PLANT SIGNALING & BEHAVIOR 2016, VOL. 11, NO. 4, e1165380 (3 pages) http://dx.doi.org/10.1080/15592324.2016.1165380
ARTICLE ADDENDUM
Properties of nitrogen fertilization are decisive in determining the effects of elevated atmospheric CO2 on the activity of nitrate reductase in plants Ranran Zhang and Shaoting Du College of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou, China
ABSTRACT
ARTICLE HISTORY
The concentration of atmospheric CO2 is predicted to double by the end of this century. The response of higher plants to an increase in atmospheric CO2 often includes a change in nitrate reductase (NR) activity. In a recent study, we showed that, under elevated CO2 levels, NR induction in low-nitrate plants and NR inhibition in high-nitrate plants are regulated by nitric oxide (NO) generated via nitric oxide synthases. This finding provides an explanation for the diverse responses of plants to elevated CO2 levels, and suggests that the use of nitrogen fertilizers on soil will have a major influence on the nitrogen assimilation capacity of plants in response to CO2 elevation.
Received 17 February 2016 Accepted 8 March 2016 KEYWORDS
Elevated CO2; NR activity; nitrate level; nitrogen form; NOS
Abbreviations: CO2, carbon dioxide; NR, nitrate reductase; NO, nitric oxide; NOS, NO synthase; N, nitrogen
Atmospheric CO2 concentrations are rising at an accelerated rate due to anthropogenic activities; the levels are currently estimated at 400–430 ppm, and are predicted to reach 530– 1000 ppm by the end of the 21st century.1 CO2 is an important resource for photosynthesis in plants; thus, CO2 enrichment has the potential to enhance plant productivity.2-4 Many studies have focused on the effect of elevated CO2 on nitrogen assimilation because nitrogen is required by plants in greatest quantity.5-10 Nitrate reductase (NR), the first enzyme in the nitrate assimilation pathway,11 has proven to be one of the enzymes to undergoes clear changes in response to elevated CO2.6 However, over the past 15 years, many studies have demonstrated that CO2 enrichment can cause an increase in,12-16 have no effect on,17 or even decrease NR activity in plants.6,13,16,18-20 The conflicting results of the effects of elevated CO2 on NR activity in plants are shown in Table 1. Some studies have shown that elevated CO2 levels stimulated the activity of NR, e.g., in Arabidopsis,13 tobacco,12 and white pine,21 which were treated with 2, 2, and 1.6 mM nitrate, respectively. Conversely, some researchers observed the opposite effect of CO2 enrichment on NR activity, under high nitrate conditions; Geiger et al.6 reported that elevated CO2 slightly stimulated NR activity in the leaves of tobacco plants fed with 2 mM nitrate, while causing an approximately 30% decrease in leaf NR activity in plants fed with a 6 mM nitrate supply. This result is similar to that of Lekshmy et al.,22 in which CO2 enrichment increased NR activity (by 11%–24%) in the leaves of wheat seedlings grown in low nitrate conditions (5 mM). These findings imply that the effect of elevated CO2 on NR activity in plants is dependent on the nitrate levels in
the growth medium; this was confirmed by our latest report: in low-level nitrate supply conditions, NR activity is stimulated by the basal endogenous nitric oxide (NO) and the NO induced by CO2 enrichment, via an NOS-dependent pathway.10 However, in high-level nitrate conditions, NR activity is inhibited by excess NO gathered from high endogenous NO, and NOSdependent NO generated under elevated CO2.10 Therefore, we assumed that an inflection point of nitrate supply may exist for the upregulation or downregulation of NR activity in plants, in relation to elevated CO2 levels. Such an inflection point might vary with species, physiological state, nutritional availability, and other factors that could affect the basal endogenous NO levels and NOS activity in plants. However, some of the data in Table 1 23–25 is inconsistent with this suggested mechanism, e.g., NR