Responses of Angelica acutiloba Kitagawa Transplants to Elevated Ambient CO2 Concentration

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  • 1 College of Water Resources and Civil Engineering, China Agricultural University, Beijing 100083, China; and Key Laboratory of Agricultural Engineering in Structure and Environment, Ministry of Agriculture and Rural Affairs, Beijing 100083, China

Long-term exposure to an elevated ambient carbon dioxide (eCO2) concentration could weaken or diminish the enhancement of plant photosynthesis and growth. To monitor this response and offer references for growth management, the whole-plant photosynthetic rate (Pn,w) and dark respiration rate (Rd,w) of Angelica acutiloba Kitagawa transplants were monitored with a growth chamber. The results showed that eCO2 increased both the Pn,w and Rd,w by (79 ± 42) % and (126 ± 51) %. The dry weight of transplants under eCO2 was 33.6% greater than that under aCO2. However, the photosynthetic acclimation to eCO2 occurred. The increase in the Pn,w was maintained until the end of the experiment due to increased leaf area. Moreover, the increase in plant dry weight mainly occurred in the first 15 days of treatment. Furthermore, the dry weight estimated based on the Pn,w and Rd,w agreed well with the measured dry weight. The relative growth rate (RGR) calculated with the estimated dry weight demonstrated the response of transplant growth to eCO2. These results indicated that the proposed method can be used to monitor the response of plant growth to eCO2.

Abstract

Long-term exposure to an elevated ambient carbon dioxide (eCO2) concentration could weaken or diminish the enhancement of plant photosynthesis and growth. To monitor this response and offer references for growth management, the whole-plant photosynthetic rate (Pn,w) and dark respiration rate (Rd,w) of Angelica acutiloba Kitagawa transplants were monitored with a growth chamber. The results showed that eCO2 increased both the Pn,w and Rd,w by (79 ± 42) % and (126 ± 51) %. The dry weight of transplants under eCO2 was 33.6% greater than that under aCO2. However, the photosynthetic acclimation to eCO2 occurred. The increase in the Pn,w was maintained until the end of the experiment due to increased leaf area. Moreover, the increase in plant dry weight mainly occurred in the first 15 days of treatment. Furthermore, the dry weight estimated based on the Pn,w and Rd,w agreed well with the measured dry weight. The relative growth rate (RGR) calculated with the estimated dry weight demonstrated the response of transplant growth to eCO2. These results indicated that the proposed method can be used to monitor the response of plant growth to eCO2.

CO2 is the substrate for plant photosynthesis. An eCO2 concentration can stimulate the photosynthetic rate by increasing the substrate availability of Rubisco carboxylation and inhibiting the competitive oxygenation of the enzyme (Long et al., 2004; Stitt and Krapp, 1999). As a result, plants exposed to eCO2 usually show accelerated growth rates and high yields (e.g., Amthor 1995; Bowes, 1993; Drake et al., 1997; Poorter, 1993; Prior et al., 2003). Considering that plants grown in horticultural facilities usually are exposed to low indoor CO2 concentrations, eCO2 is an important technology in horticultural production (e.g., Sanchez-Guerrero et al., 2005).

The stimulation of photosynthesis by eCO2 only increases the carbon availability of plants, and the extent to which stimulated photosynthesis can be translated into stimulated growth depends on the capability of a plant to use increased carbon under eCO2 (Kirschbaum, 2011). Usually, plants with a large sink size or optimized nutrient supply can take advantage of eCO2 and show stimulated photosynthetic rates and increased biomass accumulation (Dong et al., 2017; Qian et al., 2012). However, plants with a small sink size or poor nutrient supply cannot make full use of the carbon synthesized under eCO2 and show a small increase in biomass accumulation (Drake et al., 1997; Stitt and Krapp, 1999; Woodward. 2002). Bruggink (1984) found that a 40% to 50% increase in photosynthesis under eCO2 of 1000 µmol·mol−1 increased the RGR by only less than 15%. Yelle et al. (1990) reported that eCO2 of 900 µmol·mol−1 increased the RGR and yield of tomato plants only during the first 2 weeks of treatment. Moreover, excess synthesized carbon can remain in leaves and lead to the down-regulation of photosynthesis. Thus, it is necessary to monitor the growth of plants, especially dry weight production, under eCO2. Then, measures of optimizing the environment or fertilization strategies can be implemented to further improve the benefits of eCO2.

The plant dry mass can be estimated nondestructively based on the linear regression equations by inputting the easily measured parameters, such as leaf width, length, or SPAD value, etc. (Cho et al., 2007; Van Henten and Bontsema, 1995). The development of information technology further facilitates the access of those parameters and made the estimation of plant dry mass more convenient. However, the linear equation had to be validated if the growth conditions were changed (Catchpole and Wheeler, 1992; López-Díaz et al., 2011). In addition, plant dry weight production can be estimated nondestructively by measuring the CO2 flux from a canopy with an altered growth chamber (Bugbee, 1992; Teitel et al., 2008). Compared with the measurement of gas exchange at the leaf scale, this method can offer a continuous, long-term measurement of CO2 flux at the canopy level (Li et al., 2012a). Most importantly, the canopy net photosynthetic rate measured with this method can be more accurate than that calculated by scaling up the leaf photosynthetic rate (Ferraz et al., 2016). This method has been applied to measure the Pn,w of cucumber transplants (Mun et al., 2011), lettuce (Wheeler et al., 1994a), and tomato seedlings (Li et al., 2012b). Dry weight production also has been estimated based on the CO2 flux from the canopy measured with such methods (Burkart et al., 2007; Li et al., 2012b; Wheeler et al., 1994b).

