree−1 carbon after 120 days of treatment when compared to ambient CO2 -grown plants. Our data indicate that young Gmelina could accumulate signiﬁcant biomass and escape acclimatory down-regulation of photosynthesis due to high source-sink capacity even with an increase of 100 mol mol−1 CO2 . © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction One of the major issues of global concern today is rapidly increasing levels of CO2 (at 2 mol mol−1 year−1 ) in the atmosphere and its potential to change the world climate . The rising CO2 levels have severe implications on the functioning of physical and biological systems of the world. In this context, International Panel on Climate Change (IPCC) advocated an increase in the size of the carbon sinks in order to reduce the green house effect [1,2]. The Kyoto protocol of 1997 also focused on reducing carbon dioxide emission and stabilization of atmospheric CO2 by a combination of limitation on the use of fossil fuel and creation of carbon sinks within a speciﬁed time frame [3,4]. Plants act as carbon sinks by ﬁxing carbon through photosynthesis and the recent focus has been on terrestrial vegetation to facilitate efﬁcient carbon sequestration [1,2,5]. Forest ecosystems contain the majority (approximately 60%) of the carbon stored in terrestrial ecosystems and thus sequester and conserve more carbon than all other terrestrial ecosystems. Forest trees have potential to capture and retain large volumes of carbon over long periods [7–9] and account for
∗ Corresponding author. Tel.: +91 40 23134508; fax: +91 40 23010120. E-mail address: [email protected]
(A.R. Reddy). 0168-9452/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2011.07.005
90% of the annual carbon ﬂux between atmosphere and the earth’s land surface [2,6]. Globally, forest area has been reduced by almost 20% in the last 140 years, leading to an increase in deforestation-related CO2 emissions. This deforestation related CO2 emission accounts for about 20% of the total anthropogenic emissions . Planting forests (afforestation and reforestation) clearly provide an opportunity to sequester more carbon. Present estimates indicate that with appropriate policies, the carbon pool in the terrestrial system could increase by up to 100 gigatonnes (metric) of carbon dioxide (GtC) by the year 2050 compared to the level of carbon that would be sequestered without such policies . This is equivalent to about 10–20% of projected green house gases (GHG) emissions from fossil fuel consumption during the same period. Reducing deforestation, expanding forest cover and forest biomass per unit area are some of the activities that can help global community from global warming . Carbon sequestration as a climate change mitigation policy had received signiﬁcant attention over the past several years. Planting young fast growing trees species to absorb excess atmospheric CO2 , an idea of carbon offset plantings , has recently gained potentiality, leading to identiﬁcation of tree species with high CO2 sequestration capacity. The growing concern about the consequences of burning fossil fuels on the global climate system also enhanced the attention for short-rotation forestry (SRF)
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
during the last decade. Short rotation production systems employ densely planted and rapidly growing woody plants to produce huge dry matter product within a short time span as opposed to traditional forest management. Understanding the responses of these fast growing short rotation tree species to rising atmospheric CO2 concentration is of considerable importance for their implication in CO2 sequestration programmes . Elevated CO2 may act as a fertilizer, stimulating plant growth and accelerating development . Even though, there has been large amount of research done with elevated CO2 effects on forest trees, it remains difﬁcult to predict future tree growth and productivity under elevated atmospheric CO2 . A driving and largely unanswered question in the study of the effects of climate change on trees is whether biomass production will be increased as a result of increasing atmospheric CO2 concentrations. This uncertainty arises for several reasons: some trees have shown signiﬁcant enhancement in photosynthesis (net photosynthetic rates of trees grown in elevated CO2 have been shown to increase by up to 50%) and biomass gain under high CO2 [7,12]. However, many tree species grown at elevated CO2 exhibit an acclamatory downregulation, decreasing photosynthetic potential, particularly with long-term growth in elevated CO2 . Hence, tree species responses are largely uncertain due to differences in responsiveness by species, genotype, and functional group. Earlier studies on carbon sequestration efﬁcacy of plants have focussed on fast growing tropical deciduous trees which exhibit a different response than evergreens. In rapidly growing tropical deciduous angiosperm trees, the rate of photosynthesis typically accelerates in spring as trees refoliate, remains high during the summer, and declines in late summer as leaves senescence before abscising. Such existing phenological differences in tropical deciduous trees when compared to evergreens result in signiﬁcant differences in the overall source–sink relations of trees, which reduce the likelihood of photosynthetic down-regulation of fast-growing deciduous trees under elevated CO2 conditions. Almost all studies of elevated CO2 responses in tropical deciduous trees have either doubled the gas concentration (>600 mol mol−1 ) or done on a single large addition (500–600 mol mol−1 ). Little consideration has been given to understand the impact of a slightly higher increment in CO2 concentration on the growth and biomass productivity of such tropical deciduous trees. Further, there is little information on the photochemical efﬁciency of such tropical deciduous trees when grown under slightly higher CO2 increment [14–18]. In the present study, we selected young fast growing Gmelina arborea which represents a typical deciduous tree species of tropics. We examined whether young Gmelina, grown throughout a complete production cycle (spring and summer) under slightly higher increment in CO2 (460 mol mol−1 ; just a 100 mol mol−1 more CO2 above ambient) show positive evidence in terms of photochemical efﬁciency, growth and biomass productivity as reported in case of other tropical deciduous trees studied mostly under excessively high CO2 atmosphere. We also assessed the robustness of the relationships between biomass productivity and various physio-biochemical traits under elevated CO2 conditions to understand the overall source–sink relations in such tropical deciduous trees and the likelihood of photosynthetic up-regulation during their growth seasons under slightly elevated CO2 conditions.