activity under enhanced CO2 conditions were increased in the leaves of tobacco, cucumber, and barley plants growing on high nitrate at 12,23 10,24 and 20 mM,25 respectively. These contrasting results may be attributable to differences in plant culturing; the plants in these studies were grown in quartz crystal sand or perlite and vermiculite, and were watered to field capacity with a complete nutrient solution containing nitrate, either once24 or twice each day23 or weekly.25 In other words, although the level of nitrate used was high, the supply regime was intermittent, rather than sustained; therefore, the plants could be considered to have grown in an overall low nitrate supply. In this context, these studies were also consistent with our hypothesis. However, we cannot completely exclude the possibility that elevated CO2 levels increase NR activity in the case of high nitrate (> 10 mM), since the nitrate levels in our study only ranged from 0.2–10 mM.10
CONTACT Shaoting Du [email protected] Addendum to: Du ST, Zhang RR, Zhang P, Liu HJ, Yan MG, Chen N, Xie HQ, Ke SW. Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. Journal of Experimental Botany 2016; 67 (3): 893–904; doi:10.1093/jxb/erv506. © 2016 Taylor & Francis Group, LLC
e1165380-2
R. ZHANG AND S. DU
Table 1. Studies of NR activity changes under different experimental background in response to elevated CO2. Plants
Position
N source
Tobacco (Nicotian atabacum L)
Leaves
NO3¡
White pine (Pinus strobus) Tobacco nd (Nicotian atabacum L) Arabidopsis (Arabidopsis thaliana) Wheat (Triticum aestivum L)
Leaves Leaves Shoots Shoots
NO3¡ NO3¡ NO3¡ NO3¡
Arabidopsis (Arabidopsis thaliana) Leaves
NO3¡
Tobacco (Nicotian atabacum L)
Leaves
NO3¡
Cucumber (Cucumissativus L)
Leaves
NO3¡
Barley (Hordeum vulgare L)
Leaves
NO3¡
Tobacco (Nicotian atabacum L)
Leaves
NH4NO3
Tobacco (Nicotian atabacum L) Loblolly pine (Pinus taeda) Arabidopsis (Arabidopsis thaliana) Barley (Hordeum vulgare L)
Leaves Leaves Shoots Shoots
NH4NO3 NH4NO3 NH4C NH4 NO3
Cultivation methods
Concentration 2 mM 6 mM 1.6 mM 2 mM 2 mM 0.02–2 mM 4–10 mM 4 mM Fertilized twice daily with a nutrient solution containing 12 mM nitrate. Irrigated daily with a nutrient solution containing 10 mM nitrate Watered twice a week with a nutrient solutioncontaining 20 mM nitrate 1 mM 3 mM 10 mM 1 mM 5.6 g N m¡2 year¡1 2 mM 1 mM
Furthermore, under high nitrate and ammonium conditions, elevated CO2 decreased NR activity regardless of the nitrogen supply levels. For example, elevated CO2 led to a significant (30%–50%) inhibition of NR activities in plants grown at 1, 3, and 10 mM NH4NO3 conditions.6 These results are similar to the findings of Matt et al.12 and Wang et al.,20 in which elevated CO2 decreased NR activity in tobacco and barley growing at 1 mM NH4NO3 conditions. These results may be associated with the fact that CO2 enrichment preferentially stimulates ammonium uptake and assimilation, leading to an accumulation of reduced nitrogen and repression of NR.6 All of these findings indicated that the nitrogen source—concentration, availability, and form—might be a decisive factor directly affecting the rate of nitrate assimilation for plants during an increase in atmospheric CO2. This may have profound implications for research on plant responses to elevated CO2. Although elevated CO2 increased the yield of plants grown on high nitrate conditions,6 excessive use of nitrate fertilizer may result in a low efficiency of nitrogen use. Additionally, in the presence of ammonium, nitrate will also be unutilized. Therefore, a relatively low concentration of nitrate fertilizers may improve NR activity, and consequently promote nitrogen assimilation, alleviating nitrogen pollution and economic losses for farmers.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
Funding This work was financially supported by the Zhejiang Province Natural Science Foundation (No. LY14C130001), the Natural Science foundation of China (Grant Nos 30900170).