Angelica acutiloba Kitagawa (hereafter referred to as “Angelica”) is an important herb of which roots can be processed into a kind of traditional Chinese medicine (Lu et al., 2004). However, the growth rate of Angelica plants is extremely slow, and it takes 1 year to produce transplants, which limits the yield. The development of high-efficiency cultivation methods to accelerate Angelica growth and meet the growing market is needed urgently. In this study, adjusted growth chamber methods were used to estimate the Pn,w and Rd,w. The purpose of this study was to examine the effects of eCO2 on Angelica transplant growth. The RGR estimated with Pn,w and Rd,w was estimated to check the feasibility of monitoring the Angelica transplant growth under eCO2. This work would be helpful for improving the response of plant growth to eCO2.

Materials and Methods

Plant material.

Seeds of Angelica acutiloba Kitagawa were sown in 120-well plastic trays filled with rockwool. The trays were placed in a germinating chamber with a 25 °C temperature and 80% relative humidity to accelerate germination. After 3 d of germination, the trays were moved to a growth chamber with a photoperiod of 16 h [400 μmol·m−2·s−1 of photosynthetic photon flux density (PPFD) provided by “cool white” fluorescent lamps on the top surface of tray]. The day/night regimes of temperature and relative humidity were 25/19 °C and 70%/80%, respectively. The seedlings were irrigated daily with a nutrient solution for which the electrical conductivity was maintained at 2.0 dS·m−1. High-purity CO2 was supplied with a compressed gas cylinder to maintain the CO2 concentration inside the growth chamber during the photoperiod at 1000 μmol·mol−1.

Treatments.

After 14 d of germination, Angelica seedlings with two expanded leaves were transplanted into a 50-well tray filled with rockwool to avoid emitting CO2 from microorganisms into the growth chamber. Then, the transplants were transferred to two controlled-environment growth chambers (Sanyo Gallenkamp Fitotron, Leicester, UK). The growth chamber was 0.38 m in depth, 0.6 m in length, and 0.55 m in height with a volume of 125 L. The air current speed inside the growth chamber was 0.3 m·s−1. The distance from lamps to the top surface of the tray was 0.5 m. PPFD on the top surface of the tray was 400 μmol·m−2·s−1. The CO2 concentration inside the growth chambers during the photoperiod was maintained at ambient or elevated CO2 concentration (1500 μmol·mol−1) by supplying high-purity CO2 with a compressed gas cylinder. CO2 was not supplied during the dark period. The nutrient solution (Otsuka solution, 1/2 strength) was supplied through subirrigation every day.

Gas exchange measurement and calculations.

During the experiment, the Pn,w (µmol CO2·h−1/transplant) and Rd,w (µmol CO2·h−1/transplant) were estimated by using the following equations.

Pn,w=Np·k·V·(CoutCin)+Sn
Rd,w=Nd·k·V·(CoutCin)n
where Np and Nd are the numbers of air exchanges of the growth chamber during the photoperiod and dark period, respectively (h−1); k is the coefficient for converting the CO2 volume into moles (µmol·m−3) calculated following Campbell and Norman (1998); V is the air volume of the growth chamber (0.125·m3); Cout and Cin are the CO2 concentrations outside and inside the growth chamber, respectively (µmol·mol−1); S is the CO2 supply rate (µmol·h−1); and n is the number of transplants in the growth chamber.

In this experiment, the constant Np and Nd were employed and may cause errors in Pn,w and Rd,w. Then, the percent errors in Np (eNp, %), Nd (eNd, %), Pn,w (eP, %), and Rd,w (eP, %) were calculated as follows:

eNp=NpNpNp·100%
eNd=NdNdNd·100%
eP=Pn,wPn,wPn,w·100%
eR=Rd,wRd,wRd,w·100%
where Np and Nd′ are the real number of air exchanges per hour (h−1) during photoperiod and dark period, respectively, and Pn,w′ and Rd,w′ are the real net photosynthetic rate and dark respiration rate of whole-plant (µmol·h−1/transplant).

Substituting Eqs. [3] and [5] into Eq. [1], eP can be calculated as:

eP=NP·K·V·(CoutCin)Pn,w·eN

Substituting Eqs. [4] and [6] into Eq. [2], eR can be calculated as:

eR=-Nd·K·V·(CoutCin)Rd,w·eN

The dry weight accumulation of the transplants in ‘u’ days (WE,u, g/transplant) was estimated as follows:

WE,u=W0+m·j·i=0u(Lp·Pn,w,iLd·Rd,w,i)
where W0 is the initial dry weight of the transplants (g/transplant), m is the coefficient for converting moles of CO2 into mass (44 × 10−6 g·µmol−1), j is the coefficient for converting the CO2 assimilated by transplants into dry weight (0.68 g·g−1; Van Henten, 1994), Lp and Ld are the lengths of the light period and dark period, respectively (h·d−1), and Pn,w,i and Rd,w,i are the average estimated Pn,w and Rd,w on day ‘i,’ respectively.

The RGR of transplants on day ‘u’ (RGRu, g·g−1) was estimated as follows:

RGRE,u=ln(WE,u)-ln(WE,u1)

Measurements.