2. Materials and methods 2.1. Plant material, experimental design and growth conditions One month old healthy rooted saplings of G. arborea were used for CO2 enrichment experiments. The study was conducted in the experimental ﬁeld of University of Hyderabad, India located
between 17.3◦ 10 N and 78◦ 23 E at an altitude of 542.6 m above mean sea level (MSL). Rectangular open top chambers (OTCs) were constructed with steel frame having dimensions of 4 m × 4 m × 4 m covered with polycarbonate sheet (Polygal Plastic Industries Ltd., Israel) of 4 mm thickness. OTCs were equipped with temperature, humidity and rainfall sensors. Each chamber was connected with Cu piping through which CO2 was pumped from cylinders under controlled manner. Independent pipes were drawn from each chamber and connected to non-dispersion infra ray (NDIR) gas analyzer (Fuji Electric Systems Co. Ltd., Japan) to set and monitor the desired CO2 levels. A PLC-SCADA based platform was designed for controlling continuous operation of CO2 levels. In each OTC, four Gmelina plants were planted in four pits with a spacing of 2 m × 2 m at the onset of spring (February). Saplings were allowed to establish inside the OTCs for 10 days and thereafter, CO2 treatment was started. The mean CO2 concentration in the ambient CO2 chamber was ∼360 mol mol−1 and ranged from 340 to 380 mol mol−1 depending on weather conditions whereas the mean CO2 concentration in elevated CO2 chamber was maintained at ∼460 mol mol−1 . Gmelina has a phenology of a typical tropical deciduous tree species. It starts leaf ﬂushing with the advent of the spring, grows luxuriantly throughout late spring and summer seasons and undergoes complete senescence in winter. Our study intended to investigate elevated CO2 induced response in Gmelina during a complete production cycle (spring and summer); hence, all measurements and data collection in Gmelina were conﬁned to six months covering two marked growth seasons: spring (February–April) and summer (May–July) for three consecutive years (2007–2009) which included three experimental harvests. Throughout the experiment, the soil moisture content (SMC) at the rooting zone (30–50 cm soil depth) was maintained at 80–85% by means of surface irrigation at regular interval. In both the OTCs, duration of irrigation was increased during the hottest months (April–June) to compensate higher evapotranspirational moisture loss and SMC was uniformly maintained within a range of 80–85% so that the plants grew under optimal water conditions. Farmyard manure (FYM) was applied at the rate of 40 kg plant−1 in two equal splits (at the time of sapling plantation and after three months of growth). The soil had a red sandy loam texture and a pH of 7.5. Soil organic carbon content (SOC) was ∼0.82% and soil available nitrogen was ∼518 kg ha−1 . Important soil physicochemical characteristics in the two OTCs (ambient and elevated) measured during three experimental years are provided in supplementary Table 1. Soils conditions in both the OTCs were regularly monitored and no statistically signiﬁcant differences in soil characteristics were recorded between two OTC’s. Weeds inside the OTCs were removed manually and no pest or disease incidence was observed during our experimental seasons. 2.2. Photosynthetic gas exchange measurements Photosynthetic leaf gas exchange characteristics were measured using a portable infrared CO2 /H2 O gas analyzer (IRGA) (LC Pro+, ADC Bioscientiﬁc Ltd., U.K.) equipped with a broad leaf chamber. The instrument allows determination of gaseous exchange by individual leaf enclosed in leaf chamber over time. The gas analyzer was used to measure instantaneous net photosynthetic rates (Pn ; mol m−2 s−1 ), stomatal conductance to CO2 (gs ; mol m−2 s−1 ) and transpiration rates (E; mmol m−2 s−1 ), periodically during each growing season between 10:00 and 11:00 h solar time. The instant water use efﬁciency (WUEi ) was also calculated (WUEi = Pn /E; mmol CO2 mol−1 H2 O). Both Pn and gs were expressed on a projected leaf area basis which was measured with an automatic image analyzer. Once a leaf was enclosed in the chamber, an incubation time of 2 min was given to the leaf to re-adjust to its new
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
microclimate and the measurements were recorded thereafter. All photosynthetic measurements were performed in situ on young, well-expanded and light-exposed leaves randomly chosen from the upper half of the plant canopy. The incident photosynthetically active radiation (PAR) on leaf while taking gas exchange measurements (10:00–11:00 h solar time) ranged from 800 to 1000 mol m−2 s−1 in spring and from 1600 to 1800 mol m−2 s−1 in summer. PAR was measured using a silicon based PAR sensor (LCpro-32070) attached to the leaf chamber. Monthly averages of air temperature (◦ C), rainfall (mm), relative humidity (%) and PAR (mol m−2 s−1 ) at the study site for two growing seasons; spring (February–April) and summer (May–July) during three consecutive years (2007–2009) are presented in supplementary Fig. 1. 2.3. RuBPcase activity Extraction of RuBPcase and activity measurements were performed according to Cheng and Fuchigami . Fresh leaf tissue (2 g) was homogenised in 3 ml extraction buffer containing 100 mM bicine (pH 7.8), 5 mM EDTA, 0.75% (w/v) polyethylene glycol (20,000), 14 mM ␤-mercaptoethanol, 1% (v/v) Tween 80, and 1.5% (w/v) insoluble PVPP. The homogenate was centrifuged at 18,000 × g for 5 min and the supernatant was used immediately for assaying RuBPcase activity. Activity of RuBPcase was measured at 25 ◦ C by enzymatically coupling RuBP carboxylation to NADH oxidation which was monitored at 340 nm in a Shimadzu UV-160 spectrophotometer. For initial RuBPcase activity, a 50 l sample extract was added to a semi-microcuvette containing 900 l of an assay solution, followed by immediate addition of 50 l of 0.5 mM RuBP. For total RuBPcase activity (i.e. the activity following preincubation with CO2 and Mg2+ ) 50 l of 0.5 mM RuBP was added 15 min later, after a sample extract was combined with the assay solution to fully activate RuBPcase. The assay solution for both initial and total activity measurements contained: 100 mM bicine (pH 8.0), 25 mM KHCO3 , 20 mM MgCl2 , 3.5 mM ATP, 5 mM phosphocreatine, 80 nkat glyceraldehyde-3-phosphatedehydrogenase, 80 nkat 3-phospho-glyceric kinase, 80 nkat creatine phosphokinase and 0.25 mM NADH. 2.4. Chlorophyll a ﬂuorescence measurements Chlorophyll a ﬂuorescence measurements were made with the Plant Efﬁciency Analyser, PEA (Hansatech instruments Ltd., King’s Lynn, Norfolk, England). Measurements were performed on healthy top intact leaves (same leaves which were used for gas exchange measurements) grown under ambient and elevated CO2 treatments at 90 and 120 days after plantation (DAP). The leaves were initially pre-darkened with clips for 20 min prior to measurements and thereafter chlorophyll a ﬂuorescence transients of dark-adapted leaves were measured. The transients were induced by 1 s illumination with an array of three light emitting diodes providing a maximum light intensity of 3000 mol (photon) m−2 s−1 as a homogenous irradiation over a 4 mm diameter leaf area. The fast ﬂuorescence kinetics (f0 to fM ) was recorded from 50 s to 1 s and the ﬂuorescence intensity at 50 s was considered as f0 . 2.5. Analysis of the ﬂuorescence transients using the JIP-test Raw ﬂuorescence OJIP transients were transferred with WINPEA 32 software and BiolyzerP3 to a spreadsheet [21,22]. The translation of the measured parameters into JIP-test parameters provided information on the stepwise ﬂow of energy through PS II at different levels such as phenomenological ﬂuxes on the level of the excited leaf cross-section (CS) [absorption (ABS/CSm), trapping (TR0/CSm), dissipation (DI0/CSm) and electron transport (ET0/CSm)]. The performance index (PI) was calculated as combined measurement of
