HORTSCIENCE 54(5):851–855. 2019. https://doi.org/10.21273/HORTSCI13726-18 by measuring the CO2 flux from a canopy with an altered growth chamber (Bugbee, 1992; Teitel et al., 2008). Compared with the mea- Responses of acutiloba surement of gas exchange at the leaf scale, this method can offer a continuous, long-term Kitagawa Transplants to Elevated measurement of CO2 flux at the canopy level (Li et al., 2012a). Most importantly, the Ambient CO2 Concentration canopy net photosynthetic rate measured with this method can be more accurate than Ming Li1 and Wei-tang Song that calculated by scaling up the leaf photo- College of Water Resources and Civil Engineering, Agricultural synthetic rate (Ferraz et al., 2016). This University, Beijing 100083, China; and Key Laboratory of Agricultural methodhasbeenappliedtomeasurethe Pn,w of cucumber transplants (Mun et al., Engineering in Structure and Environment, Ministry of Agriculture and 2011), lettuce (Wheeler et al., 1994a), and Rural Affairs, Beijing 100083, China tomato seedlings (Li et al., 2012b). Dry Additional index words. elevated CO concentration, Angelica, canopy net photosynthetic weight production also has been estimated 2 based on the CO flux from the canopy rate, dark respiration rate, dry weight 2 measured with such methods (Burkart Abstract. Long-term exposure to an elevated ambient carbon dioxide (eCO2) concentra- et al., 2007; Li et al., 2012b; Wheeler tion could weaken or diminish the enhancement of photosynthesis and growth. To et al., 1994b). monitor this response and offer references for growth management, the whole-plant Angelica acutiloba Kitagawa (hereafter photosynthetic rate (Pn,w) and dark respiration rate (Rd,w)ofAngelica acutiloba referred to as ‘‘Angelica’’) is an important Kitagawa transplants were monitored with a growth chamber. The results showed herb of which roots can be processed into that eCO2 increasedboththePn,w and Rd,w by (79 ± 42) % and (126 ± 51) %. The dry a kind of traditional Chinese medicine (Lu weight of transplants under eCO2 was 33.6% greater than that under aCO2. However, the et al., 2004). However, the growth rate of photosynthetic acclimation to eCO2 occurred. The increase in the Pn,w was maintained until Angelica is extremely slow, and it takes the end of the experiment due to increased leaf area. Moreover, the increase in plant dry 1 year to produce transplants, which limits the weight mainly occurred in the first 15 days of treatment. Furthermore, the dry weight yield. The development of high-efficiency estimated based on the Pn,w and Rd,w agreed well with the measured dry weight. The relative cultivation methods to accelerate Angelica growth rate (RGR) calculated with the estimated dry weight demonstrated the response of growth and meet the growing market is transplant growth to eCO2. These results indicated that the proposed method can be used to needed urgently. In this study, adjusted monitor the response of plant growth to eCO2. growth chamber methods were used to esti- mate the Pn,w and Rd,w. The purpose of this study was to examine the effects of eCO2 on CO2 is the substrate for plant photosyn- biomass accumulation (Dong et al., 2017; Angelica transplant growth. The RGR esti- thesis. An eCO2 concentration can stimu- Qian et al., 2012). However, plants with a mated with Pn,w and Rd,w was estimated to late the photosynthetic rate by increasing small sink size or poor nutrient supply cannot check the feasibility of monitoring the Angel- the substrate availability of Rubisco car- make full use of the carbon synthesized under ica transplant growth under eCO2. This work would be helpful for improving the response of boxylation and inhibiting the competitive eCO2 and show a small increase in biomass oxygenation of the enzyme (Long et al., accumulation (Drake et al., 1997; Stitt and plantgrowthtoeCO2. 2004; Stitt and Krapp, 1999). As a result, Krapp, 1999; Woodward. 