Seedling Time of CO2 treatment age
Changes in NR level
References
Vermiculite
45 d
45 d
Nutrition solution Nutrition solution Nutrition solution Nutrition solution
105 d 39 d 35 d 20 d
105 d 25 d 7d 20 d
Nutrition solution
35 d
4h
Quartz crystal sand
35 d
11 d
" # " " " " # " # "
Perlite vermiculite
21 d
2h
"
24
Perlite and vermiculite
16 d
16 d
"
25
Vermiculite
45 d
45 d
6
39 d 22 years 35 d 27 d
25 d 7 years 7d 15 d
# # # # # ¡(no change) #
Nutrition solution Acidic soils Nutrition solution Nutrition solution
6 21 12 13 22 10 23
12 19 13 20
References 1. IPCC. Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press; 2014. 2. Long SP, Ainsworth EA, Rogers A, Ort DR. Rising atmospheric carbon dioxide: plants FACE the future. Ann Rev Plant Biol 2004; 55:591-628; PMID:15377233; http://dx.doi.org/10.1146/annurev.arplant.55.031903. 141610 3. Ainsworth EA, Long SP. What have we learned from 15 years of freeair CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 2005; 165:351-72; PMID:15720649; http://dx.doi. org/10.1111/j.1469-8137.2004.01224.x 4. Ainsworth EA. Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentrations. Global Change Biol 2008; 14:1642-50; http://dx.doi.org/ 10.1111/j.1365-2486.2008.01594.x 5. Cheng SH, Moore BD, Seemann JR. Effects of short- and long-term elevated CO2 on the expression of ribulose-1, 5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiol 1998; 116:715-23; PMID:9489018; http://dx.doi.org/10.1104/pp.116.2.715 6. Stitt M, Krapp A. The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 1999; 22:583-621; http://dx.doi.org/10.1046/j.13653040.1999.00386.x 7. Sun JD, Gibson KM, Kiirats O, Okita TW, Edwards GE. Interactions of nitrate and CO2 enrichment on growth, carbohydrates, and rubisco in arabidopsis starch mutants. Significance of starch and hexose. Plant Physiol 2002; 130:1573-83; PMID:12428022; http://dx.doi.org/ 10.1104/pp.010058 8. Li PH, Ainsworth EA, Leakey ADB, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ. Arabidopsis transcript and metabolite profiles: ecotypespecific responses to open-air elevated [CO2]. Plant Cell Environ 2008; 31:1673-87; PMID:18721265; http://dx.doi.org/10.1111/j.13653040.2008.01874.x 9. Sanz-Saez A, Erice G, Aranjuelo I, Nogues S, Irigoyen JJ, Sanchez-Dıaz M. Photosynthetic down-regulation under elevated CO2 exposure can be prevented by nitrogen supply in nodulated alfalfa. J Plant Physiol
PLANT SIGNALING & BEHAVIOR
10.
11.
12.
13.
14.
15.
16.
17.