the amount of photosynthetic reaction centres (RC/ABS), the maximal energy ﬂux which reaches to the PS II reaction centres and the electron transport at the onset of illumination was calculated using the formula: PIABS =
RC Eo ˚Po · · ABS 1 − ˚Po 1 − Eo
2.6. Non-destructive measurements Non-destructive measurements were made on the developing shoots at approximately 25–30 days intervals. The height (cm) of the main stem (measured vertically from soil surface till apical meristem) of each tree was measured with a ruler. In addition, the main stem diameter was measured at a consistent point (0.5 cm above the base of the stem) using callipers. Plant height growth rate (PHGR, cm day−1 ) and stem diameter growth rate (SDGR, cm day−1 ) were also calculated. 2.7. Destructive harvest and biomass determination Total plant biomass was determined destructively on four successive harvest dates (30, 60, 90 and 120 days from the start of the experiment) using four trees per chamber which were selected at random from within the four plants in each chamber. At each harvest, plants were separated into leaves and stems. Fresh weight was measured immediately after harvest and dry weights of stems and leaves were obtained after oven drying for 48 h at 85 ◦ C. Soil was then excavated so that roots could be separated from soil and collected from 1 m × 1 m × 1 m volume around the plant base. The roots were brought to the laboratory to enable pieces of soil particles to be removed by hand, the fresh weights were taken and was then oven dried to obtain dry weights. The above-ground and root biomass were added to derive total plant biomass. Absolute growth rate (AGR: the rate of increase in dry matter per plant per unit time) was calculated according to Radford . AGR = (W2 − W1 )/(t2 − t1 ) where W1 = dry weight (mass) of plant in g at time t1 ; and W2 = dry weight (mass) of plant in g at time t2 . AGR was expressed in g plant−1 day−1 . Relative height growth rate (RHGR) and stem basal diameter growth rate (SDGR) were calculated every month: RHGR = (H2 − H1 )/(t2 − t1 ) where H1 = height of the plant in cm at time t1 and H2 = height of the plant in cm at time t2 ; SDGR = (D2 − D1 )/(t2 − t1 ) where D1 = basal diameter in cm at time t1 and D2 = basal diameter in cm at time t2 . 2.8. Carbon content in above ground biomass The estimation of the above ground biomass and carbon content in the stem was determined using the tree height, diameter and basal girth of the tree. Weight of the woody biomass was calculated by multiplying volume of biomass and speciﬁc gravity (SG) of the stem wood. Volume of individual trees was estimated according to Newbould : volume = basal area × total height × 0.5. The above ground biomass stock and above ground carbon of the trees was calculated using volume of biomass and speciﬁc gravity of the trees according to Rajput et al.  and Negi et al. . Biomass (g) = volume of biomass (m3 ) × speciﬁc gravity (SG), where SG = oven dry weight/green volume. The average carbon content was generally 50% of the tree’s biomass and the carbon dioxide sequestered by tree was calculated as the weight of carbon in the tree × 3.663. 2.9. Statistical analysis The data presented on height, biomass parameters and AGR are the mean ± SE of three years (2007–2009) of repeated exper-
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Table 1 Photosynthetic characteristics as inﬂuenced by CO2 (ambient, 360 mol mol−1 ; elevated, 460 mol mol−1 ) in young Gmelina arborea recorded during two growth seasons (spring and summer) at periodic intervals (DAP, days after plantation). The parameters investigated were photosynthetic rate (Pn ), stomatal conductance (gs ), transpiration rate (E) and instantaneous water use efﬁciency (WUEi). Values are the mean ± standard deviation. Effects of CO2 were tested by paired t-test.
30 DAP Ambient Elevated 60 DAP Ambient Elevated 90 DAP Ambient Elevated 120DAP Ambient Elevated
Pn (mol m−2 s−1 )
gs (mol m−2 s−1 )
E (mmol m−2 s−1 )
WUEi (mmol CO2 mol−1 H2 O)
10.9 ± 0.7 10.8 ± 0.6 n.s.
0.34 ± 0.02 0.36 ± 0.01 n.s.
4.9 ± 0.6 5.1 ± 0.4 n.s.
2.2 ± 0.2 2.0 ± 0.1 n.s.
17.9 ± 0.7 18.7 ± 0.6 n.s.
0.37 ± 0.03 0.32 ± 0.02*
5.1 ± 0.4 4.9 ± 0.4n.s.
3.5 ± 0.2 3.8 ± 0.2n.s.
24.9 ± 0.4 28.6 ± 0.9**
0.38 ± 0.03 0.29 ± 0.02**
5.2 ± 0.5 4.4 ± 0.5**
4.7 ± 0.6 6.4 ± 0.2**
25.3 ± 0.8 34.9 ± 0.9***
0.39 ± 0.02 0.26 ± 0.02**
5.4 ± 0.6 4.0 ± 0.3**
4.6 ± 0.4 8.6 ± 0.3***
n.s., not signiﬁcant. ** p < 0.01. *** p < 0.001.
iments. Further, growth and biomass data were analyzed using non-parametric Kolmogorov–Smirnov (KS) test to detect statistically signiﬁcant differences between the means of those tested variables from ambient and elevated CO2 conditions. KS test was performed using statistical package OriginPro8. Growth and biomass data were also analyzed by two-way analysis of variance (ANOVA) with CO2 and time of treatment as the main factors. Data on photosynthetic parameters and RuBPcase activity are represented as mean ± SE of three years’ (2007–2009) experiments. To determine signiﬁcance of differences between mean values of physiological, chlorophyll ﬂuorescence and biochemical parameters of plants grown under ambient and elevated CO2 plants we used parametric analysis (paired t-test) as number of observations were high (n = 20–30). Correlation coefﬁcient (r) of linear relationships between the investigated parameters was established using linear regression analysis. The linear regression slopes were analyzed using bivariate correlation signiﬁcance tests. Parametric tests and regression analysis were performed using statistical package Sigma Plot 11.0.
grown at ambient CO2 concentration (Table 1). The Pn of Gmelina under ambient and high CO2 atmosphere at 30 DAP showed no signiﬁcant difference and Pn was ∼10.4 mol mol−1 . However at 120 DAP, a signiﬁcant increase in Pn (p < 0.001) of ∼30% was observed in high CO2 -grown plants (34.9 mol m−2 s−1 ) compared to ambient CO2 -grown plants, while the gs and E decreased (p < 0.05) in the plants grown under elevated CO2 atmosphere. During 30 DAP, gs was recorded as ∼0.35 mol m−2 s−1 in high CO2 plants but at 120 DAP, the gs was ∼0.25 mol m−2 s−1 showing a reduction of ∼30% compared to ambient CO2 -grown plants (Table 1). A reduction of ∼25% in the rates of E in CO2 -enriched plants was observed at 120 DAP when compared to those in ambient grown counterparts. A progressive increasing trend in WUEi was recorded in ambient as well as high CO2 -grown plants. WUEi was signiﬁcantly more in CO2 -enriched Gmelina, depicting a signiﬁcant increase of ∼46.5% (p < 0.001), compared to ambient CO2 -grown plants (Table 1).