CO2 concentrations inside and outside the growth chamber were measured using an infrared gas analyzer (GMP 222; Vaisala Oyj, Helsinki, Finland; precision: ± 15 µmol·mol−1). The sensors inside the growth chamber were located at the center of the interior space at the same height as that of the sensors located outside. Hourly averaged data were recorded and used to estimate Pn,w and Rd,w. The CO2 concentrations were measured every 10 min and averaged per hour automatically. The CO2 injection rate was adjusted manually by adjusting the knob of the air pump in the first 2 h of photoperiod to maintain the target CO2 concentration inside the growth chamber. After then, the CO2 was injected into the growth chamber at a constant rate and the accumulated amount of injected CO2 was recorded with a flow meter (TC-1000-200; Tokyo Keiso Corp., Japan). The CO2 injection rate was calculated as the ratio of the accumulated CO2 amount injected into growth chamber with time. The data collected during the first 2 h after both the dark–light transition and the light–dark transition were discarded to ensure that the environmental conditions were stable.

Both NP and Nd were measured in the absence of plants and calculated following Li et al. (2012b). Every 5 d, five transplants were sampled from each treatment to measure the leaf area and dry weight. The leaves of the sampled transplants were scanned with digital cameras, and the area was measured with image analysis software (LIA for Win32, freely available from http://www.agr.nagoya-u.ac.jp/%7Eshinkan/LIA32/index). Then, the whole plants were dried at 60 °C for 1 week to determine the dry weight with an electronic balance (PL303, precision: ±0.001 g; Mettler–Toledo, Greifensee, Switzerland). The significant difference in dry weight data were analyzed using analysis of variance at P < 0.05 with Student’s t test in SPSS 22.0 (IBM Corp., Armonk, NY).

At the end of the experiment, three transplants from each treatment were selected to measure the CO2 assimilation rate of their third leaf (counting from the bottom) using a portable photosynthesis system (LI-6400; LI-COR, Inc., Lincoln, NE). At the inlet of the leaf chamber, the CO2 concentration was set at 200, 250, 300, 400, 600, 800, 1000, or 1200 µmol·mol−1. The PPFD and air temperature were maintained at 400 µmol·m−2·s−1 and 25 °C, respectively. The measurements were repeated three times.

Results

The CO2 injection rate and CO2 concentrations inside and outside growth chamber are shown in Fig. 1. The CO2 concentrations inside growth chambers with eCO2 and aCO2 during photoperiod were maintained at 1523 ± 23 µmol·mol−1 and 313 ± 23 µmol·mol−1 throughout the experiment, respectively. The number of transplants inside the growth chamber is shown in Fig. 2. For one growth chamber, the number of air exchanges during photoperiod (Np) and dark period (Nd) were 5.73 h−1 and 2.31 h−1, respectively. Np and Nd of another growth chamber were 1.52 h−1 and 0.89 h−1, respectively. In contrast, PPFD on the top of transplants increased with the increase in transplant height. However, the difference in PPFD between the transplants under eCO2 and aCO2 was less than 10 µmol·m−2·s−1. Hence, the effects of this difference on transplant growth can be neglected.

Fig. 1.
Fig. 1.

CO2 injection rate and CO2 concentrations inside and outside the growth chamber during the photoperiod (A) and dark period (B). Data represent the mean ± sd. CO2 = carbon dioxide.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

Fig. 2.
Fig. 2.

Number of Angelica transplants inside the growth chamber.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

To test the accuracy of the method used to measure the Pn,w and Rd,w, the estimated transplant dry weight (WE) was plotted against the measured dry weight (WM) (Fig. 3). The linear equation of WE and WM for transplants under eCO2 was WM = 0.92·WE with an r2 value of 0.96 (P > 0.05), whereas it was WM = 0.95·WE with an r2 value of 0.91 for transplants under aCO2 (P > 0.05). The largest differences between WM and WE were less than 12%. Thus, the measured Pn,w and Rd,w were accurate and could be employed to monitor the response of transplant dry weight to eCO2.

Fig. 3.
Fig. 3.

Dry weight accumulation of Angelica transplants estimated based on the whole-plant net photosynthetic rate and dark respiration rate (WE) plotted against the measured dry weight (WM). Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

During the experiments, the Pn,w and Rn,w of transplants grown under either eCO2 or aCO2 increased with time (Figs. 4 and 5). The ratios of Rn,w to Pn,w of the transplants under eCO2 and aCO2 were (74 ± 12) % and (60 ± 16) % during the experiment. Finally, the CO2 released by transplants under eCO2 and aCO2 during dark period were (37 ± 6) % and (30 ± 8) % of those fixed during photoperiod, respectively. In contrast, both Pn,w and Rn,w were greater under eCO2 than under aCO2. During the experiment, the increases in both Pn,w and Rn,w were (13.9 ± 3.9) µmol CO2·h−1/transplant and (13.8 ± 4.2) µmol CO2·h−1/transplant, respectively. However, these increases already had occurred at the beginning of treatment and lasted until the end of the experiment. As a result, the increased ratios of the Pn,w and Rn,w decreased with time. The Pn,w and Rn,w were (79 ± 42) % and (126 ± 51) % greater under eCO2 than that under aCO2.

Fig. 4.
Fig. 4.

Whole-plant net photosynthetic rate of Angelica transplants (Pn,w) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

Fig. 5.
Fig. 5.