2002). Bruggink plants exposed to eCO2 usually show accelera- (1984) found that a 40% to 50% increase in Materials and Methods ted growth rates and high yields (e.g., Amthor photosynthesis under eCO of 1000 mmol·mol–1 2 Plant material. Seeds of Angelica acuti- 1995; Bowes, 1993; Drake et al., 1997; increased the RGR by only less than 15%. loba Kitagawa were sown in 120-well plastic Poorter, 1993; Prior et al., 2003). Considering Yelle et al. (1990) reported that eCO of 2 trays filled with rockwool. The trays were that plants grown in horticultural facilities 900 mmol·mol–1 increased the RGR and usually are exposed to low indoor CO placed in a germinating chamber with a 25 C 2 yield of tomato plants only during the first concentrations, eCO is an important tech- temperature and 80% relative humidity to 2 2 weeks of treatment. Moreover, excess nology in horticultural production (e.g., accelerate germination. After 3 d of germi- Sanchez-Guerrero et al., 2005). synthesized carbon can remain in leaves and nation, the trays were moved to a growth The stimulation of photosynthesis by lead to the down-regulation of photosynthesis. chamber with a photoperiod of 16 h Thus, it is necessary to monitor the growth m –2 –1 eCO2 only increases the carbon availability [400 mol·m ·s of photosynthetic photon of plants, and the extent to which stimulated of plants, especially dry weight production, flux density (PPFD)providedby‘‘coolwhite’’ photosynthesis can be translated into stimu- under eCO2. Then, measures of optimizing fluorescent lamps on the top surface of tray]. lated growth depends on the capability of a the environment or fertilization strategies The day/night regimes of temperature and plant to use increased carbon under eCO2 can be implemented to further improve the relative humidity were 25/19 Cand70%/ (Kirschbaum, 2011). Usually, plants with a benefits of eCO2. 80%, respectively. The seedlings were irri- large sink size or optimized nutrient supply The plant dry mass can be estimated non- gated daily with a nutrient solution for can take advantage of eCO2 and show stim- destructively based on the linear regression which the electrical conductivity was main- –1 ulated photosynthetic rates and increased equations by inputting the easily measured tained at 2.0 dS·m . High-purity CO2 was parameters, such as leaf width, length, or supplied with a compressed gas cylinder to SPAD value, etc. (Cho et al., 2007; Van maintain the CO2 concentration inside the Henten and Bontsema, 1995). The develop- growth chamber during the photoperiod at Received for publication 2 Nov. 2018. Accepted ment of information technology further facil- 1000 mmol·mol–1. for publication 3 Feb. 2019. itates the access of those parameters and made Treatments. After 14 d of germination, This work was supported by the Fundamental the estimation of plant dry mass more conve- Angelica seedlings with two expanded leaves Research Funds of China Agricultural University and the open projects of Key Laboratory of nient. However, the linear equation had to be were transplanted into a 50-well tray filled Protected Agriculture Engineering in the Middle validated if the growth conditions were changed with rockwool to avoid emitting CO2 from and Lower Reaches of Yangtze River, Ministry of (Catchpole and Wheeler, 1992; Lopez-D íaz microorganisms into the growth chamber. Agriculture. et al., 2011). In addition, plant dry weight Then, the transplants were transferred to 1Corresponding author. E-mail: [email protected]. production can be estimated nondestructively two controlled-environment growth chambers

HORTSCIENCE VOL. 54(5) MAY 2019 851 (Sanyo Gallenkamp Fitotron, Leicester, UK). At the end of the experiment, three trans- 0· ð Þ The growth chamber was 0.38 m in depth, Nd K · V · Cout Cin plants from each treatment were selected to eR ¼ 0 · eN [8] 0.6 m in length, and 0.55 m in height with a Rd;w measure the CO2 assimilation rate of their volume of 125 L. The air current speed inside the third leaf (counting from the bottom) using a growth chamber was 0.3 m·s–1. The distance The dry weight accumulation of the trans- portable photosynthesis system (LI-6400; LI- from lamps to the top surface of the tray was plants in ‘u’ days (WE,u, g/transplant) was COR, Inc., Lincoln, NE). At the inlet of the estimated as follows: 0.5 m. PPFD onthetopsurfaceofthetraywas leaf chamber, the CO2 concentration was set m –2 –1 at 200, 250, 300, 400, 600, 800, 1000, or 1200 400 mol·m ·s .TheCO2 concentration inside W ; E u X m · –1 the growth chambers during the photoperiod u mol mol . The PPFD and air temperature ¼ þ · · ð · · Þ m –2 –1 was maintained at ambient or elevated CO W0 m j ¼ Lp Pn;w;i Ld Rd;w;i were maintained at 400 mol·m ·s and 2 i 0 concentration (1500 mmol·mol–1) by supplying [9] 25 C, respectively. The measurements were high-purity CO with a compressed gas repeated three times. 