Can higher CO₂ concentrations affect yield and quality parameters in lettuce and sugar beet crops?

O aumento de CO₂ pode afetar os parâmetros de rendimento e qualidade nas culturas de alface e beterraba sacarina?

¿El aumento de CO₂ puede afectar los parámetros de rendimiento y calidad en los cultivos de lechuga y remolacha azucarera?

Pedro Alexander Velasquez-Vasconez¹; Maria Alejandra Velasquez-Vasconez²; Cristian Cardenas³; Øyvind Skarsgard Nyheim⁴; Hugo Ruiz-Eraso⁵

¹Ph.D. Student. Genetics and Plant Breeding. Escola Superior de Agricultura “Luis de Queiroz” – Universidade de São Paulo. Piracicaba, São Paulo, Brasil. (55) 19971685578. pavelasquezv@usp.br; ²Zootechnist. Universidad de Nariño, Pasto, Nariño, Colombia. alejitavelasquezvasconez@gmail.com; ³Agricultural Engineer Universidad de Nariño, Pasto, Nariño, cris30tn@gmail.com; ⁴MSc. Student. Norwegian University of Life Sciences, oyvind0810@gmail.com; ⁵Ph.D. Soils and Plant Nutrition. Universidad de Nariño, Pasto, Nariño, Colombia. (55) 3217565392. hugoruize@yahoo.com

Recebido: 14/08/2020; Aprovado: 30/11/2020

Abstract: It has been suggested that the increase in CO₂ levels in the coming decades will have positive consequences on the nutritional content and yield of agricultural crops. However, the effects of the increase in CO₂ concentrations remain little known in Andean region. This study evaluated the effect of increased CO₂ on the protein content and growth of sugar beet and lettuce plants in the Andean region of Colombia. We used a Randomized Complete Block Design, strip 1 was open field, strip 2 was low tunnel with ambient CO₂ and strip 3 was low tunnel with 1000 ppm CO₂. The sugar beet experiment three harvest periods were evaluated. The results indicated that CO₂ fertilization did not have a significant effect on the yield and head diameter of the lettuce. However, biomass production tended to increase in the first sugar beet harvest but decreased significantly in the last two harvests, probably due to a negative effect caused by acclimatization to CO₂ enrichment. The protein content was not affected by the increase in CO₂ levels in any of the crops. The results suggest the increase in atmospheric CO₂ in the next years will not cause any benefit in lettuce or sugar beet grown in the Andean region.

Key words: Protected crops; Climatic change; Carbon fertilization; Vegetables; Plant nutrition.

Resumo: A literatura sugere que o aumento dos níveis de CO₂ nas próximas décadas terá consequências positivas no conteúdo nutricional e na produtividade das culturas agrícolas. No entanto, os efeitos do aumento do CO₂ são pouco conhecidos nas regiões Andinas. Este estudo avaliou o efeito do aumento de CO₂ no conteúdo de proteína e no crescimento de plantas de beterraba e alface na região andina da Colômbia. O estudo foi conduzido em um Delineamento Blocos Casualizados onde a faixa 1 foi campo aberto, a faixa 2 foi o com concentrações de CO₂ ambiental e faixa 3 foi o túnel baixo com aumento da concentração de CO₂ de 1000 ppm. As avaliações em beterraba foram realizadas em três safras. Os resultados indicam que a fertilização com CO₂ não teve efeito significativo na produtividade e no diâmetro da cabeça da alface. Por outro lado, a produção de biomassa teve uma tendência a aumentar na primeira safra de beterraba, mas diminui significativamente nas duas últimas safras, provavelmente devido às características de cumprimento curtas em altitudes mais elevadas que influencia as fixações de CO₂, como também das condições climáticas nestas regiões que podem alterar o crescimento das plantas. Os resultados sugerem que o aumento do CO₂ atmosférico devido às mudanças climáticas não trará nenhum benefício na produtividade das comodities agrícolas Andinas.

Palavras-chave: Cultivo protegido; Mudanças climáticas; Fertilização com carbono; Vegetais; Nutrição de plantas.