Whole-plant dark respiration rate of Angelica transplants (Rd,w) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

At the end of the experiment, the responses of the leaf net photosynthetic rate (Pl) to different CO2 concentrations were measured and are shown in Fig. 6. After 25 d of treatment, Pl of transplants grown under eCO2 was lower than that of transplants grown under aCO2; when the third leaf of transplants was exposed to the same CO2 concentration, it ranged from 50 to 1200 µmol·mol−1. Both the CO2 compensation and saturation points of the transplants under eCO2 decreased. This result suggests that the photosynthesis of transplants under eCO2 acclimated to the eCO2 by the end of the experiments (Hao et al., 2006). In addition, Pl in each day was calculated as the ratio of Pn,w to leaf area and is shown in Fig. 7. The results showed that the initial enhancement of Pl under eCO2 weakened with exposure time and diminished in the last few days of the experiment. Together with the phenomenon of photosynthetic acclimation observed in the transplants under eCO2, this result suggested that the photosynthetic capacity of transplant leaves under eCO2 decreased.

Fig. 6.
Fig. 6.

Response of net photosynthetic rate of Angelica transplants (Pl) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations to different CO2 concentrations at the end of experiment. Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

Fig. 7.
Fig. 7.

Estimated net photosynthetic rate of Angelica transplants per leaf area (Pl) under Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

The leaf area of the transplants under eCO2 and aCO2 increased exponentially with time (Fig. 8). eCO2 stimulated the extension of transplant leaves. In the first 15 d of treatment, the differences in leaf area between the transplants under eCO2 and those under aCO2 increased with treatment time and reached 0.0012 m2/transplant after 15 d of treatment. However, the differences were not further enlarged with the treatment time and became 0.0015 m2/transplant. Thus, the stimulation of leaf area by eCO2 mainly occurred during the first 15 d of treatment.

Fig. 8.
Fig. 8.

Leaf area of Angelica transplants grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations. Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

The dry weights of transplants under eCO2 (Wm,e) and aCO2 (Wm,a) increased with time. Wm,e was always greater than WaC through the experiment. At the end of the experiment, Wm,e was 33.6% greater than Wm,a (Fig. 9). Nevertheless, (Wm,eWm,a) after 15 d of treatment was 81% of that at the end of the experiment. Thus, the enhancement of eCO2 on dry weights was mainly formed in the first 15 d of treatment.

Fig. 9.
Fig. 9.

Dry weight accumulation of Angelica transplants grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2). (* and NS indicate significant differences at P < 0.05 and nonsignificant differences, respectively.) Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

Based on WE, the RGR was calculated (Fig. 10). The initial increase in RGR decreased with exposure time and almost diminished in the last dozen days of the experiment. Thus, both the initial increases in leaf area and dry weight accumulation mainly occurred in the first 15 d of treatment. These results coincide with those of Yelle (1990). Hence, the change in plant responses to eCO2 can be detected with these methods.

Fig. 10.
Fig. 10.

Relative growth rate (RGR) of Angelica transplants calculated based on the estimated dry weight of the transplants grown. Data represent the mean ± sd.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13726-18

Discussion

The growth chamber method has been widely applied to measure the Pn,w and Rd,w. To prevent the inaccuracy of measured Pn,w and Rd,w, all of the concentration sensors were calibrated with standard gases in advance. The pure CO2 was injected into the chamber at a constant rate, which was calculated with the accumulated amount of CO2 injected into the chamber during photoperiod. This method had been calibrated by draining water from a measuring cylinder with pure nitrogen. Thus, the error caused by the CO2 injection speed can be neglected. Then, the over- or underestimated Pn,w and Rd,w may be aroused by the number of air exchanges according to Eqs. [1] and [2].

The percent errors in Pn,w (eP) and Rd,w (eR) caused by the percent errors in number of air exchanges during photoperiod and dark period can be evaluated with Eqs. [7] and [8]. eP and eR are in proportion to eNp and eNd, respectively. It is possible to prevent and cause over- or underestimated Pn,w and Rd,w by diminishing the variation of Np and Nd, which may change with the room temperature (Li et al., 2012b). In this experiment, the air conditioner had been operated continuously to maintain the room temperature, even though the room temperature changed sometimes due to the operation of other equipment or human activates and enlarged eP and eR. However, the good agreement of WE and WM indicates that the measured Pn,w and Rd,w were highly accurate. They can be applied for further analysis.

Photosynthesis is well known to increase under eCO2. However, this enhancement is not sustainable after long-term exposure to eCO2, a phenomenon that frequently is referred to as photosynthetic acclimation or down-regulation (e.g., Ainsworth and Rogers, 2007). The angelica transplants under eCO2 also showed this phenomenon. This phenomenon normally occurs in response to excess nonconstructive carbohydrates due to limited sink size or poor nutrient supply. In contrast, plants with a large sink size or sufficient nutrient supply can avoid this phenomenon and maintain a high photosynthetic capacity (Dong et al., 2017; Qian et al., 2012).

There are fewer reports on the response of Pn,w to eCO2. According to the results presented here, the variation in Pn,w differs from that in Pl. The initial increase in Pn,w due to eCO2 was maintained until the end of the experiment because the leaf area of the transplants increased in response to eCO2 and thus offset the impacts of Pl on Pn,w. However, the transplants in the experiment were young, with a leaf area index ranging from 1.3 to 3.4. A further increase in leaf area would intensify shading and no longer increase the canopy photosynthetic rate. Then, the positive effect of eCO2 on the canopy photosynthetic rate may be further weakened.

Leaf area plays an important role in plant growth and the photosynthetic rate. Wheeler et al. (2015) observed that the onion under eCO2 of 532 µmol·mol−1 showed a greater leaf area than those grown under aCO2 of 374 µmol·mol−1. The results of this experiment coincide with those results. However, some reports have observed negative or neutral effects of eCO2 on leaf area, which result from differences in growth conditions and plant species (Rachel and Gail, 2010; Usuda, 2004).