2 where W is the initial dry weight of the cylinder. CO was not supplied during the 0 2 transplants (g/transplant), m is the coeffi- dark period. The nutrient solution (Otsuka Results cient for converting moles of CO into mass solution, 1/2 strength) was supplied through 2 (44 · 10–6 g·mmol–1), j is the coefficient for The CO injection rate and CO concen- subirrigation every day. 2 2 converting the CO2 assimilated by trans- trations inside and outside growth chamber Gas exchange measurement and calculations. · –1 –1 plants into dry weight (0.68 g g ; Van Henten, are shown in Fig. 1. The CO2 concentrations During the experiment, the Pn,w (mmol CO2·h / 1994), Lp and Ld are the lengths of the light inside growth chambers with eCO and aCO transplant) and R (mmol CO ·h–1/transplant) 2 2 d,w 2 period and dark period, respectively (h·d–1), and during photoperiod were maintained at 1523 ± were estimated by using the following equations. –1 –1 Pn,w,i and Rd,w,i are the average estimated Pn,w 23 mmol·mol and 313 ± 23 mmol·mol ð Þþ Np · k · V · Cout Cin S and Rd,w on day ‘i,’ respectively. throughout the experiment, respectively. The P ; ¼ [1] n w n The RGR of transplants on day ‘u’ number of transplants inside the growth cham- –1 (RGRu,g·g ) was estimated as follows: ber is shown in Fig. 2. For one growth ð Þ chamber, the number of air exchanges during Nd · k · V · Cout Cin ¼ ð Þ ð Þ Rd;w ¼ [2] RGRE;u ln WE;u ln WE;u1 [10] photoperiod (Np) and dark period (Nd)were n –1 –1 5.73 h and2.31h , respectively. Np and Nd Measurements. CO2 concentrations inside –1 where Np and Nd are the numbers of air of another growth chamber were 1.52 h exchanges of the growth chamber during the and outside the growth chamber were mea- and0.89h–1, respectively. In contrast, photoperiod and dark period, respectively (h–1); sured using an infrared gas analyzer (GMP PPFD on the top of transplants increased k is the coefficient for converting the CO 222; Vaisala Oyj, Helsinki, Finland; preci- with the increase in transplant height. How- 2 m –1 volume into moles (mmol·m–3) calculated fol- sion: ± 15 mol·mol ). The sensors inside ever, the difference in PPFD between the the growth chamber were located at the center lowing Campbell and Norman (1998); V is the transplants under eCO2 and aCO2 waslessthan air volume of the growth chamber (0.125·m3); of the interior space at the same height as that 10 mmol·m–2·s–1. Hence, the effects of this differ- of the sensors located outside. Hourly aver- Cout and Cin are the CO2 concentrations out- ence on transplant growth can be neglected. side and inside the growth chamber, respec- aged data were recorded and used to estimate To test the accuracy of the method used to –1 P and R .TheCO concentrations were tively (mmol·mol ); S is the CO2 supply rate n,w d,w 2 measure the Pn,w and Rd,w, the estimated –1 measured every 10 min and averaged per hour (mmol·h ); and n is the number of transplants in transplant dry weight (WE) was plotted against automatically. The CO injection rate was the growth chamber. 2 the measured dry weight (WM) (Fig. 3). The adjusted manually by adjusting the knob of In this experiment, the constant Np and Nd linear equation of WE and WM for transplants the air pump in the first 2 h of photoperiod to 2 were employed and may cause errors in Pn,w under eCO2 was WM =0.92·WE with an r value maintain the target CO concentration inside and Rd,w. Then, the percent errors in Np (eNp,%), 2 the growth chamber. After then, the CO was Nd (eNd,%),Pn,w (eP,%),andRd,w (eP,%) 2 were calculated as follows: injected into the growth chamber at a constant 0 rate and the accumulated amount of injected CO2 Np Np eNp ¼ 0 · 100% [3] was recorded with a flow