Resumen: La literatura sugiere que el aumento de CO₂ en las próximas décadas tendrá consecuencias positivas sobre el contenido nutricional y la productividad de los cultivos agrícolas. Sin embargo, los efectos del aumento de CO₂ son poco conocidos en las regiones de los Andes. Este estudio evaluó el efecto del incremento de CO₂ sobre el contenido de proteína y el crecimiento de las plantas de remolacha y lechuga en la región andina de Colombia. El estudio se realizó en un diseño de bloques completos al azar donde los tratamientos fueron cultivo a campo abierto, cultivo bajo condiciones de microtúnel con concentraciones de CO₂ ambiental y cultivo bajo condiciones de microtúnel con 1000 ppm de CO₂. Las evaluaciones de remolacha se realizaron en tres cosechas. Los resultados indican que la fertilización con CO₂ no tuvo un efecto significativo sobre la productividad y el diámetro de la lechuga. Por otro lado, la producción de biomasa tuvo un aumento en la primera cosecha de remolacha, pero disminuyó significativamente en las dos últimas cosechas, probablemente debido a las características de cumplimiento corto en altitudes más altas que influyen en las fijaciones de CO₂, así como las condiciones climáticas que, en estas regiones, pueden alterar el crecimiento de las plantas. Los resultados sugieren que el aumento de CO₂ atmosférico debido al cambio climático no traerá ningún beneficio en la productividad de las empresas agrícolas Andinas.

Palabras clave: Cultivo protegido; Cambio climático; Fertilización con carbono; Hortalizas; Nutrición vegetal.

INTRODUCTION

For the last 650,000 - 800,000 years CO₂ concentrations in the atmosphere have not exceeded 280 ppm (LUTHI et al., 2008). However, with the industrial revolution, CO₂ levels started to rise dramatically and may reach levels close to 1000 ppm by the end of the 21st century (FUSS et al., 2014). Rising CO₂ levels is predicted to stimulate the yield of C3 crops by reducing stomatal conductance and by stimulating CO₂ uptake (GRAY et al., 2016). In lettuce, studies have shown that increasing CO₂ concentrations improves productivity (FURLAN et al., 2001; PÉREZ-LÓPEZ et al., 2013). In addition, several other factors also influence the effects of elevated CO₂ levels in crops, including genotype, exposure time and environmental conditions.

The short timescale and many influencing factors make it hard to predict how plants will respond to higher CO₂ levels based solely on the available scientific literature. For instance, several studies have found that the benefits of carbon fertilization are lost in the long term, when plants acclimatize to CO_2. Lee et al. (2011) and Warren et al. (2011) showed how the effect of CO₂ fertilization on plants tends to decrease over time, eventually stabilizing at the same level of photoassimilate production as before CO₂ fertilization.

The chemical properties of rubisco are highly dependent on the CO₂ concentration in the environment. Under natural conditions, the oxygen concentration around the leaf is much higher (210 000 µmol mol^-1) than the CO₂ concentration inside the chloroplasts (415 µmol mol^-1) (BUSCH, 2020). Increasing CO₂ concentrations increases carboxylation and suppresses the oxidation of rubisco, stimulating the photosynthetic rate. The CO₂ concentration around the rubisco can be affected by the resistance to CO₂ diffusion imposed by the membrane and cell wall of the stomata and mesophyll. These biochemical properties cause a progressive gradient from the CO₂ concentration in the environment to the chloroplasts (BUCKLEY, 2019). Changes in CO₂ concentrations can be strongly influenced by external conditions such as light intensity and quality, CO₂ concentration, air humidity and the general water status of the plant (BUCKLEY, 2019).

Some studies have suggested food quality will decrease as CO₂ levels in the atmosphere increase. Bloom et al., (2014), Duval et al. (2013) and Weigel; Manderscheid (2012) showed that protein content in plants, as well as zinc, iron and sulfur content can decrease due to high CO₂ concentrations. However, there are few studies on the effect of increasing CO₂ on horticultural crops in the Andean region. This study evaluated the effect of elevated CO₂ concentrations on the protein content and yield of sugar beet and lettuce plants.

MATERIAL AND METHODS

The research was carried out at Botana Experimental Center, University of Nariño, located at 1° 10' latitude N and 77° 16' longitude W, altitude 2960 MASL. The center has an average temperature of 12 °C, annual rainfall of 900 mm, relative humidity 73%, solar brightness 1182 hours/year and average radiation between 4 and 4.5 kWh/m2/day (IDEAM, 2014). The experiment was carried out in Vitric Haplustands soils. The relative humidity and temperature values were collected with CO₂ sensors (NDIR, non-dispersive infrared).