2010; 167:1558-65; PMID:20708820; http://dx.doi.org/10.1016/j. jplph.2010.06.015 Du ST, Zhang RR, Zhang P, Liu HJ, Yan MG, Chen N, Xie HQ, Ke SW. Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. J Exp Bot 2016; 3:893-904; PMID:20708820; http://dx.doi.org/10.1093/jxb/erv506 Buchanan BB, Gruissem W, Jones RL. Biochemistry and molecular biology of plants. Rockville, MD: American Society of Plant Physiologists 2000; ISBN: 0-943088-39-9 Matt P, Geiger M, Liu PW, Engels C, Krapp A, Stitt M. Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ 2001; 24:1119-37; http://dx. doi.org/10.1046/j.1365-3040.2001.00771.x Niu YF, Cai RS, Dong HF, Wang H, Tang CX, Zhang YS. Effect of elevated CO2 on phosphorus nutrition of phosphate-deficient Arabidopsis thaliana (L.) Heynh under different nitrogen forms. J Exp Bot 2012; 64:355-67; PMID:23183255; http://dx.doi.org/10.1093/jxb/ ers341 Alexandre A, Silva J, Buapet P, Bjork M, Santos R. Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol Evol 2012; 2(10):2625-2635; PMID:23145346; http://dx.doi.org/10.1002/ece3.333 Hofmann LC, Straub S, Bischof K. Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis. J Exp Bot 2013; 64:899-908; PMID:23314813; http://dx.doi.org/10.1093/jxb/ers369 Sailo N, Verma R, Pandey R, Jain V. Effect of elevated carbon dioxide on nitrogen assimilation and mobilization in wheat and rye genotypes of different ploidy levels. Indian J Plant Physiol 2013; 18:333-8; http:// dx.doi.org/10.1007/s40502-013-0049-4 Cousins AB, Bloom AJ. Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photo-assimilation in maize (Zea mays L.). Plant, Cell Environ 2003; 26:1525-30; http://dx.doi.org/ 10.1046/j.1365-3040.2003.01075.x
e1165380-3
18. Sicher RC. Responses of nitrogen metabolism in N sufficient barley primary leaves to plant growth in elevated atmospheric carbon dioxide. Photosynth Res 2001; 68:193-201; PMID:16228342; http://dx.doi. org/10.1023/A:1012951708207 19. Natali SM, Sa~ nudo-Wilhelmy SA, Lerdau MT. Effects of elevated carbon dioxide and nitrogen fertilization on nitrate reductase activity in sweetgum and loblolly pine trees in two temperate forests. Plant Soil 2009; 314(1):197-210; http://dx.doi.org/10.1007/s11104-008-9718-x 20. Wang L, Pedas P, Eriksson D, Schjoerring JK. Elevated atmospheric CO2 decreases the ammonia compensation point of barley plants. J Exp Bot 2013; 10(64):2713-24; PMID:23740933; http://dx.doi.org/ 10.1093/jxb/ert117 21. Bauer GA, Berntson GM. Ammonium and nitrate acquisition by plants in response to elevated CO2 concentration: the roles of root physiology and architecture. Tree Physiol 2001; 21:137-44; PMID:11303644; http://dx.doi.org/10.1093/treephys/21.2-3.137 22. Lekshmy S, Jain V, Khetarpal S, Pandey R. Inhibition of nitrate uptake and assimilation in wheat seedlings grown under elevated CO2. Indian J Plant Physiol 2013; 18:23-9; http://dx.doi.org/10.1007/s40502-0130010-6 23. Geiger M, Liu PW, Engels C, Harnecker J, Schulze ED, Ludewig F, Sonnewald U, Scheible WR, Stitt M. Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants. Plant Cell Environ 1998; 21:253-68; http://dx.doi.org/10.1046/j.13653040.1998.00277.x 24. Larios B, Ag€ uera E, de la Haba P, Perez-Vicente Maldonado JM. A short-term exposure of cucumber plants to rising atmospheric CO2 increases leaf carbohydrate content and enhances nitrate reductase expression and activity. Planta 2001; 212:305-12; PMID:11216852; http://dx.doi.org/10.1007/s004250000395 25. Robredo A, Perez-L opez U, Miranda-Apodaca J, Lacuesta M. Elevated CO2 reduces the drought effect on nitrogen metabolism in barley plants during drought and subsequent recovery. Environ Exp Bot 2011; 71:399-408; http://dx.doi.org/10.1016/j. envexpbot.2011.02.011
ARTICLE ADDENDUM
Properties of nitrogen fertilization are decisive in determining the effects of elevated atmospheric CO2 on the activity of nitrate reductase in plants Ranran Zhang and Shaoting Du College of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou, China
ABSTRACT
ARTICLE HISTORY
The concentration of atmospheric CO2 is predicted to double by the end of this century. The response of higher plants to an increase in atmospheric CO2 often includes a change in nitrate reductase (NR) activity. In a recent study, we showed that, under elevated CO2 levels, NR induction in low-nitrate plants and NR inhibition in high-nitrate plants are regulated by nitric oxide (NO) generated via nitric oxide synthases. This finding provides an explanation for the diverse responses of plants to elevated CO2 levels, and suggests that the use of nitrogen fertilizers on soil will have a major influence on the nitrogen assimilation capacity of plants in response to CO2 elevation.