meter (TC-1000-200; Np Tokyo Keiso Corp., ). The CO2 injection rate was calculated as the ratio of the accumu- N N 0 d d lated CO2 amount injected into growth chamber eNd ¼ 0 · 100% [4] Nd with time. The data collected during the first 2 h after both the dark–light transition and the 0 light–dark transition were discarded to ensure ¼ Pn;w Pn;w % eP 0 · 100 [5] that the environmental conditions were stable. Pn;w Both NP and Nd were measured in the 0 absence of plants and calculated following Li Rd;w Rd;w et al. (2012b). Every 5 d, five transplants were eR ¼ 0 · 100% [6] Rd;w sampled from each treatment to measure the leaf area and dry weight. The leaves of the where Np# and Nd# are the real number of air –1 sampled transplants were scanned with exchanges per hour (h ) during photoperiod digital cameras, and the area was mea- and dark period, respectively, and Pn,w# and # sured with image analysis software (LIA Rd,w are the real net photosynthetic rate and for Win32, freely available from http:// dark respiration rate of whole-plant (mmol·h–1/ www.agr.nagoya-u.ac.jp/%7Eshinkan/LIA32/ transplant). index). Then, the whole plants were dried at Substituting Eqs. [3] and [5] into Eq. [1], 60 C for 1 week to determine the dry weight e can be calculated as: P with an electronic balance (PL303, precision: 0 · · · ð Þ ±0.001 g; Mettler–Toledo, Greifensee, Swit- ¼ NP K V Cout Cin eP 0 · eN [7] zerland). The significant difference in dry Pn;w Fig. 1. CO2 injection rate and CO2 concentrations weight data were analyzed using analysis of inside and outside the growth chamber during Substituting Eqs. [4] and [6] into Eq. [2], variance at P < 0.05 with Student’s t test in the photoperiod (A) and dark period (B). Data eR can be calculated as: SPSS 22.0 (IBM Corp., Armonk, NY). represent the mean ± SD.CO2 = carbon dioxide.

852 HORTSCIENCE VOL. 54(5) MAY 2019 Fig. 2. Number of Angelica transplants inside the growth chamber. Fig. 6. Response of net photosynthetic rate of Angelica transplants (Pl) grown under elevated Fig. 3. Dry weight accumulation of Angelica carbon dioxide (eCO2) and ambient carbon of 0.96 (P >0.05),whereasitwasWM = transplants estimated based on the whole-plant dioxide (aCO ) concentrations to different CO 2 2 2 0.95·WE with an r value of 0.91 for trans- net photosynthetic rate and dark respiration rate concentrations at the end of experiment. Data plants under aCO2 (P > 0.05). The largest (WE) plotted against the measured dry weight represent the mean ± SD. (W ). Data represent the mean ± SD. differences between WM and WE were less M 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. 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, re- spectively. In contrast, both Pn,w and Rn,w were Fig. 7. Estimated net photosynthetic rate of Angelica Fig. 4. Whole-plant net photosynthetic rate of transplants per leaf area (P ) under Data repre- greater under eCO2 than under aCO2.During l Angelica transplants (Pn,w) grown under ele- sent the mean ± SD. the experiment, the increases in both Pn,w and vated carbon dioxide (eCO ) and ambient carbon m –1 2 Rn,w were (13.9 ± 3.9) mol CO2·h /transplant dioxide (aCO ) concentrations. –1 2 and (13.8 ± 4.2) mmol CO2·h /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)%greaterunder eCO2 than that under aCO2. At the end of the experiment, the re- sponses 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 Fig. 8. Leaf area of Angelica transplants grown under eCO was lower than that of trans- 2 under elevated carbon dioxide (eCO2) and am- plants grown under aCO2; when the third Fig. 5. Whole-plant dark respiration rate of Angelica bient carbon dioxide (aCO2) concentrations. leaf of transplants was exposed to the same transplants (Rd,w) grown under elevated carbon Data represent the mean ± SD. CO2 concentration, it ranged from 50 to dioxide (eCO2) and ambient carbon dioxide –1 1200 mmol·mol .BoththeCO2 compensa- (aCO2) concentrations. tion and saturation points of the transplants experiment, Wm,e was 33.6% greater than under eCO2 decreased. This result suggests Wm,a (Fig. 9). Nevertheless, (Wm,e – Wm,a) that the photosynthesis of transplants under time (Fig. 8). eCO2 