Culture conditions

Two experiments were performed to evaluate the effect of elevated CO₂ levels on sugar beet, a biennial plant, and lettuce, a short-cycle plants. The first experiment was conducted on 210 sugar beet plants of the Altissima variety. The seedlings were transplanted with 45 cm between each plant and planted in three beds 18 m long and 0.8 m wide. The second experiment was conducted with 245 Batavia lettuce of the Coolguard variety. Lettuce seedlings were also planted in three beds 18 m long and 0.8 m wide, but with only 40 cm between each plant.

This variety has a life cycle of more than two years and grows mainly in the tropical zone. The plants develop glabrous leaves and the large petiolate leaf at the base of the stem. The Coolguard variety has a compact head, along with thick and wavy leaves. The leaves form a closed head and protects of protecting the bud from mechanical damage.

Experimental design

The two experiments (lettuce and sugar beet) were conducted using a strip within Randomized Complete Block Design, with three treatments: strip 1 field planting, strip 2 low tunnel and strip 3 low tunnel with elevated CO₂ (around 1000 ppm). For each treatment, we used three randomized blocks.

CO₂ supply system in low tunnel

The low tunnel system was built with iron arches covered with plastic (polyethylene). Each low tunnel was 18 m long, 0.8 m wide and 0.6 m high. CO₂ was supplied by a tank with a storage capacity of 25 kg. The gas outlet force was controlled with a pressure regulator (ref: CO₂ TM 425-CD100-325) coupled to the tank valve. A stop valve located at the end of the regulator, controlled the CO₂ outflow. The high-pressure hose was extended from the stop valve to the experimental field. The hose was perforated every 5 cm to facilitate CO₂ diffusion inside the low tunnel. CO₂ enrichment was carried out daily from 10 am to 3 pm the concentration was around 1000 ppm (Table 1). The CO₂ concentration was recorded with a CO₂ sensor (NDIR, non-dispersive infrared, model CO210, accuracy ± 50 ppm).

The variables in sugar beet and lettuce

In sugar beet we evaluated foliar biomass in three harvest periods. The first collection was made by cutting the leaves after 60 days. In the second collection, another leaf cut was made after 45 days. In the third and last collection, a leaf cut was made at 45 days. In lettuce, the evaluated parameters were days to harvest, number of leaves, head diameter, protein concentration and yield. The parameters were measured when more than 50% of the lettuces had formed their compact heads. The protein content was determined by means of a bromatological analysis. In the two experiments (lettuce and sugar beet), variance analysis was performed with the statistical software SAS, version 9.4. The treatments were compared using the Duncan test at significance level p<0.05.

Table 1. Mean temperature, relative humidity and atmospheric concentration of CO₂ in the three culture conditions (field planting, low tunnel and low tunnel with elevated CO₂) in sugar beet.

Culture system	Sugar beet			Lettuce
	Temperature (°C)	Relative humidity (%)	CO2 concentration (ppm)	Temperature (°C)	Relative humidity (%)	CO2 concentration (ppm)
Field planting	18.3	61.2	406.7 ±7.1 sd	17.2	68.5	404.9 ±4.3 sd
Low tunnel	27.2	54.9	392.5 ±4.2 sd	25.8	59.9	383.6 ±2.3 sd
Low tunnel with elevated CO2	28.6	55.2	1097.7 ±224.1 sd	27.1	57.1	1027.9 ±184.2 sd

RESULTS AND DISCUSSION

For sugar beet in low tunnel, CO₂ fertilization led to a non-significant increase of 3,4% in the first harvest, while in the second and third harvest, yield decreased significantly by 12% (Fig. 1). Considering all three harvests, the yield of the sugar beet plants grown in low tunnel was 8.6% lower when subject to CO₂ fertilization.

Figure 1. Effect of three types of culture conditions (field planting, low tunnel and low tunnel with elevated CO₂) on sugar beet yield in the three harvests. There was no biomass production in the open field in the first harvest. Different letters indicate a significant difference.