Received 17 February 2016 Accepted 8 March 2016 KEYWORDS
Elevated CO2; NR activity; nitrate level; nitrogen form; NOS
Abbreviations: CO2, carbon dioxide; NR, nitrate reductase; NO, nitric oxide; NOS, NO synthase; N, nitrogen
Atmospheric CO2 concentrations are rising at an accelerated rate due to anthropogenic activities; the levels are currently estimated at 400–430 ppm, and are predicted to reach 530– 1000 ppm by the end of the 21st century.1 CO2 is an important resource for photosynthesis in plants; thus, CO2 enrichment has the potential to enhance plant productivity.2-4 Many studies have focused on the effect of elevated CO2 on nitrogen assimilation because nitrogen is required by plants in greatest quantity.5-10 Nitrate reductase (NR), the first enzyme in the nitrate assimilation pathway,11 has proven to be one of the enzymes to undergoes clear changes in response to elevated CO2.6 However, over the past 15 years, many studies have demonstrated that CO2 enrichment can cause an increase in,12-16 have no effect on,17 or even decrease NR activity in plants.6,13,16,18-20 The conflicting results of the effects of elevated CO2 on NR activity in plants are shown in Table 1. Some studies have shown that elevated CO2 levels stimulated the activity of NR, e.g., in Arabidopsis,13 tobacco,12 and white pine,21 which were treated with 2, 2, and 1.6 mM nitrate, respectively. Conversely, some researchers observed the opposite effect of CO2 enrichment on NR activity, under high nitrate conditions; Geiger et al.6 reported that elevated CO2 slightly stimulated NR activity in the leaves of tobacco plants fed with 2 mM nitrate, while causing an approximately 30% decrease in leaf NR activity in plants fed with a 6 mM nitrate supply. This result is similar to that of Lekshmy et al.,22 in which CO2 enrichment increased NR activity (by 11%–24%) in the leaves of wheat seedlings grown in low nitrate conditions (5 mM). These findings imply that the effect of elevated CO2 on NR activity in plants is dependent on the nitrate levels in
the growth medium; this was confirmed by our latest report: in low-level nitrate supply conditions, NR activity is stimulated by the basal endogenous nitric oxide (NO) and the NO induced by CO2 enrichment, via an NOS-dependent pathway.10 However, in high-level nitrate conditions, NR activity is inhibited by excess NO gathered from high endogenous NO, and NOSdependent NO generated under elevated CO2.10 Therefore, we assumed that an inflection point of nitrate supply may exist for the upregulation or downregulation of NR activity in plants, in relation to elevated CO2 levels. Such an inflection point might vary with species, physiological state, nutritional availability, and other factors that could affect the basal endogenous NO levels and NOS activity in plants. However, some of the data in Table 1 23–25 is inconsistent with this suggested mechanism, e.g., NR activity under enhanced CO2 conditions were increased in the leaves of tobacco, cucumber, and barley plants growing on high nitrate at 12,23 10,24 and 20 mM,25 respectively. These contrasting results may be attributable to differences in plant culturing; the plants in these studies were grown in quartz crystal sand or perlite and vermiculite, and were watered to field capacity with a complete nutrient solution containing nitrate, either once24 or twice each day23 or weekly.25 In other words, although the level of nitrate used was high, the supply regime was intermittent, rather than sustained; therefore, the plants could be considered to have grown in an overall low nitrate supply. In this context, these studies were also consistent with our hypothesis. However, we cannot completely exclude the possibility that elevated CO2 levels increase NR activity in the case of high nitrate (> 10 mM), since the nitrate levels in our study only ranged from 0.2–10 mM.10