Dark respiration is a major determinant of plant dry weight accumulation, as it can return as much as 24%≈50% of photosynthetically fixed carbon to the atmosphere (Amthor, 1995; Yokoi et al., 2005). However, the effects of eCO2 on the Rd,w vary according to plant species and growth conditions. eCO2 reportedly can stimulate dark respiration by increasing carbohydrates or intensifying maintenance and growth respiration (Li et al., 2013; Thomas and Griffin, 1994). In this study, the Rd,w of Angelica transplants under eCO2 was intensified as the result of increased carbohydrates and enhanced growth.

The increase in biomass accumulation caused by eCO2 also depends on the plant sink size or nutrient supply (Kirschbaum, 2011). Only if the plants can make full use of the increased photosynthetically synthesized carbon can their dry weights respond strongly to eCO2. In this experiment, the plants were still young and had not yet developed large roots to consume the artificially increased carbon. In addition, the nutrient supply was not adjusted to meet the increased requirements of transplants under eCO2. Thus, the enhancement of the biomass of Angelica transplants caused by eCO2 weakened with exposure time and diminished after 15 d of treatment. It is important to detect the response of plant growth to eCO2 and take measures as soon as possible to maintain the strong response of plant growth to eCO2.

Conclusions

In conclusion, the Pn,w and Rd,w were monitored with altered growth chambers. WE of Angelica transplants grown under eCO2 and aCO2 agreed well with the WM. According to the results, eCO2 increased both the Pn,w and Rd,w but induced photosynthetic acclimation at the end of the experiment. The increase in Pn,w under eCO2 was maintained over the experiment due to increased leaf area. In addition, the increase in transplant dry weight under eCO2 mainly occurred in the first 15 d of treatment. This phenomenon could be detected by the RGR calculated based on the WE. These results indicated that this method can be used to monitor the dry weight accumulation of Angelica transplants under eCO2.

Literature Cited

  • Ainsworth, E.A. & Rogers, A. 2007 The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions Plant Cell Environ. 30 258 270

    • Search Google Scholar
    • Export Citation
  • Amthor, J.S. 1995 Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle Glob. Change Biol. 1 4 851 855

    • Search Google Scholar
    • Export Citation
  • Bowes, G. 1993 Facing the inevitable: Plants and increasing atmospheric CO2 Annu. Rev. Plant Physiol. Plant Mol. Biol. 44 309 332

  • Bruggink, G.T. 1984 Effects of CO2 concentration on growth and photosynthesis of young tomato and carnation plants Acta Hort. 162 279 280

  • Bugbee, B. 1992 Steady-state canopy gas exchange: System design and operation HortScience 27 7 851 855

  • Burkart, S., Manderscheid, R. & Weigel, H.J. 2007 Design and performance of a portable gas exchange chamber system for CO2- and H2O-flux measurements in crop canopies Environ. Exp. Bot. 61 1 851 855

    • Search Google Scholar
    • Export Citation
  • Campbell, G.S. & Norman, J.M. 1998 An introduction to environmental biophysics. 2nd ed. Springer-Verlag, New York

  • Catchpole, W.R. & Wheeler, C.J. 1992 Estimating plant biomass: A review of techniques Austral. J. Ecol. 17 2 851 855

  • Cho, Y.Y., Oh, S., Oh, M.M. & Son, J.E. 2007 Estimation of individual leaf area, fresh weight, and dry weight of hydroponically grown cucumbers (Cucumis sativus L.) using leaf length, width, and SPAD value Scientia Hort. 111 4 851 855

    • Search Google Scholar
    • Export Citation
  • Dong, J., Li, X., Chu, W. & Duan, Z. 2017 High nitrate supply promotes nitrate assimilation and alleviates photosynthetic acclimation of cucumber plants under elevated CO2 Scientia Hort. 218 275 283

    • Search Google Scholar
    • Export Citation
  • Drake, B.G., Gonzalez-Meler, M.A. & Long, S.P. 1997 More efficient plants: A consequence of rising atmospheric CO2? Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 609 639

    • Search Google Scholar
    • Export Citation
  • Ferraz, T.M., Rodrigues, W.P., Netto, A.T., de Oliveira Reis, F., Peçanha, A.L., Lopes, A., de Assis Figueiredo, F.A.M.M., de Sousa, E.F., Glenn, D.M. & Campostrin, E. 2016 Comparison between single-leaf and whole-canopy gas exchange measurements in papaya (Carica papaya L.) plants Scientia Hort. 209 73 78

    • Search Google Scholar
    • Export Citation
  • Hao, X., Wang, Q. & Khosla, S. 2006 Responses of a long greenhouse tomato crop to summer CO2 enrichment Can. J. Plant Sci. 86 Special Issue 851 855

  • Kirschbaum, M.U. 2011 Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies Plant Physiol. 155 1 851 855

  • Li, M., Kozai, T., Ohyama, K., Shimamura, S., Gonda, K. & Sekiyama, T. 2012a Estimation of hourly CO2 assimilation rate of lettuce plants in a closed system with artificial lighting for commercial production Ecol. Eng. 24 24 851 855

    • Search Google Scholar
    • Export Citation
  • Li, M., Kozai, T., Niu, G., Takagaki, M. & Takagaki, M. 2012b Estimating the air exchange rate using water vapor as a tracer gas in a semiclosed growth chamber Biosyst. Eng. 113 1 851 855

    • Search Google Scholar
    • Export Citation
  • Li, X., Zhang, G., Sun, B., Zhang, S., Zhang, Y., Liao, Y., Zhou, Y., Xia, X., Shi, K. & Yu, J. 2013 Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere Sci. Rep. 3 7478 3433