Elevated CO₂ concentrations did not significantly affect any of the evaluated variables in lettuce plants. The increase in CO₂ concentrations tended to increase the yield, but not significantly (Fig. 2). Bromatological analysis suggested that CO₂ fertilization did not affect dry matter and protein percentage values in sugar beet or lettuce (Fig. 3-4).

Figure 2. Effect of three types of culture conditions (field planting, low tunnel and low tunnel with elevated CO₂) on sugar beet yield in the three harvests. Different letters indicate a significant difference.

Figure 3. Average protein and dry matter percentage for sugar beet produced in low tunnel systems with and without elevated CO₂ levels. Different letters indicate a significant difference.

Figure 4. Average protein and dry matter percentage for lettuce produced in low tunnel systems with and without elevated CO₂ levels. Different letters indicate a significant difference.

Average air temperature in low tunnel was 9.6 °C higher for sugar beet and 9.2 °C higher for lettuce (Table 1) compared to open field planting. In both species, air humidity was approximately 10% lower in the low tunnel. These conditions affected both precocity and foliar biomass in sugar beet plants. The low tunnel microclimate affected the growth rate of both sugar beet and lettuce. Sugar beet grown under the warmer temperatures of the low tunnel were harvested 30 days earlier. Thus, the low tunnel sugar beet culture produced three harvests during the five months of the experiment, while field planting produced only two. As a result, open field planting yielded 39.9% less foliar biomass overall than low tunnel planting. In lettuce, low tunnel conditions increased the number of leaves and head diameter by 25.4% and 27.9% respectively, compared to field planting (Fig. 5-6). In addition, the lettuce plants grown in low tunnel were harvested 10 days earlier than in open field conditions.

Figure 5. Effect of three different culture conditions (field planting, low tunnel and low tunnel with elevated CO₂) on head diameter of lettuce. Different letters indicate a significant difference.

Figure 6. Effect of three types of culture conditions (field planting, low tunnel and low tunnel with elevated CO₂) on the number of lettuce unfolded leaves. Different letters indicate a significant difference.

In our study, CO₂ fertilization did not lead to higher yields in sugar beet and lettuce. Sugar beet yields actually dropped significantly in the last two harvests with CO₂ enrichment. This yield reduction can be explained by the sugar beet plants acclimatizing to higher CO₂ levels. Changes in the ultrastructure of chloroplasts in sugar beet in response to long periods of elevated CO₂ levels have been well documented. The elevated CO₂ levels reduced the proportion of total thylakoids and increased chloroplast stroma (TIAN et al., 2020). Biochemical changes can also occur in prolonged periods of high CO₂ exposure. The accumulation of assimilates that are not used in respiration or storage can activate changes in the chloroplast biochemistry to stop the synthesis of photosynthetic components. Studies of long-term exposure to elevated CO₂ levels in five C3 species indicate that the rubisco activation state was reduced after prolonged exposure to high CO₂ concentrations (IÑIGUEZ et al., 2020). Thus, biochemical and morphological changes in chloroplasts induced by elevated CO₂ levels could explain why shoot biomass decreased in the last two harvests compared to control.

Environmental conditions also play an important role in how plants respond to CO₂ fertilization. Temperature and light intensity can influence how efficiently carbon dioxide is utilized, which affects the photosynthetic rate of plants. Pérez-López et al. (2013) found that stoma closure leads implies low CO₂ fixation. Iñiguez et al. (2020) showed that increases in temperature in C3 plants limit the production of rubisco which can result in low photosynthetic rates.

CO₂ enrichment increases net photosynthetic rates, and thus has frequently been demonstrated to increase plant productivity and yield (LONG et al., 2004; LIU et al., 2017; DONG et al., 2018). However, other studies have found no effect from CO₂ fertilization, or a fleeting effect that disappears when plants acclimatize to higher CO₂ levels (GRAY et al., 2016; IÑIGUEZ et al., 2020). Photosynthetic rate models have indicated that lighting is more important than CO₂ enrichment for increasing lettuce yield in greenhouses (JUNG et al., 2018). Besides, some studies demonstrate that higher light intensity increases the concentration of nitrate reductase in lettuce, which could affect the photosynthetic process (SIGNORE et al., 2020).