The initial and total RuBPcase activity in the leaf samples for Gmelina grown under ambient and elevated CO2 were shown in Fig. 1A and B. Initial and total RuBPcase activity increased progressively during 120 days of treatment. At 120 DAP, Gmelina plants grown under elevated CO2 , showed signiﬁcantly high initial (∼35.7 mol mg−1 protein h−1 ; p < 0.001) and total RuBPcase
3.1. Photosynthetic leaf gas exchange CO2 enrichment had a profound inﬂuence on the gas exchange physiology of young Gmelina when compared to its counterparts
3.2. RuBPcase activity
Fig. 1. Initial (A) and total activity (B) of RuBPcase in leaves of Gmelina grown at ambient and elevated CO2 concentrations. Activities were determined at regular intervals during 120 days treatment. Values are the mean ± S.E. Inset (C) and (D) depict correlation analysis between initial activity of RuBPcase and photosynthetic rates Pn (C), ﬁnal activity of RuBPcase and photosynthetic rates Pn (D) in young Gmelina under ambient and elevated CO2 conditions (, ambient; 䊉, elevated).
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Fig. 2. Chlorophyll a ﬂuorescence characteristics during 90 and 120 days after plantation (DAP) in the leaves of Gmelina arborea. (FV /FM ) (A); phenomenological ﬂux parameters including ABS/CSm (B), TRo/CSm (C), ETo/CSm (D), DIo/CSm (E), PI (ABS) (F). Energy pipeline models per excited cross-section in Gmelina leaves grown under ambient (G) and elevated CO2 (H) atmosphere.
activity (∼46.11 mol mg−1 protein h−1 ; p < 0.001) when compared to the plants grown under ambient CO2 conditions. The values of Pn and RuBPcase initial activities when plotted together showed a strong positive correlation (r2 = 0.95, p < 0.001) under elevated CO2 (Fig. 1C). Strong positive correlation (r2 = 0.95, p < 0.001) was also recorded between Pn and total activity of RuBPcase under elevated CO2 -grown Gmelina (Fig. 1D).
The dissipation rate (DI0 /CSm) was found to be signiﬁcantly low (p < 0.0; Fig. 2E) in elevated CO2 grown plants. The overall performance of PSII assessed by performance index on absorption basis (PIAbs ) was signiﬁcantly high (∼45%, p < 0.001) in plants grown under elevated CO2 -atmosphere (Fig. 2F). The dynamic leaf models of Gmelina grown under elevated CO2 showed more number of active RCs in PSII cross section (Fig. 2H) when compared to ambient CO2 -grown plants (Fig. 2G).
3.3. Chlorophyll a ﬂuorescence 3.4. Non-destructive growth characteristics There was a signiﬁcant effect of elevated CO2 on chlorophyll a ﬂuorescence characteristics. At elevated CO2 conditions the FV /FM ratios were slightly high (∼13%, p < 0.05) when compared to ambient CO2 -grown plants. The FV /FM ratio was ∼0.70 in elevated CO2 -grown plants, whereas in ambient CO2 -grown plants showed FV /FM of ∼0.62 (Fig. 2A). Interestingly, plants grown under ambient CO2 -conditions showed slightly high ABS/CSm (p < 0.05; Fig. 2B) and TR0 /CSm (p < 0.05; Fig. 2C) compared to those grown under elevated CO2 . Electron transport in PSII cross-section (ET0 /CSm) (p < 0.001; Fig. 2D) was signiﬁcantly high (p < 0.001) in elevated CO2 -grown plants compared to ambient CO2 -grown counterparts.
Plant height was signiﬁcantly (p < 0.001) increased after 90 days growth in elevated CO2 atmosphere (Fig. 3A), and the increment continued until ﬁnal harvest (120 DAP) as the trees were ﬁnally ∼42% taller than those grown in ambient CO2 concentrations (Fig. 3A). The basal stem diameter at 120 DAP in elevated CO2 -grown plants was ∼28 cm which was ∼52% more compared to ambient CO2 -grown plants (Fig. 3B). Plants grown under elevated CO2 atmosphere showed signiﬁcantly higher PHGR (∼40%, p < 0.001) when compared to ambient CO2 -grown plants (Fig. 3C). SDGR was signiﬁcantly (p < 0.001) higher on 60 DAP in plants
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Fig. 3. Comparative growth morphology of Gmelina arborea grown in OTCs under ambient and elevated CO2 atmosphere. Plant height (A) and basal stem diameter (B). Signiﬁcantly enhanced plant height growth rate (cm day−1 ) is depicted in the inset (C); stem diameter growth rate (cm day−1 ). (D) Morphology of ﬁve-month-old Gmelina arborea plants grown in open top chambers under ambient (E) and elevated (F) CO2 concentrations. Inset (G) and (H) depict one-month-old Gmelina grown under ambient and elevated CO2 , respectively. Single leaf morphology of Gmelina, grown under ambient (inset I) and elevated CO2 (inset J) showing the variation in leaf size. (K and L) The changes in basal stem diameter in ambient and elevated CO2 -grown plants, respectively.
grown under elevated CO2 conditions and was ﬁnally ∼0.3 cm day−1 plant−1 on 120 DAP which was ∼46% high when compared to ambient CO2 -grown plants (Fig. 3D). Fig. 3E and F shows Gmelina trees grown in OTCs under ambient and elevated CO2 conditions, respectively after 120 DAP. The plants grown under ambient CO2 conditions showed a maximum height of ∼210 cm, whereas, plants grown under elevated CO2 showed a maximum height ∼360 cm after 120 DAP (Fig. 3A). More number of branches was also observed in elevated CO2 -grown plants when compared to ambient CO2 grown plants (Fig. 3A and B). Fig. 3G and H depicts Gmelina plants at 30 DAP in ambient and high CO2 chambers, respectively. On 30 DAP, plant morphology was almost similar between the two treatments and there was not much difference in plant height or number of branches. Single leaf morphology of Gmelina grown under ambient and elevated CO2 atmosphere was depicted in Fig. 3I and J, respectively. Signiﬁcant leaf size increment was observed under high CO2 compared to ambient CO2 -grown plants. Fig. 3K and L portray the basal stem morphology of ambient and elevated CO2 grown plants indicating that the basal diameter was signiﬁcantly (p < 0.001) high in elevated CO2 -grown plants compared to ambient CO2 -grown plants. 3.5. Destructive harvest and biomass determination Elevated CO2 had signiﬁcant effect on total biomass accumulation per tree and the biomass of individual plant organs (p < 0.001, Fig. 4). Fresh weights of leaf (Fig. 4A), stem (Fig. 4B) and root (Fig. 4C) were signiﬁcantly (p < 0.001) high in elevated CO2 -grown plants. After 90 DAP, plants under elevated CO2 showed a ∼40% increase in total fresh weight (Fig. 4A). The stem fresh weight was ∼23 kg during 120 DAP in elevated CO2 -grown plants, which was ∼42% more compared to ambient CO2 -grown plants (Fig. 4B). Plants grown under elevated CO2 atmosphere showed ∼40% more
fresh root weight after 120 days of treatment (Fig. 4C). The dry weights of individual organs also showed a similar pattern as of fresh weights. A signiﬁcant (p < 0.001) increase in dry weights were observed after 90 DAP (Fig. 4D, E and F). Interestingly, leaf dry weight was ∼45% high in elevated CO2 atmosphere after 120 days of treatment when compared with the corresponding ambient CO2 -grown plants (Fig. 4D). During initial 30 days of treatment, there was no signiﬁcant difference observed in the total stem dry weight in both ambient and elevated CO2 -grown plants (Fig. 4E). After 120 days of treatment, the elevated CO2 -grown plants showed a signiﬁcant (p < 0.001) increase in dry weights (∼40.6%) compared to ambient CO2 -grown plants. During the initial CO2 treatment (30 DAP), the root dry weight was ∼0.3 kg in both ambient and elevated CO2 grown plants showing statistically non-signiﬁcant difference but by 90 DAP, the increase in the root dry weights was signiﬁcantly (p < 0.001) high in elevated CO2 grown plants compared to ambient CO2 -grown counterparts (Fig. 4F). Total above ground fresh biomass (TAGFB) also showed same trend as of fresh and dry weights of individual organs. TAGFB started to increase after 90 days of treatment in both elevated and ambient CO2 grown plants (Fig. 4G). After 120 days of treatment TAGFB was signiﬁcantly high in elevated CO2 grown plants accounting for ∼32% high when compared to ambient CO2 -grown plants (Fig. 4G). Total above ground dry biomass (TAGDB) was ∼45% high in elevated CO2 -grown plants when compared with ambient CO2 -grown plants (Fig. 4H). Fig. 4I and J depicts the total fresh and dry biomass (TFB and TDB, respectively) in plants grown under ambient and elevated CO2 atmosphere. TFB was signiﬁcantly (p < 0.001) high in elevated CO2 -grown plants after 120 days of treatment when compared to ambient CO2 -grown plants (Fig. 4I). TDB was ∼13 kg in elevated CO2 -grown plants which was ∼53% high when compared to ambient CO2 -grown plants (Fig. 4J).