    • Search Google Scholar
    • Export Citation
  • Long, S.P., Ainsworth, E.A., Rogers, A. & Ort, D.R. 2004 Rising atmospheric carbon dioxide: Plants FACE the Future Annu. Rev. Plant Biol. 55 591 628

  • López-Díaz, J.E., Roca-Fernández, A.I. & González-Rodríguez, A. 2011 Measuring herbage mass by non-destructive methods: A review J. Agr. Sci. Technol. 1 303 314

    • Search Google Scholar
    • Export Citation
  • Lu, G.H., Chan, K., Chan, C., Leung, K., Jiang, Z. & Zhao, Z. 2004 Quantification of ligustilides in the roots of Angelica sinensis and related umbelliferous medicinal plants by high-performance liquid chromatography and liquid chromatography-mass spectrometry J. Chromatography 1046 1 851 855

    • Search Google Scholar
    • Export Citation
  • Mun, B., Jang, Y., Goto, E., Ishigami, Y. & Chun, C. 2011 Measurement system of whole-canopy carbon dioxide exchange rates in grafted cucumber transplants in which scions were exposed to different water regimes using a semiopen multichamber Scientia Hort. 130 3 851 855

    • Search Google Scholar
    • Export Citation
  • Poorter, H. 1993 Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration Vegetatio 104/105 77 97

  • Prior, S.A., Torbert, H.A., Runion, G.B. & Rogers, H.H. 2003 Implications of elevated CO2-induced changes in agroecosystem productivity J. Crop Prod. 8 217 244

    • Search Google Scholar
    • Export Citation
  • Qian, T., Dieleman, J.A., Elings, A. & Marcelis, L.F.M. 2012 Leaf photosynthetic and morphological responses to elevated CO2, concentration and altered fruit number in the semiclosed greenhouse Scientia Hort. 145 3 851 855

    • Search Google Scholar
    • Export Citation
  • Rachel, F. & Gail, T. 2010 Contrasting effects of elevated CO2 on the root and shoot growth of four native herbs commonly found in chalk grassland New Phytol. 125 4 851 855

    • Search Google Scholar
    • Export Citation
  • Sanchez Guerrero, M.C., Lorenzo, P., Medrano, E., Castilla, N., Soriano, T. & Baille, A. 2005 Effect of variable CO2 enrichment on greenhouse production in mild winter climates Agr. For. Meteorol. 132 3 851 855

    • Search Google Scholar
    • Export Citation
  • Stitt, M. & Krapp, A. 1999 The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background Plant Cell Environ. 22 583 621

    • Search Google Scholar
    • Export Citation
  • Teitel, M., Liran, O., Tanny, J. & Barak, M. 2008 Wind driven ventilation of a mono-span greenhouse with a rose crop and continuous screened side vents and its effect on flow patterns and microclimate Biosyst. Eng. 101 1 851 855

    • Search Google Scholar
    • Export Citation
  • Thomas, R.B. & Griffin, K.L. 1994 Direct and indirect effects of atmospheric carbon dioxide environment on leaf respiration of Glycine max (L.) Merr Plant Physiol. 103 355 361

    • Search Google Scholar
    • Export Citation
  • Usuda, H. 2004 Evaluation of the effect of photosynthesis on biomass production with simultaneous analysis of growth and continuous Monitoring of CO2 exchange in the whole plants of radish, cv Kosena under ambient and elevated CO2 Plant Prod. Sci. 7 4 851 855

    • Search Google Scholar
    • Export Citation
  • Van Henten, E.J. 1994 Validation of a dynamic lettuce growth model for greenhouse climate control Agr. Syst. 45 1 851 855

  • Van Henten, E.J. & Bontsema, J. 1995 Non-destructive crop measurements by image processing for crop growth control J. Agr. Eng. Res. 61 2 851 855

  • Wheeler, R.M., Mackowiak, C.L., Sager, J.C., Yorio, N.C., Knott, W.M. & Berry, W.L. 1994a Growth and gas exchange by lettuce stands in a closed, controlled environment J. Amer. Soc. Hort. Sci. 119 3 851 855

    • Search Google Scholar
    • Export Citation
  • Wheeler, R.M., Mackowiak, C.L., Sager, J.C. & Knott, W.M. 1994b Growth of soybean and potato at high CO2 partial pressures Adv. Space Res. 14 251 255

  • Wheeler, T.R., Daymond, A.J., Morison, J., Ellis, R.H. & Hadley, P. 2015 Acclimation of photosynthesis to elevated CO2 in onion (Allium cepa) grown at a range of temperatures Ann. Appl. Biol. 144 1 851 855

    • Search Google Scholar
    • Export Citation
  • Woodward, F. 2002 Potential impacts of global elevated CO2 concentrations on plants Curr. Opin. Plant Biol. 5 207 211

  • Yelle, S., Beeson, R.C.J., Trudel, M.J. & Gosselin, A. 1990 Duration of CO2 enrichment influences growth, yield, and gas exchange of two tomato species J. Amer. Soc. Hort. Sci. 115 52 57

    • Search Google Scholar
    • Export Citation
  • Yokoi, S., Kozai, T., Hasegawa, T., Chun, C. & Kubota, C. 2005 CO2 and water utilization efficiencies of a closed transplant production system as affected by leaf area index of tomato seedling populations and the number of air exchanges (in Japanese) J. Soc. High Technol. Agr. 17 182 191

    • Search Google Scholar
    • Export Citation

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Contributor Notes

This work was supported by the Fundamental Research Funds of China Agricultural University and the open projects of Key Laboratory of Protected Agriculture Engineering in the Middle and Lower Reaches of Yangtze River, Ministry of Agriculture.