More studies modeling photosynthetic rates in different temperatures, light conditions and CO₂ concentrations will be necessary in order to predict how plants will respond to higher CO₂ levels. Atmospheric CO₂ concentrations will likely double during the 21st century, and it is vital to know how this increase in CO₂ will affect future food production (FUSS et al., 2014).

Simulations with global climate models (GCMs) suggest that the projected increase in CO₂ will alter global and local climatic conditions in other ways, leading to increasing temperatures, changing precipitation patterns, and more severe droughts- and floods. These diverse effects on local growing conditions also need to be calculated to evaluate the net effect of higher CO₂ concentrations on food production (BEACH et al., 2019). However, more studies are necessary to elucidate the effect increasing carbon dioxide concentrations will have on agricultural crops.

Elevated CO₂ levels did not have a significant effect on the protein and dry matter percentage in our study. The effect of elevated CO₂ levels on protein content depends on other factors, such as genotype and type of fertilizer. For instance, Baslam et al. (2012) showed that the effect of increased CO₂ concentrations on protein accumulation in tissues differed between the two lettuce cultivars “Batavia Rubia Munguía” and “Maravilla de Verano”. Bloom et al. (2014) found that protein concentrations can be reduced in C3 plants subject to higher CO₂ concentrations when an ammonia fertilizer is used. In our study we used an ammonia fertilizer that may have facilitated nitrogen assimilation to proteins. Nevertheless, there is no substantial evidence that increasing CO₂ levels can influence food quality. Our results suggest that lettuce can retain its protein quality while subject to CO₂ concentrations of 1000 ppm.

Interestingly, low tunnel conditions increase the precocity and yield of sugar beet and lettuce. The favorable effect of low tunnel on the growth rate of plants has also been well documented in other studies (JÚNIOR et al., 2004; KUMAR et al., 2018). Low tunnel accelerates the physiological processes in plants mainly due to an increase in temperature. In some cases, the low tunnel system can increase the number of harvests per year, as was demonstrated in lettuce by (VELASQUEZ et al., 2014). Recently, physiological models have been developed to predict the effect of temperature on crop development (HE et al., 2012; KUMUDINI et al., 2014), and the molecular mechanisms involved in how plants respond to temperature changes are being elucidated (BROWN et al., 2013; KINMONTH-SCHULTZ et al., 2018).

CONCLUSIONS

The protein content and yield of lettuce and sugar beet were not affected by elevated CO₂ levels. The sugar beet yield increased due to the enrichment of CO₂ in the first harvest but then decreased significantly in the last two harvests. The Lettuce and sugar beet crops will probably not be affected by increased CO₂ concentrations in the coming years. The effects CO₂ fertilization has on the photosynthesis of crop plants will depend on several factors and more studies are necessary for carbon fertilization to be used in agricultural productions.

REFERENCES

BASLAM, M.; GARMENDIA, I.; GOICOECHEA, N. Elevated CO₂ may impair the beneficial effect of arbuscular mycorrhizal fungi on the mineral and phytochemical quality of lettuce. Annals of Applied Biology, 161(2):180–191, 2012. 10.1111/j.1744-7348.2012.00563.x .

BEACH, R. H.; SULSER, T. B.; CRIMMINS, A.; CENACCHI, N.; COLE, J.; FUKAGAWA, N. K.; MASON-D’CROZ, D.; MYERS, S.; SAROFIM, M. C.; SMITH, M.; ZISKA, L. H. Combining the effects of increased atmospheric carbon dioxide on protein, iron, and zinc availability and projected climate change on global diets: a modelling study. The Lancet Planetary Health, 3(7):307–317, 2019. 10.1016/S2542-5196(19)30094-4.

BLOOM, A.; BURGER, M.; KIMBALL, B.; PINTER, P. Nitrate assimilation is inhibited by elevated CO₂ in field-grown wheat. Nature Climate Change, 4(6):477–480, 2014. 10.1038/nclimate2183.

BROWN, H. E.; JAMIESON, P. D.; BROOKING, I. R.; MOOT, D. J.; HUTH, N. I. Integration of molecular and physiological models to explain time of anthesis in wheat. Annals of Botany, 112(9):1683–1703, 2013. 10.1093/aob/mct224.