stimulated the extension after 15 d of treatment was 81% of that at eCO2 acclimated to the eCO2 by the end of of transplant leaves. In the first 15 d of the end of the experiment. Thus, the en- the experiments (Hao et al., 2006). In addition, treatment, the differences in leaf area be- hancement of eCO2 on dry weights was Pl in each day was calculated as the ratio of tween the transplants under eCO2 and those mainly formed in the first 15 d of treat- Pn,w to leaf area and is shown in Fig. 7. The under aCO2 increased with treatment time ment. 2 results showed that the initial enhancement of Pl and reached 0.0012 m /transplant after 15 d Based on WE,theRGR was calculated under eCO2 weakened with exposure time and of treatment. However, the differences were (Fig. 10). The initial increase in RGR diminished in the last few days of the exper- not further enlarged with the treatment time decreased with exposure time and almost iment. Together with the phenomenon of and became 0.0015 m2/transplant. Thus, the diminished in the last dozen days of the exper- photosynthetic acclimation observed in the stimulation of leaf area by eCO2 mainly iment. Thus, both the initial increases in leaf transplants under eCO2, this result suggested occurred during the first 15 d of treatment. area and dry weight accumulation mainly that the photosynthetic capacity of transplant The dry weights of transplants under occurred in the first 15 d of treatment. These leaves under eCO2 decreased. eCO2 (Wm,e) and aCO2 (Wm,a) increased with results coincide with those of Yelle (1990). The leaf area of the transplants under time. Wm,e was always greater than WaC Hence, the change in plant responses to eCO2 and aCO2 increased exponentially with through the experiment. At the end of the eCO2 can be detected with these methods.

HORTSCIENCE VOL. 54(5) MAY 2019 853 However, the good agreement of WE and WM to meet the increased requirements of trans- indicates that the measured Pn,w and Rd,w plants under eCO2. Thus, the enhancement of were highly accurate. They can be applied for the biomass of Angelica transplants caused further analysis. by eCO2 weakened with exposure time and Photosynthesis is well known to in- diminished after 15 d of treatment. It is impor- crease under eCO2. However, this enhance- tant to detect the response of plant growth to ment is not sustainable after long-term eCO2 and take measures as soon as possible exposure to eCO2, a phenomenon that to maintain the strong response of plant frequently is referred to as photosynthetic growth to eCO2. acclimation or down-regulation (e.g., Ainsworth and Rogers, 2007). The angelica transplants Conclusions under eCO2 also showed this phenomenon. Fig. 9. Dry weight accumulation of Angelica This phenomenon normally occurs in re- In conclusion, the Pn,w and Rd,w were transplants grown under elevated carbon di- sponse to excess nonconstructive carbohy- monitored with altered growth chambers. oxide (eCO ) and ambient carbon dioxide 2 drates due to limited sink size or poor WE of Angelica transplants grown under (aCO2). (* and NS indicate significant differ- nutrient supply. In contrast, plants with a large eCO2 and aCO2 agreed well with the WM. ences at P < 0.05 and nonsignificant differ- According to the results, eCO increased ences, respectively.) Data represent the mean sink size or sufficient nutrient supply can avoid 2 both the P and R but induced photosyn- ± SD. this phenomenon and maintain a high photo- n,w d,w synthetic capacity (Dong et al., 2017; Qian thetic acclimation at the end of the experiment. et al., 2012). The increase in Pn,w under eCO2 was main- There are fewer reports on the response of tained over the experiment due to increased Pn,w to eCO2. According to the results pre- leaf area. In addition, the increase in trans- sented here, the variation in Pn,w differs from plant dry weight under eCO2 mainly occurred that in Pl. The initial increase in Pn,w due to in the first 15 d of treatment. This phenom- eCO2 was maintained until the end of the enon could be detected by the RGR calcu- experiment because the leaf area of the trans- lated based on the WE. These results plants increased in response to eCO2 and thus indicated that this method can be used to offset the impacts of Pl on Pn,w. However, the monitor the dry weight accumulation of An- transplants in the experiment were young, with gelica transplants under eCO2. a leaf area index ranging from 1.3 to 3.4. A further increase in leaf area would intensify Literature Cited shading and no longer increase the canopy Ainsworth, E.A. and A. Rogers. 