CONTACT Shaoting Du [email protected] Addendum to: Du ST, Zhang RR, Zhang P, Liu HJ, Yan MG, Chen N, Xie HQ, Ke SW. Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. Journal of Experimental Botany 2016; 67 (3): 893–904; doi:10.1093/jxb/erv506. © 2016 Taylor & Francis Group, LLC
e1165380-2
R. ZHANG AND S. DU
Table 1. Studies of NR activity changes under different experimental background in response to elevated CO2. Plants
Position
N source
Tobacco (Nicotian atabacum L)
Leaves
NO3¡
White pine (Pinus strobus) Tobacco nd (Nicotian atabacum L) Arabidopsis (Arabidopsis thaliana) Wheat (Triticum aestivum L)
Leaves Leaves Shoots Shoots
NO3¡ NO3¡ NO3¡ NO3¡
Arabidopsis (Arabidopsis thaliana) Leaves
NO3¡
Tobacco (Nicotian atabacum L)
Leaves
NO3¡
Cucumber (Cucumissativus L)
Leaves
NO3¡
Barley (Hordeum vulgare L)
Leaves
NO3¡
Tobacco (Nicotian atabacum L)
Leaves
NH4NO3
Tobacco (Nicotian atabacum L) Loblolly pine (Pinus taeda) Arabidopsis (Arabidopsis thaliana) Barley (Hordeum vulgare L)
Leaves Leaves Shoots Shoots
NH4NO3 NH4NO3 NH4C NH4 NO3
Cultivation methods
Concentration 2 mM 6 mM 1.6 mM 2 mM 2 mM 0.02–2 mM 4–10 mM 4 mM Fertilized twice daily with a nutrient solution containing 12 mM nitrate. Irrigated daily with a nutrient solution containing 10 mM nitrate Watered twice a week with a nutrient solutioncontaining 20 mM nitrate 1 mM 3 mM 10 mM 1 mM 5.6 g N m¡2 year¡1 2 mM 1 mM
Furthermore, under high nitrate and ammonium conditions, elevated CO2 decreased NR activity regardless of the nitrogen supply levels. For example, elevated CO2 led to a significant (30%–50%) inhibition of NR activities in plants grown at 1, 3, and 10 mM NH4NO3 conditions.6 These results are similar to the findings of Matt et al.12 and Wang et al.,20 in which elevated CO2 decreased NR activity in tobacco and barley growing at 1 mM NH4NO3 conditions. These results may be associated with the fact that CO2 enrichment preferentially stimulates ammonium uptake and assimilation, leading to an accumulation of reduced nitrogen and repression of NR.6 All of these findings indicated that the nitrogen source—concentration, availability, and form—might be a decisive factor directly affecting the rate of nitrate assimilation for plants during an increase in atmospheric CO2. This may have profound implications for research on plant responses to elevated CO2. Although elevated CO2 increased the yield of plants grown on high nitrate conditions,6 excessive use of nitrate fertilizer may result in a low efficiency of nitrogen use. Additionally, in the presence of ammonium, nitrate will also be unutilized. Therefore, a relatively low concentration of nitrate fertilizers may improve NR activity, and consequently promote nitrogen assimilation, alleviating nitrogen pollution and economic losses for farmers.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
Funding This work was financially supported by the Zhejiang Province Natural Science Foundation (No. LY14C130001), the Natural Science foundation of China (Grant Nos 30900170).