Corresponding author. E-mail: lim_abe@cau.edu.cn.

  • View in gallery

    CO2 injection rate and CO2 concentrations inside and outside the growth chamber during the photoperiod (A) and dark period (B). Data represent the mean ± sd. CO2 = carbon dioxide.

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    Number of Angelica transplants inside the growth chamber.

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    Dry weight accumulation of Angelica transplants estimated based on the whole-plant net photosynthetic rate and dark respiration rate (WE) plotted against the measured dry weight (WM). Data represent the mean ± sd.

  • View in gallery

    Whole-plant net photosynthetic rate of Angelica transplants (Pn,w) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations.

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    Whole-plant dark respiration rate of Angelica transplants (Rd,w) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations.

  • View in gallery

    Response of net photosynthetic rate of Angelica transplants (Pl) grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations to different CO2 concentrations at the end of experiment. Data represent the mean ± sd.

  • View in gallery

    Estimated net photosynthetic rate of Angelica transplants per leaf area (Pl) under Data represent the mean ± sd.

  • View in gallery

    Leaf area of Angelica transplants grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2) concentrations. Data represent the mean ± sd.

  • View in gallery

    Dry weight accumulation of Angelica transplants grown under elevated carbon dioxide (eCO2) and ambient carbon dioxide (aCO2). (* and NS indicate significant differences at P < 0.05 and nonsignificant differences, respectively.) Data represent the mean ± sd.

  • View in gallery

    Relative growth rate (RGR) of Angelica transplants calculated based on the estimated dry weight of the transplants grown. Data represent the mean ± sd.

  • Ainsworth, E.A. & Rogers, A. 2007 The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions Plant Cell Environ. 30 258 270

    • Search Google Scholar
    • Export Citation
  • Amthor, J.S. 1995 Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle Glob. Change Biol. 1 4 851 855

    • Search Google Scholar
    • Export Citation
  • Bowes, G. 1993 Facing the inevitable: Plants and increasing atmospheric CO2 Annu. Rev. Plant Physiol. Plant Mol. Biol. 44 309 332

  • Bruggink, G.T. 1984 Effects of CO2 concentration on growth and photosynthesis of young tomato and carnation plants Acta Hort. 162 279 280

  • Bugbee, B. 1992 Steady-state canopy gas exchange: System design and operation HortScience 27 7 851 855

  • Burkart, S., Manderscheid, R. & Weigel, H.J. 2007 Design and performance of a portable gas exchange chamber system for CO2- and H2O-flux measurements in crop canopies Environ. Exp. Bot. 61 1 851 855

    • Search Google Scholar
    • Export Citation
  • Campbell, G.S. & Norman, J.M. 1998 An introduction to environmental biophysics. 2nd ed. Springer-Verlag, New York

  • Catchpole, W.R. & Wheeler, C.J. 1992 Estimating plant biomass: A review of techniques Austral. J. Ecol. 17 2 851 855

  • Cho, Y.Y., Oh, S., Oh, M.M. & Son, J.E. 2007 Estimation of individual leaf area, fresh weight, and dry weight of hydroponically grown cucumbers (Cucumis sativus L.) using leaf length, width, and SPAD value Scientia Hort. 111 4 851 855

    • Search Google Scholar
    • Export Citation
  • Dong, J., Li, X., Chu, W. & Duan, Z. 2017 High nitrate supply promotes nitrate assimilation and alleviates photosynthetic acclimation of cucumber plants under elevated CO2 Scientia Hort. 218 275 283

    • Search Google Scholar
    • Export Citation
  • Drake, B.G., Gonzalez-Meler, M.A. & Long, S.P. 1997 More efficient plants: A consequence of rising atmospheric CO2? Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 609 639

    • Search Google Scholar
    • Export Citation
  • Ferraz, T.M., Rodrigues, W.P., Netto, A.T., de Oliveira Reis, F., Peçanha, A.L., Lopes, A., de Assis Figueiredo, F.A.M.M., de Sousa, E.F., Glenn, D.M. & Campostrin, E. 2016 Comparison between single-leaf and whole-canopy gas exchange measurements in papaya (Carica papaya L.) plants Scientia Hort. 209 73 78

    • Search Google Scholar
    • Export Citation
  • Hao, X., Wang, Q. & Khosla, S. 2006 Responses of a long greenhouse tomato crop to summer CO2 enrichment Can. J. Plant Sci. 86 Special Issue 851 855

  • Kirschbaum, M.U. 2011 Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies Plant Physiol. 155 1 851 855

  • Li, M., Kozai, T., Ohyama, K., Shimamura, S., Gonda, K. & Sekiyama, T. 2012a Estimation of hourly CO2 assimilation rate of lettuce plants in a closed system with artificial lighting for commercial production Ecol. Eng. 24 24 851 855

    • Search Google Scholar
    • Export Citation
  • Li, M., Kozai, T., Niu, G., Takagaki, M. & Takagaki, M. 2012b Estimating the air exchange rate using water vapor as a tracer gas in a semiclosed growth chamber Biosyst. Eng. 113 1 851 855

    • Search Google Scholar
    • Export Citation
  • Li, X., Zhang, G., Sun, B., Zhang, S., Zhang, Y., Liao, Y., Zhou, Y., Xia, X., Shi, K. & Yu, J. 2013 Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere Sci. Rep. 3 7478 3433