BUCKLEY, T. N. How do stomata respond to water status? New Phytologist, 224(1):21–36, 2019. 10.1111/nph.15899.

BUSCH, F. A. Photorespiration in the context of rubisco biochemistry, CO₂ diffusion and metabolism. The Plant Journal, 101(4):919–939, 2020. 10.1111/tpj.14674.

DONG, J.; GRUDA, N.; LAM, S. K.; LI, X.; DUAN, Z. Effects of elevated CO₂ on nutritional quality of vegetables: a review. Frontiers in Plant Science, 9:1–11, 2018. 10.3389/fpls.2018.00924.

DUVAL, B. D.; DIJKSTRA, P.; DRAKE, B. G.; JOHNSON, D. W.; KETTERER, M. E.; MEGONIGAL, J. P.; HUNGATE, B. A. Element pool changes within a scrub-oak ecosystem after 11 years of exposure to elevated CO₂. Plos One, 8(5):2013. 10.1371/journal.pone.0064386.

FURLAN, R. A.; ALVES, D. R.; FOLEGATTI, M. V.; BOTREL, T. A.; MINAMI, K. Carbon dioxide applied via irrigation water to lettuce culture. Horticultura Brasileira, 19(1):25–29, 2001.

FUSS, S.; CANADELL, J. G.; PETERS, G. P.; TAVONI, M.; ANDREW, R. M.; CIAIS, P.; JACKSON, R. B.; JONES, C. D.; KRAXNER, F.; NAKICENOVIC, N.; QUÉRÉ, C. LE; RAUPACH, M. R.; SHARIFI, A.; SMITH, P.; YAMAGATA, Y. Betting on negative emissions. Nature Publishing Group, 4(10):850–853, 2014. 10.1038/nclimate2392.

GRAY, S. B.; DERMODY, O.; KLEIN, S. P.; LOCKE, A. M.; MCGRATH, J. M.; PAUL, E.; ROSENTHAL, D. M.; RUIZ-VERA, U. M.; SIEBERS, M. H.; STRELLNER, R.; AINSWORTH, A.; BERNACCHI, C. J.; LONG, S. P.; ORT, D. R.; LEAKEY, A. D. B. Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean Sharon. Nature Plants, 2(9):1–8, 2016. 10.1038/nplants.2016.132.

HE, J.; LE GOUIS, J.; STRATONOVITCH, P.; ALLARD, V.; GAJU, O.; HEUMEZ, E.; ORFORD, S.; GRIFFITHS, S.; SNAPE, J. W.; FOULKES, M. J.; SEMENOV, M. A.; MARTRE, P. Simulation of environmental and genotypic variations of final leaf number and anthesis date for wheat. European Journal of Agronomy, 42:22–33, 2012. 10.1016/j.eja.2011.11.002.

IÑIGUEZ, C.; CAPÓ‐BAUÇÀ, S.; NIINEMETS, Ü.; STOLL, H.; AGUILÓ‐NICOLAU, P.; GALMÉS, J. (2020). Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms. The Plant Journal, 101(4):897–918, 2020. 10.1111/tpj.14643.

JUNG, D. H.; KIM, T. Y.; CHO, Y.; SON, J. E. Development and validation of a canopy photosynthetic rate Model of lettuce using light intensity, CO₂ concentration, and day after transplanting.. Protected Horticulture and Plant Factory, 27(2):132–139, 2018. 10.12791/KSBEC.2018.27.2.132.

JÚNIOR, A. P. B.; GRANGEIRO, L. C.; NETO, F. B.; NEGREIROS, M. Z.; DE SOUZA, J. D. O.; AZEVEDO, P. E.; DE MEDEIROS, D. C. Lettuce cultivation in low tunnels of agricultural textile. Horticultura Brasileira, 22(4):801–803, 2004.

KINMONTH-SCHULTZ, H. A.; MACEWEN, M. J.; SEATON, D. D.; MILLAR, A. J.; IMAIZUMI, T.; KIM, S.-H. Mechanistic model of temperature influence on flowering through whole-plant accumulation of FT. BioRxiv, 1–38, 2018. 10.1101/267104.