Seedling Time of CO2 treatment age
Changes in NR level
References
Vermiculite
45 d
45 d
Nutrition solution Nutrition solution Nutrition solution Nutrition solution
105 d 39 d 35 d 20 d
105 d 25 d 7d 20 d
Nutrition solution
35 d
4h
Quartz crystal sand
35 d
11 d
" # " " " " # " # "
Perlite vermiculite
21 d
2h
"
24
Perlite and vermiculite
16 d
16 d
"
25
Vermiculite
45 d
45 d
6
39 d 22 years 35 d 27 d
25 d 7 years 7d 15 d
# # # # # ¡(no change) #
Nutrition solution Acidic soils Nutrition solution Nutrition solution
6 21 12 13 22 10 23
12 19 13 20
References 1. IPCC. Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press; 2014. 2. Long SP, Ainsworth EA, Rogers A, Ort DR. Rising atmospheric carbon dioxide: plants FACE the future. Ann Rev Plant Biol 2004; 55:591-628; PMID:15377233; http://dx.doi.org/10.1146/annurev.arplant.55.031903. 141610 3. Ainsworth EA, Long SP. What have we learned from 15 years of freeair CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 2005; 165:351-72; PMID:15720649; http://dx.doi. org/10.1111/j.1469-8137.2004.01224.x 4. Ainsworth EA. Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentrations. Global Change Biol 2008; 14:1642-50; http://dx.doi.org/ 10.1111/j.1365-2486.2008.01594.x 5. Cheng SH, Moore BD, Seemann JR. Effects of short- and long-term elevated CO2 on the expression of ribulose-1, 5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiol 1998; 116:715-23; PMID:9489018; http://dx.doi.org/10.1104/pp.116.2.715 6. Stitt M, Krapp A. The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 1999; 22:583-621; http://dx.doi.org/10.1046/j.13653040.1999.00386.x 7. Sun JD, Gibson KM, Kiirats O, Okita TW, Edwards GE. Interactions of nitrate and CO2 enrichment on growth, carbohydrates, and rubisco in arabidopsis starch mutants. Significance of starch and hexose. Plant Physiol 2002; 130:1573-83; PMID:12428022; http://dx.doi.org/ 10.1104/pp.010058 8. Li PH, Ainsworth EA, Leakey ADB, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ. Arabidopsis transcript and metabolite profiles: ecotypespecific responses to open-air elevated [CO2]. Plant Cell Environ 2008; 31:1673-87; PMID:18721265; http://dx.doi.org/10.1111/j.13653040.2008.01874.x 9. Sanz-Saez A, Erice G, Aranjuelo I, Nogues S, Irigoyen JJ, Sanchez-Dıaz M. Photosynthetic down-regulation under elevated CO2 exposure can be prevented by nitrogen supply in nodulated alfalfa. J Plant Physiol
PLANT SIGNALING & BEHAVIOR
10.
11.
12.
13.
14.
15.
16.
17.
2010; 167:1558-65; PMID:20708820; http://dx.doi.org/10.1016/j. jplph.2010.06.015 Du ST, Zhang RR, Zhang P, Liu HJ, Yan MG, Chen N, Xie HQ, Ke SW. Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. J Exp Bot 2016; 3:893-904; PMID:20708820; http://dx.doi.org/10.1093/jxb/erv506 Buchanan BB, Gruissem W, Jones RL. Biochemistry and molecular biology of plants. Rockville, MD: American Society of Plant Physiologists 2000; ISBN: 0-943088-39-9 Matt P, Geiger M, Liu PW, Engels C, Krapp A, Stitt M. Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ 2001; 24:1119-37; http://dx. doi.org/10.1046/j.1365-3040.2001.00771.x Niu YF, Cai RS, Dong HF, Wang H, Tang CX, Zhang YS. Effect of elevated CO2 on phosphorus nutrition of phosphate-deficient Arabidopsis thaliana (L.) Heynh under different nitrogen forms. J Exp Bot 2012; 64:355-67; PMID:23183255; http://dx.doi.org/10.1093/jxb/ ers341 Alexandre A, Silva J, Buapet P, Bjork M, Santos R. Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol Evol 2012; 2(10):2625-2635; PMID:23145346; http://dx.doi.org/10.1002/ece3.333 Hofmann LC, Straub S, Bischof K. Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis. J Exp Bot 2013; 64:899-908; PMID:23314813; http://dx.doi.org/10.1093/jxb/ers369 Sailo N, Verma R, Pandey R, Jain V. Effect of elevated carbon dioxide on nitrogen assimilation and mobilization in wheat and rye genotypes of different ploidy levels. Indian J Plant Physiol 2013; 18:333-8; http:// dx.doi.org/10.1007/s40502-013-0049-4 Cousins AB, Bloom AJ. Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photo-assimilation in maize (Zea mays L.). Plant, Cell Environ 2003; 26:1525-30; http://dx.doi.org/ 10.1046/j.1365-3040.2003.01075.x
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