    • Search Google Scholar
    • Export Citation
  • Long, S.P., Ainsworth, E.A., Rogers, A. & Ort, D.R. 2004 Rising atmospheric carbon dioxide: Plants FACE the Future Annu. Rev. Plant Biol. 55 591 628

  • López-Díaz, J.E., Roca-Fernández, A.I. & González-Rodríguez, A. 2011 Measuring herbage mass by non-destructive methods: A review J. Agr. Sci. Technol. 1 303 314

    • Search Google Scholar
    • Export Citation
  • Lu, G.H., Chan, K., Chan, C., Leung, K., Jiang, Z. & Zhao, Z. 2004 Quantification of ligustilides in the roots of Angelica sinensis and related umbelliferous medicinal plants by high-performance liquid chromatography and liquid chromatography-mass spectrometry J. Chromatography 1046 1 851 855

    • Search Google Scholar
    • Export Citation
  • Mun, B., Jang, Y., Goto, E., Ishigami, Y. & Chun, C. 2011 Measurement system of whole-canopy carbon dioxide exchange rates in grafted cucumber transplants in which scions were exposed to different water regimes using a semiopen multichamber Scientia Hort. 130 3 851 855

    • Search Google Scholar
    • Export Citation
  • Poorter, H. 1993 Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration Vegetatio 104/105 77 97

  • Prior, S.A., Torbert, H.A., Runion, G.B. & Rogers, H.H. 2003 Implications of elevated CO2-induced changes in agroecosystem productivity J. Crop Prod. 8 217 244

    • Search Google Scholar
    • Export Citation
  • Qian, T., Dieleman, J.A., Elings, A. & Marcelis, L.F.M. 2012 Leaf photosynthetic and morphological responses to elevated CO2, concentration and altered fruit number in the semiclosed greenhouse Scientia Hort. 145 3 851 855

    • Search Google Scholar
    • Export Citation
  • Rachel, F. & Gail, T. 2010 Contrasting effects of elevated CO2 on the root and shoot growth of four native herbs commonly found in chalk grassland New Phytol. 125 4 851 855

    • Search Google Scholar
    • Export Citation
  • Sanchez Guerrero, M.C., Lorenzo, P., Medrano, E., Castilla, N., Soriano, T. & Baille, A. 2005 Effect of variable CO2 enrichment on greenhouse production in mild winter climates Agr. For. Meteorol. 132 3 851 855

    • Search Google Scholar
    • Export Citation
  • Stitt, M. & Krapp, A. 1999 The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background Plant Cell Environ. 22 583 621

    • Search Google Scholar
    • Export Citation
  • Teitel, M., Liran, O., Tanny, J. & Barak, M. 2008 Wind driven ventilation of a mono-span greenhouse with a rose crop and continuous screened side vents and its effect on flow patterns and microclimate Biosyst. Eng. 101 1 851 855

    • Search Google Scholar
    • Export Citation
  • Thomas, R.B. & Griffin, K.L. 1994 Direct and indirect effects of atmospheric carbon dioxide environment on leaf respiration of Glycine max (L.) Merr Plant Physiol. 103 355 361

    • Search Google Scholar
    • Export Citation
  • Usuda, H. 2004 Evaluation of the effect of photosynthesis on biomass production with simultaneous analysis of growth and continuous Monitoring of CO2 exchange in the whole plants of radish, cv Kosena under ambient and elevated CO2 Plant Prod. Sci. 7 4 851 855

    • Search Google Scholar
    • Export Citation
  • Van Henten, E.J. 1994 Validation of a dynamic lettuce growth model for greenhouse climate control Agr. Syst. 45 1 851 855

  • Van Henten, E.J. & Bontsema, J. 1995 Non-destructive crop measurements by image processing for crop growth control J. Agr. Eng. Res. 61 2 851 855

  • Wheeler, R.M., Mackowiak, C.L., Sager, J.C., Yorio, N.C., Knott, W.M. & Berry, W.L. 1994a Growth and gas exchange by lettuce stands in a closed, controlled environment J. Amer. Soc. Hort. Sci. 119 3 851 855

    • Search Google Scholar
    • Export Citation
  • Wheeler, R.M., Mackowiak, C.L., Sager, J.C. & Knott, W.M. 1994b Growth of soybean and potato at high CO2 partial pressures Adv. Space Res. 14 251 255

  • Wheeler, T.R., Daymond, A.J., Morison, J., Ellis, R.H. & Hadley, P. 2015 Acclimation of photosynthesis to elevated CO2 in onion (Allium cepa) grown at a range of temperatures Ann. Appl. Biol. 144 1 851 855

    • Search Google Scholar
    • Export Citation
  • Woodward, F. 2002 Potential impacts of global elevated CO2 concentrations on plants Curr. Opin. Plant Biol. 5 207 211

  • Yelle, S., Beeson, R.C.J., Trudel, M.J. & Gosselin, A. 1990 Duration of CO2 enrichment influences growth, yield, and gas exchange of two tomato species J. Amer. Soc. Hort. Sci. 115 52 57

    • Search Google Scholar
    • Export Citation
  • Yokoi, S., Kozai, T., Hasegawa, T., Chun, C. & Kubota, C. 2005 CO2 and water utilization efficiencies of a closed transplant production system as affected by leaf area index of tomato seedling populations and the number of air exchanges (in Japanese) J. Soc. High Technol. Agr. 17 182 191

    • Search Google Scholar
    • Export Citation