KUMAR, S.; KUMAR, A.; SINGH, S. S.; PRASAD, R.; KANT, S. Effect of plastic low tunnel on flowering and fruiting behaviour during off season of bottle gourd Lagenaria siceraria (Mol.) Standl. International Journal of Current Microbiology and Applied Sciences, 7, 4829–4835. 2018.

KUMUDINI, S.; ANDRADE, F. H.; BOOTE, K. J.; BROWN, G. A.; DZOTSI, K. A.; EDMEADES, G. O.; GOCKEN, T.; GOODWIN, M.; HALTER, A. L.; HAMMER, G. L.; HATFIELD, J. L.; JONES, J. W.; KEMANIAN, A. R.; KIM, S. H.; KINIRY, J.; LIZASO, J. I.; NENDEL, C.; NIELSEN, R. L.; PARENT, B.; TOLLENAAR, M. Predicting maize phenology: intercomparison of functions for developmental response to temperature. Agronomy Journal, 106(6):2087–2097, 2014. 10.2134/agronj14.0200.

LEE, T. D.; BARROTT, S. H.; REICH, P. B. Photosynthetic responses of 13 grassland species across 11 years of free-air CO₂ enrichment is modest, consistent and independent of N supply. Global Change Biology, 17(9):2893–2904, 2011. 10.1111/j.1365-2486.2011.02435.x.

LIU, J.; HUANG, W.; CHI, H.; WANG, C.; HUA, H.; WU, G. Effects of elevated CO₂ on the fitness and potential population damage of Helicoverpa armigera based on two-sex life table. Scientific Reports, 7(1), 2017. 10.1038/s41598-017-01257-7.

LONG, S. P.; AINSWORTH, E. A.; ROGERS, A.; ORT, D. R. Rising a atmospheric carbon dioxide: plants face the future. Annual Review of Plant Biology, 55(1):591–628, 2004. 10.1146/annurev.arplant.55.031903.141610.

LUTHI, D.; FLOCH, M. L. E; BEREITER, B.; BLUNIER, T.; BARNOLA, J.; SIEGENTHALER, U.; RAYNAUD, D.; JOUZEL, J.; FISCHER, H.; KAWAMURA, K.; STOCKER, T. F. High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Letters to Nature, 453(7193):379–382, 2008. 10.1038/nature06949.

PÉREZ-LÓPEZ, U.; MIRANDA-APODACA, J.; MENA-PETITE, A.; MU, A. Responses of nutrient dynamics in barley seedlings to the interaction of salinity and carbon dioxide enrichment. Journal of Plant Physiology, 170(17):1517-1525, 2013. 10.1016/j.envexpbot.2013.11.004.

SIGNORE, A.; BELL, L.; SANTAMARIA, P.; WAGSTAFF, C.; VAN LABEKE, M. C. Red light is effective in reducing nitrate concentration in rocket by increasing nitrate reductase activity, and contributes to increased total glucosinolates content. Frontiers in Plant Science, 11, 2020. 10.3389/fpls.2020.00604.

TIAN, Y.; ZHOU, Y.; ZONG, Y.; LI, J.; YANG, N.; ZHANG, M.; GUO, Z.; SONG, H. Construction of functionally compartmental inorganic photocatalyst-enzyme system via imitating chloroplast for efficient photoreduction of CO₂ to formic acid. ACS Applied Materials and Interfaces, 12(31):34795–34805, 2020. 10.1021/acsami.0c06684.

VELASQUEZ, P.; RUÌZ, H.; CHAVES, G.; LUNA, C. Productivity of lettuce Lactuca sativa in high tunnel conditions on Vitric Haplustands Soil. Revista De Ciencias Agrícolase Ciencias Agrícolas, 31(2):93–105, 2014. 10.22267/rcia.143102.34.

WARREN, J. M.; ELISABETH, P.; WULLSCHLEGER, S. D.; THORNTON, P. E.; HASENAUER, H.; NORBY, R. J. Ecohydrologic impact of reduced stomatal conductance in forests exposed to elevated CO₂. Ecohydrology, 210(4):196–210, 2011. 10.1002/eco.

WEIGEL, H.; MANDERSCHEID, R. Crop growth responses to free air CO₂ enrichment and nitrogen fertilization: rotating barley, ryegrass, sugar beet and wheat. European Journal of Agronomy, 43:97–107,2012. 10.1016/j.eja.2012.05.011.