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Fig. 4. Analysis of various growth and characteristics of Gmelina grown under ambient and elevated CO2 concentrations. Leaf fresh weight (A), stem fresh weight (B), root fresh weight (C), leaf dry weight (D), stem dry weight (E), root dry weight (F), total above ground fresh biomass (TAGFB) (G), total above ground dry biomass (TAGDB) (H), total fresh biomass (TFB) (I) and total dry biomass (J). Values are the mean ± S.E.
3.6. AGR, above ground biomass and carbon sequestration potential The plants grown under elevated CO2 showed a signiﬁcant (p < 0.001) effect on AGR (Fig. 5A). After 90 days of treatment, AGR in elevated CO2 -grown plants was ∼150 g plant−1 day−1 , which was ∼65% higher when compared to ambient CO2 -grown plants. At 120 DAP, the AGR was ∼45% higher in elevated CO2 -grown plants (∼162 g plant−1 day−1 ) when compared to ambient CO2 grown plants (∼90 g plant−1 day−1 ). The absolute above ground biomass (AGB) was also high (p < 0.001) in elevated CO2 -grown plants compared to ambient CO2 -grown plants (Fig. 5B). After 120 days of treatment, ∼1200 g of biomass was accumulated in plants grown under elevated CO2 atmosphere which is ∼49% high compared to that of ambient counterparts (Fig. 5B). The efﬁciency of carbon sequestration was signiﬁcantly higher (p < 0.001) in elevated CO2 -grown plants when compared to ambient CO2 -grown plants (Fig. 5C) and ∼2 kg of CO2 was sequestered per tree after 120 days of CO2 treatment (Fig. 5C). After 90 days of treatment, the carbon sequestered in elevated CO2 -grown plants was ∼1500 g tree−1 which increased to a level of ∼2100 g tree−1 by 120 days of treatment. During this period the ambient CO2 -grown plants could sequester ∼1000 g tree−1 which was ∼48% less when compared to the elevated CO2 -grown plants (Fig. 5C). 3.7. Pn in relation to TDB, AGR, stem dry weight and TAGDB and relationships within the growth variables Regression analysis and relationships were established between Pn versus TDB, AGR, stem dry weight and TAGDB to understand
growth dynamics and productivity rates in relation to photosynthetic physiology in Gmelina grown under ambient and elevated CO2 -conditions (Fig. 6). Coefﬁcient correlation of relationship between Pn and TDB was 0.95 in elevated CO2 grown plants which was signiﬁcantly high compared to ambient CO2 grown plants (r = 0.76, p < 0.01) (Fig. 6A). A strong positive correlation (r = 0.92, p < 0.001) between Pn and AGR was also observed in elevated CO2 grown plants whereas, the ambient CO2 -grown plants showed a weak, however signiﬁcant positive correlation (r = 0.78) (Fig. 6B). The correlation between TDB and AGR was signiﬁcantly high in both ambient (r = 0.95, p < 0.001) and elevated CO2 (r = 0.91, p < 0.001)-grown plants (Fig. 6C). The relationship between the stem basal diameter and stem dry weight also showed a positive correlation in elevated CO2 grown plants (r = 0.97, p < 0.001) compared to ambient CO2 grown plants (r = 0.90, p < 0.01) (Fig. 6D). Plants grown under elevated CO2 atmosphere showed a signiﬁcant positive linear relationship between stem basal diameter and TAGDB (r = 0.94; p < 0.001) (Fig. 6E) whereas, the coefﬁcient correlation of relationship between stem basal diameter and TAGDB was ∼0.88 (p < 0.010) in ambient CO2 -grown plants (Fig. 6E). The relationship between TDB and stem dry weight showed a strong positive correlation in both ambient (r = 0.92; p < 0.001) and elevated (r = 0.95; p < 0.001) CO2 -grown plants (Fig. 6F).
4. Discussion The increasing CO2 concentration in the atmosphere and its consequences on climate change prompted a renewed interest in enhancing the size of carbon pools, especially in the tropics through
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Fig. 5. Absolute growth rates (AGR) (A), above ground biomass (B) and CO2 sequestration per tree (C) during different growth stages in Gmelina under ambient and elevated CO2 atmosphere. Values are mean ± S.E.