2007. The re- Fig. 10. Relative growth rate (RGR) of Angelica photosynthetic rate. Then, the positive effect sponse of photosynthesis and stomatal con- transplants calculated based on the estimated dry of eCO2 on the canopy photosynthetic rate ductance to rising [CO2]: mechanisms and weight of the transplants grown. Data represent may be further weakened. environmental interactions. Plant Cell Environ. the mean ± SD. Leaf area plays an important role in plant 30:258–270. growth and the photosynthetic rate. Wheeler Amthor, J.S. 1995. Terrestrial higher-plant response et al. (2015) observed that the under to increasing atmospheric [CO2]inrelationto m · –1 the global carbon cycle. Glob. Change Biol. 1(4): Discussion eCO2 of 532 mol mol showed a greater 243–274. leaf area than those grown under aCO2 of Bowes, G. 1993. Facing the inevitable: Plants and The growth chamber method has been 374 mmol·mol–1. The results of this experi- increasing atmospheric CO2. Annu. Rev. Plant widely applied to measure the Pn,w and Rd,w. ment coincide with those results. However, Physiol. Plant Mol. Biol. 44:309–332. To prevent the inaccuracy of measured Pn,w some reports have observed negative or Bruggink, G.T. 1984. Effects of CO2 concentration and Rd,w, all of the concentration sensors neutral effects of eCO2 on leaf area, which on growth and photosynthesis of young tomato were calibrated with standard gases in ad- result from differences in growth conditions and carnation plants. Acta Hort. 162:279–280. Bugbee, B. 1992. Steady-state canopy gas ex- vance. The pure CO2 was injected into the and plant species (Rachel and Gail, 2010; chamber at a constant rate, which was calcu- Usuda, 2004). change: System design and operation. Hort- Science 27(7):770–776. lated with the accumulated amount of CO2 Dark respiration is a major determinant of Burkart, S., R. Manderscheid, and H.J. Weigel. injected into the chamber during photope- plant dry weight accumulation, as it can return 2007. Design and performance of a portable gas riod. This method had been calibrated by as much as 24%50% of photosynthetically exchange chamber system for CO2- and H2O- draining water from a measuring cylinder fixed carbon to the atmosphere (Amthor, flux measurements in crop canopies. Environ. with pure nitrogen. Thus, the error caused by 1995; Yokoi et al., 2005). However, the effects Exp. Bot. 61(1):25–34. the CO2 injection speed can be neglected. of eCO2 on the Rd,w vary according to plant Campbell, G.S. and J.M. Norman. 1998. An in- Then, the over- or underestimated Pn,w and species and growth conditions. eCO2 report- troduction to environmental biophysics. 2nd ed. Springer-Verlag, New York. Rd,w may be aroused by the number of air edly can stimulate dark respiration by increas- exchanges according to Eqs. [1] and [2]. ing carbohydrates or intensifying maintenance Catchpole, W.R. and C.J. Wheeler. 1992. Estimat- ing plant biomass: A review of techniques. The percent errors in Pn,w (eP) and Rd,w and growth respiration (Li et al., 2013; Thomas Austral. J. Ecol. 17(2):121–131. (eR) caused by the percent errors in number of and Griffin, 1994). In this study, the Rd,w of Cho, Y.Y., S. Oh, M.M. Oh, and J.E. Son. 2007. air exchanges during photoperiod and dark Angelica transplants under eCO2 was in- Estimation of individual leaf area, fresh weight, period can be evaluated with Eqs. [7] and [8]. tensified as the result of increased carbohy- and dry weight of hydroponically grown cu- eP and eR are in proportion to eNp and eNd, drates and enhanced growth. cumbers (Cucumis sativus L.) using leaf length, respectively. It is possible to prevent and The increase in biomass accumulation width, and SPAD value. 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