planting fast growing tree species. Our investigation over the last four years on carbon sequestration potential among tree species demonstrate that G. arborea is potential tree species for effective carbon sequestration as it showed a positive growth response to elevated CO2 throughout the experimentation. Gmelina plants were ∼42% taller with 52% thicker stems after 120 days of high CO2 treatment when compared to ambient CO2 . Interestingly, the relative growth rates were also signiﬁcantly high in elevated CO2 grown plants compared to ambient CO2 -grown plants. Such, transient growth stimulation by elevated CO2 has been reported in certain herbaceous species [27,28]. However, the physiological drive which stimulates such growth changes is poorly understood. In our study, the Pn of Gmelina were signiﬁcantly high during the growth seasons under elevated CO2 atmosphere. The Pn were maintained high in elevated CO2 -grown Gmelina even under the reduced gs and E during the two growing seasons. The increase in Pn of Gmelina grown under elevated CO2 with concurrent decrease in the E resulted in dramatic increases in leaf-level WUEi which were in consistent with two such observations [29,30]. The CO2 exchange between the plants and its atmosphere mainly occurs through the stomata and gs is one of the major limitations in carbon assimilation, particularly when plants are grown under elevated CO2 [29,31–33]. Stomatal conductance (gs ) is mainly dependent on the stomatal density and on stomatal aperture (adaptable according to environmental conditions). Studies on temperate tree species showed a substantially reduced stomatal density in
response to the increases in atmospheric CO2 . Atmospheric CO2 concentrations above present ambient CO2 concentrations also showed a signiﬁcant effect on the transpiration rates of trees which is likely to be through partial stomatal closure, a direct response of guard cells to increased intercellular CO2 concentration (ci ) . Until recently, most experiments on tree species had found at least some reduction in gs in elevated CO2 [36,37] although the responses were very variable . Along with stomatal density and stomatal aperture, increased leaf area ratio in elevated CO2 grown Gmelina might have been responsible for the reduction in gs . The signiﬁcantly high photosynthetic rates despite the decrease in gs is believed to be due to accelerated internal photosynthetic activity [16,39–43]. Enzymatic processes like modulation of rubisco activity and expression of certain other key photosynthetic enzymes probably play a important role in inﬂuencing the Pn in young tree species under high CO2 atmosphere [44–47]. Elevated atmospheric CO2 has been known to typically increase the rate of instantaneous photosynthesis in many C3 species by increasing CO2 concentration at the site of rubisco, resulting enhanced carboxylation efﬁciency and reducing photorespiration [9,33]. High CO2 -induced photosynthetic capacity was mainly due to differential expression of this key photosynethtic enzyme [48–53]. Evidently, the initial and total activities of RuBPcase in Gmelina strongly suggest that the increased photosynthetic rates observed in Gmelina grown under CO2 were due to efﬁcient RuBPcase activity. However, a number of plant species could not maintain the increased rates of photosynthesis under high CO2 as they tend to re-adjust their photosynthetic machinery to match the rates of resource availability . Incident light source and its processing through photochemical membranes are believed to signiﬁcantly affect photosynthesis, especially in plants grown under tropical climate. Elevated CO2 concentration, under natural high light irradiance, might either support a greater load of electron transport [8,55], or decrease photochemical efﬁciency, leading to an increased susceptibility of photoinhibition [56,57]. The chlorophyll a ﬂuorescence data in Gmelina grown under elevated CO2 indicated that the greater photosynthetic capacity was due to increased photochemical efﬁciency (FV /FM ) associated with effective electron transport rates under saturated light conditions (Fig. 2). Lightsaturated photosynthesis was greatly enhanced under elevated CO2 which might be due of signiﬁcant increase in electron transport rates and potent decrease in heat dissipation [8,58,59]. Changes in CO2 atmospheric concentration effected the processing of light energy through photochemical membrane, either by supporting a greater load of electron transport or by decreasing photochemical efﬁciency leading to an increased susceptibility of photoinhibition. The relationship between the carbon assimilation and PSII photochemistry is signiﬁcant to understand how the physical environment affects plant growth as well as to identify potent photochemically efﬁcient tree species for better carbon sequestration. Our data on Chlorophyll a ﬂuorescence conjoint with other physiology data demonstrate that future increase in atmospheric CO2 may have positive effects on photochemical efﬁciency in fast growing tropical tree species like, G. arborea. The ability of plant growth under elevated CO2 not only depends on increased photosynthetic capacity but also on the ability of plants to posses or to develop greater sinks [49,50]. In this study, growth in Gmelina was evidenced by signiﬁcant development of side shoots under high CO2 atmosphere, leading to better resource utilization when compared to those grown under ambient CO2 . Under elevated CO2 atmosphere, the increase in sink strength also suggests that the demand for carbohydrate was sufﬁcient to balance the increased carbohydrate supply associated with high photosynthetic rates [51,60–62]. Recent studies on effects of elevated CO2 on plants showed that increase in the carbon availability for the sink organs resulted in higher biomass yields
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
Fig. 6. Correlation analysis between total dry biomass (TDB) and photosynthetic rates (Pn ) (A), absolute growth rate (AGR) and Pn (B), AGR and TDB (C), stem dry weight and stem basal diameter (D), total above ground dry biomass and stem basal diameter (E), stem dry weight and TDB (F) in Gmelina grown under ambient and elevated CO2 conditions (, ambient; 䊉, elevated).
[63,64]. Coherently, the growth and productivity were enhanced in Gmelina grown under elevated CO2 indicating sustained increases in biomass yields. We attribute that the positive correlation between photosynthesis and the morphological growth characteristics of Gmelina under elevated CO2 were due to its potential positive relationship between source and sink capacity. Reduction in photosynthetic capacity under elevated CO2 was not pronounced in young Gmelina due to its fast and determinate juvenile growth pattern. In-turn, the high metabolic rates and efﬁcient sink capacity in Gmelina might lead to the sustained photosynthetic responses to elevated CO2 [32,65,66]. Elevated CO2 atmosphere persistently enhanced all the growth characteristics in Gmelina including plant height, number of branches, internodes, intermodal distance, aerial biomass and total plant biomass suggesting that Gmelina plants have signiﬁcantly greater sink capacity for carbon accumulation to match the efﬁcient carbon sequestration. Our data also demonstrate that Gmelina could store signiﬁcantly high amount of carbon into rapidly increasing biomass. Photosynthetic carbon gain is directly proportional to biomass yields, suggesting that the increased photosynthesis will result in more carbon or biomass in plants . Our data on the absolute growth rates and above ground biomass depicts increased sequestration of carbon into plant under elevated atmospheric CO2 . These results also suggest that Gmelina, selected for rapid growth can be better options for afforestation projects aimed to increase carbon uptake into wood. It is also conceivable that the greater biomass allocation into stem tissue of Gmelina grown under high CO2 atmosphere was due to the fact that stem is the primary sink in Gmelina which also reﬂects the normal storage strategy of this fast growing tree species. Our data strongly suggests that Gmelina trees could confront the photosynthetic down regulation by combining high capacity of source which could match the high sink demand. Our results are very signiﬁcant in understanding the responses of tropical deciduous trees to slightly elevated CO2 conditions. Our study elucidates that young Gmelina when grown even under a
100 mol increment in CO2 concentration than ambient for a complete production cycle (spring and summer seasons), can generate signiﬁcantly higher biomass by virtue of enhanced photochemical efﬁciency, high sink demand and better growth dynamics. Such ﬁndings are very important with respect to managing carbon sequestration which suggests that there are management options for creating short-rotation deciduous tree plantations to achieve increased sequestration of carbon in a future elevated CO2 environment. Acknowledgements This work was supported by a grant (BT/PR6402/BCE/08/ 416/2005) from the Department of Biotechnology, Government of India to Attipalli R Reddy. Facilities through FIST grant to the department from DST, New Delhi is also gratefully acknowledged. GKR and AG acknowledge Senior Research Fellowships (SRF) from CSIR, New Delhi. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.plantsci.2011.07.005. References  Intergovernmental Panel on Climate Change (IPCC), Climate change mitigation, in: B. Metz, O.R. Davidson, P.R. Bosch, R. Dave, L.A. Meyer (Eds.), Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom/New York, USA, 2007.  Intergovernmental Panel on Climate Change (IPCC), in: R. Watson, I.R. Noble, B. Bolin, N.H. Ravindranath, D.J. Verardo, D.J. Dokken (Eds.), Land use, Land-use Change, and Forestry: A Special Report, Cambridge University Press, Cambridge, UK, 2000.  Intergovernmental Panel on Climate Change (IPCC), Climate change 2001, impacts, adaptation, and vulnerability, in: J.J. McCarthy, O.F. Canziani, N.A.
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
   
    
  
Leary, D.J. Dokken (Eds.), White. Contribution of Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom/New York, NY, USA, 2001. R. Lemus, R. Lal, Bioenergy crops and carbon sequestration, Crit. Rev. Plant. Sci. 24 (2005) 1–21. S. Brown, Measuring carbon in forests: current status and future challenges, Environ. Pollut. 116 (2002) 363–372. J.K. Winjum, R.K. Dixon, P.E. Schroeder, Forest management and carbon storage: a look at 12 key forest nations, Water Air Soil Pollut. 70 (1993) 239–257. C.A. Gunderson, J.D. Sholtis, S.D. Wullschleger, D.T. Tissue, P.J. Hanson, R.J. Norby, Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciﬂua L.) plantation during 3 years of CO2 enrichment, Plant Cell Environ. 25 (2002) 379–393. S.P. Long, E.A. Ainsworth, A. Rogers, D.R. Ort, Rising atmospheric carbon dioxide: plants face the future, Annu. Rev. Plant Biol. 55 (2004) 591–628. O. Urban, Physiological impacts of elevated CO2 concentration ranging from molecular to whole plant responses, Photosynthetica 41 (2003) 9–20. C. Streck, S.M. Scholz, The role of forests in global climate change: whence we come and where we go, Int. Aff. 82 (2006) 861–879. F.J. Dyson, Can we control the carbon dioxide in the atmosphere? Energy 2 (1977) 287–291. R.J. Norby, E.H. DeLuciac, B. Gielend, C. Calfapietrae, C.P. Giardinaf, J.S. King, J. Ledforda, H.R. McCarthy, D.J.P. Moorei, R. Ceulemans, P.D. Angelis, A.C. Finzi, D.F. Karnosky, M.E. Kubiske, M. Lukac, K.S. Pregitzerk, G.E. Scarascia-Mugnozzan, W.H. Schlesingerb, R. Oren, Forest response to elevated CO2 is conserved across a broad range of productivity, Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 18052–18056. A.M. Rae, P.J. Tricker, S.M. Bunn, G. Taylor, Adaptation of tree growth to elevated CO2 : quantitative trait loci for biomass in Populus, New Phytol. 175 (2007) 59–69. D. Eamus, R. Ceulemans, Effects of greenhouse gases on the gas exchange of forest trees, in: D.F. Karnosky, R. Ceulemans, J.L. Scarascia-Mugnozza, J.L. Innes (Eds.), The Impact of Carbon Dioxide and other Greenhouse Gases on Forest Ecosystems, Wallingford, CABI Press, 2001, pp. 17–56. J.D. Herrick, R.B. Thomas, No photosynthetic down-regulation in sweet gum trees (Liquidambar styraciﬂua L.) after three years of CO2 enrichment at Duke Forest FACE experiment, Plant Cell Environ. 24 (2001) 53–64. A. Noormets, E.P. McDonald, E.L. Kruger, J.G. Isebrands, R.E. Dickson, D.F. Karnosky, The effect of elevated carbon dioxide and ozone on leaf- and branchlevel photosynthesis and potential plant level carbon gain in aspen, Trees Struct. Funct. 15 (2001) 262–270. R.J. Norby, S.D. Wullschleger, C.A. Gunderson, D.W. Johnson, R. Ceulemans, Tree responses to rising CO2 in ﬁeld experiments: implications for the future forest, Plant Cell Environ. 22 (1999) 683–714. R.J. Norby, D.E. Todd, J. Fults, D.W. Johnson, Allometric determination of tree growth in a CO2 -enriched sweetgum stand, New Phytol. 150 (2001) 477–487. L. Cheng, L.H. Fuchigami, Rubisco activation state decreases with increasing nitrogen content in apple leaves, J. Exp. Bot. 51 (2000) 1687–1694. B.J. Strasser, R.J. Strasser, Measuring fast ﬂuorescence transients to address environment questions: the JIP-test, in: P. Mathis (Ed.), Photosynthesis: from Light to Biosphere, Kluwer Academic, Dordrecht-Boston/London, 1995. K.R. Albert, T.N. Mikkelsen, H. Ro-Poulsen, Effects of ambient versus reduced UV-B radiation on high arctic Salix arctica assessed by measurements and calculations of chlorophyll-a-ﬂuorescence parameters from ﬂuorescence transients, Physiol. Plant. 124 (2005) 208–226. R.J. Strasser, Govindjee, The Fo and O-J-I-P ﬂuorescence rise in higher plants and algae, in: J.H. Argyroudi-Akoyunoglou (Ed.), Regulation of Chloroplast Biogenesis, Plenum Press, New York, 1992. P.J. Radford, Growth analysis formulae—their use and abuse, Crop Sci. 7 (1967) 171–175. P.J. Newbould, Methods for Estimating the Primary Production of Forests, IBP Handbook No. 2, International Biological Programme, Oxford, 1967. S.S. Rajput, N.K. Shukla, V.K. Gupta, J.D. Jain, Timber Mechanics: Strength Classiﬁcation and Grading of Timber, ICFRE-Publication-38, New Forest, Dehradun, 1996. J.D.S. Negi, R.K. Manhas, P.S. Chauhan, Carbon allocation in different components of some tree species of India: a new approach for carbon estimation, Curr. Sci. 85 (2003) 101–104. M. Centritto, H. Lee, P. Jarvis, Interactive effects of elevated [CO2 ] and water stress on cherry (Prunus avium) seedlings. I. Growth, total plant water use efﬁciency and uptake, New Phytol. 141 (1999) 129–140. S.R. Zhang, Q.L. Dang, X.G. Yu, Nutrient and [CO2 ] elevation had synergistic effects on biomass production but not on biomass allocation of white birch seedlings, Forest Ecol. Manage. 234 (2006) 238–244. L.J. Anderson, H. Maherali, H.B. Johnson, H.W. Polley, R.B. Jackson, Gas exchange and photosynthetic acclimation over sub ambient to elevated CO2 in C3 –C4 grassland, Global Change Biol. 7 (2001) 693–707. M. Possell, C.N. Hewitt, Gas exchange and photosynthetic performance of the topical tree Acacia nigrescens when grown in different CO2 concentrations, Planta 229 (2009) 837–846. R.G. Jensen, Activation of Rubisco regulates photosynthesis at high temperature and CO2 , Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 12937–12938. P.A. Beedlow, D.T. Tingey, D.L. Phillips, W.E. Hogsett, D.M. Olszyk, Rising atmospheric CO2 and carbon sequestration in forests, Front. Ecol. Environ. 2 (2004) 315–322.
 E.A. Ainsworth, A. Rogers, The response of photosynthesis and stomatal conductance to rising [CO2 ]: molecular mechanisms and environmental interactions, Plant Cell Environ. 30 (2007) 258–270.  F.I. Woodward, Stomatal numbers are sensitive to increases in CO2 from preindustrial levels, Nature 327 (1987) 617–618.  E. Paoletti, N.E. Grulke, Does living in elevated CO2 ameliorate tree response to ozone? A review on stomatal responses, Environ. Pollut. 137 (2005) 483–493.  D. Eamus, P.G. Jarvis, The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests, Adv. Ecol. Res. 19 (1989) 1–55.  C.B. Field, R.B. Jackson, H.A. Mooney, Stomatal responses to increased CO2 implications from the plant to the global scale, Plant Cell Environ. 18 (1995) 1214–1225.  P.S. Curtis, A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide, Plant Cell Environ. 19 (1996) 127–137.  G.D. Farquhar, T.D. Sharkey, Stomatal conductance and photosynthesis, Annu. Rev. Plant Biol. 33 (1982) 317–345.  A. Rey, P.G. Jarvis, Long-term photosynthetic acclimation to increased atmospheric CO2 concentration in young birch (Betula pendula) trees, Tree Physiol. 18 (1998) 441–450.  S.M. Assmann, The cellular basis of guard cell sensing of rising CO2 , Plant Cell Environ. 22 (1999) 629–637.  R.F. Sage, How terrestrial organisms sense signal and respond to carbondioxide, Integr. Comp. Biol. 42 (2002) 469–480.  J.D. Herrick, H. Maherali, R.B. Thomas, Reduced stomatal conductance in sweetgum (Liquidambar styraciﬂua) sustained over long-term CO2 enrichment, New Phytol. 162 (2004) 387–396.  C.R. Warren, M.A. Adams, Evergreen trees do not maximize instantaneous photosynthesis, Trends Plant Sci. 9 (2004) 270–274.  J.R. Coleman, Carbonic anhydrase and its role in photosyhthesis, in: R.C. Leegood, T.D. Sharkey, S. von Caemmerer (Eds.), Photosynthesis: Physiology and Metabolism, The Kluwer Academic, Netherlands, 2000.  S. von Caemmerer, W.P. Quick, Rubisco: physiology in vivo, in: R.C. Leegood, T.D. Sharkey, S. von Caemmerer (Eds.), Photosynthesis: Physiology and Metabolism, The Kluwer Academic, Netherlands, 2000.  S.M. Messinger, T.N. Buckley, K.A. Mott, Evidence for the involvement of photosynthetic process in the stomatal responses to CO2 , Plant Physiol. 140 (2006) 771–778.  T.D. Sharkey, Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations, Bot. Rev. 51 (1985) 53–105.  I. Aranjuelo, P. Pérez, L. Hernández, J.J. Irigoyen, G. Zita, R. Martínez-Carrasco, et al., The response of nodulated alfalfa to water supply, temperature and elevated CO2 : photosynthetic down-regulation, Physiol. Plant. 123 (2005) 348–358.  B.D. Moore, S.H. Cheng, D. Sims, J.R. Seemann, The biochemical and molecular basis for photosynthetic acclimation to elevated CO2 , Plant Cell Environ. 22 (1999) 567–582.  P.B. Reich, S.E. Hobbie, T. Lee, D.S. Ellsworth, J.B. West, D. Tilman, J.M.H. Knops, S. Naeem, J. Trost, Nitrogen limitation constrains sustainability of ecosystem response to CO2 , Nature 440 (2006) 922–925.  A. Rogers, Y. Gibon, M. Stitt, P.B. Morgan, C.J. Bernacchi, D.R. Ort, S.P. Long, Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume, Plant Cell Environ. 29 (2006) 1651–1658.  M. Stitt, A. Krapp, The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients, Plant Cell Environ. 22 (1999) 583–622.  R.F. Sage, Acclimation of photosynthesis to increasing atmospheric CO2 ; the gas exchange perspective, Photosynth. Res. 39 (1994) 351–368.  S.P. Long, Modiﬁcation of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ. 14 (1991) 729–739.  I. Aranjuelo, G. Erice, S. Norgues, F. Morales, J.J. Irigoyen, M. Sanchez-Diaz, The mechanism(s) involved in the photoprotection of PSII at elevated CO2 in nodulated alfalfa plants, Environ. Exp. Bot. 64 (2008) 295–306.  J.S. Roden, M.C. Ball, The effect of elevated [CO2 ] on growth and photosynthesis of two eucalyptus species exposed to high temperatures and water deﬁcits, Plant Physiol. 111 (1996) 909–919.  C.J. Bernacchi, C. Pimentel, S.P. Long, In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis, Plant Cell Environ. 26 (2003) 1419–1430.  A. Rogers, S.W. Humphries, A mechanistic evaluation of photosynthetic acclimation at elevated CO2 , Global Change Biol. 6 (2000) 1005–1011.  D.J. Nowak, D.E. Crane, Carbon storage and sequestration by urban trees in the USA, Environ. Pollut. 116 (2002) 381–389.  B.Kr. Jana, S. Biswas, M.P. Majumder, Kr. Roy, A. Mazumdar, Carbon sequestration rate and aboveground biomass carbon potential of four young species, J. Ecol. Nat. Environ. 2 (2009) 015–024.  B. Strain, R. Thomas, Anticipated effects of elevated CO2 and climate change on plants from Mediterranean-type ecosystems utilizing results of studies in other ecosystems, in: J. Moreno, W. Oechel (Eds.), Global Change and Mediterranean-Type Ecosystems, Spinger-Verlag, Berlin, 1995, pp. 121–139.  P. Hogy, A. Fangmeier, Atmospheric CO2 enrichment affects potatoes: 1. Aboveground biomass production and tuber yield, Eur. J. Agron. 30 (2009) 78–84.
G.K. Rasineni et al. / Plant Science 181 (2011) 428–438
 R.L. Lindroth, K.K. Kinney, C.L. Platz, Responses of deciduous trees to elevated atmospheric CO2 : productivity, phytochemistry and insect performance, Ecology 74 (1993) 763–777.  J.G. Isebrands, E.P. McDonald, E. Kruger, G. Hendrey, K. Pregitzer, K. Percy, et al., Growth responses of Populus tremuloides clones to interacting carbon dioxide and tropospheric ozone, Environ. Pollut. 115 (2001) 359–371.
 C. Korner, Plant CO2 responses: an issue of deﬁnition, time and resource supply, New Phytol. 172 (2006) 393–411.  V.E. Wittig, C.J. Bernacchi, X.G. Zhu, C. Calfapietra, R. Ceulemans, P. Deangelis, B. Gielen, F. Miglietta, P.B. Morgan, S.P. Long, Gross primary production is stimulated for three Populus species grown under free-air CO2 enrichment from planting through canopy closure, Global Change Biol. 11 (2005) 644–656.