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Home , C3 carbon fixation, Photorespiration

RevIeW ARTICLe t As rises, food quality will decline without careful nitrogen management

by Arnold J. Bloom

Rising atmospheric concentrations of carbon dioxide could dramatically infl uence the performance of crops, but experimental results to date have been highly variable. For example, when C3 plants are grown under car- bon dioxide enrichment, productivity increases dramatically at fi rst. But over time, organic nitrogen in the plants decreases and productivity diminishes in soils where is an important source of this nutrient. We have discovered a phenomenon that provides a relatively simple explana- tion for the latter responses: in C3 plants, elevated carbon dioxide con- centrations inhibit , which in turn inhibits shoot nitrate assimilation. Agriculture would ben- efi t from the careful management of nitrogen , particularly those that are ammonium based. The rise in atmospheric carbon-dioxide levels — about 35% since 1800 — changes how plants metabolize important nutrients, which in turn alters food quality and , infl uences where plants and crops can grow, and affects pest management and other tmospheric carbon dioxide (CO2) cultivation practices. Lesley Randall of the UC Davis Department of Plant Sciences attends has increased about 35% since to plants growing in hydroponic culture under elevated carbon-dioxide atmospheres, in A1800 (from 280 to 380 parts per million environmental chambers at the UC Davis Controlled Environment Facility. [ppm]), and computer models predict that it will reach between 530 and 970 Atmospheric Denitrification nitrogen (N ) 193 ppm by the end of the century (IPCC Nylon Nitrous oxide 2 production (N O) 2007). This rise in carbon dioxide could 2 Biological Shoot fixation potentially be mitigated by crop plants, assimilation Biological in which converts at- Volatili- Atmospheric fixation zation fixation mospheric carbon dioxide into carbohy- 228 100 5 Nitrous oxide drates and other organic compounds. (N2O) (NH ) The extent of this mitigation remains 3 Industrial Root Free-living Nitric oxide uncertain, however, due to the complex fixation absorption N fixers Plant & (NO) 100 Soil 2 relationship between carbon and nitro- 1,200 animal wastes microbes Symbiotic (NO –) gen in plants (Finzi et al. N2 fixers 2 2007; Johnson 2006; Reich et al. 2006). Decaying organic matter Nitrate Carbon metabolism provides the Immobilization Ammonification Nitrification (NO –) Leaching 3 36 energy and carbon to syn- Ammonium (NH +) 4 Groundwater thesize organic nitrogen compounds #s = teragrams N/year in plants, whereas nitrogen metabo- lism provides the amino groups for Fig. 1. Major processes of the biogeochemical nitrogen cycle. Fluxes (red numbers) are in teragrams (Tg = 1012 g) N/year. Terrestrial organisms and soils contain organic nitrogen that all (fi g. 1). Proteins include all is active in the cycle. Assuming that the amount of atmospheric molecular nitrogen remains that catalyze (facilitate) bio- constant (inputs = outputs), the mean residence time of nitrogen in organic forms is about 370 chemical reactions in plants, including years. Source: Bloom 2009.

http://CaliforniaAgriculture.ucop.edu • April–June 2009 67 At elevated carbon dioxide concentrations, C3 plants that rely on nitrate as a nitrogen source carbon metabolism. Any environmental suffer severe deprivation of organic nitrogen. perturbation that interferes with nitro- gen metabolism sooner or later inhibits carbon metabolism. Carbon dioxide acclimation

C Photorespiration The focal point of crop responses 3 to rising carbon dioxide levels is the ATP (ribulose-1,5-bisphos- ATP NADPH CO O phate carboxylase/). Rubisco RuBP 2 2 CO : Inger Andersson Inger Molecule: RuBP 2 is the most prevalent on Earth and contains as much as half of the nitrogen in plant leaves. It catalyzes two different chemical reactions: one reaction combines a 5-carbon sugar PGA RuBP (ribulose-1,5-bisphosphate) with carbon dioxide, and the other reaction

CH2O CO2 combines this same sugar with . Rubisco The reaction of RuBP with carbon dioxide produces a 6-carbon com- 2 PGA PG + PGA ATP ATP pound that immediately divides into NADPH NADPH two molecules of a 3-carbon compound (3-phosphoglycerate), hence the name Fig. 2. C3 carbon fi xation and photorespiration pathways in which the enzyme rubisco (ribbon C3 carbon fi xation (fi g. 2). These prod- model in center) catalyzes reactions between a 5-carbon sugar, RuBP (ribulose-1,5-biphosphate) ucts pass through an elaborate bio- and either CO2 or O2. The fi rst stable products of C3 carbon fi xation are two molecules of PGA (a 3-carbon compound, 3-phosphoglycerate); the fi rst stable products of photorespiration are chemical cycle (Calvin-Benson cycle) one molecule of PGA and one molecule of PG (a 2-carbon compound, 2-phosphoglycolate). that eventually forms one molecule High-energy compounds ATP and NADPH, generated from photosynthesis, drive these of a 6-carbon sugar (fructose-6-phos- reactions. As atmospheric CO2 increases, there is an initial increase in C3 carbon fi xation phate) and regenerates RuBP. (and sugar productivity), while photorespiration is inhibited. We have shown that inhibiting photorespiration diminishes nitrate assimilation. In plants that depend on nitrate as a nitrogen The reaction of RuBP with oxygen source, this eventually inhibits plant productivity and lowers protein content. Nitrogen is part oxidizes the RuBP, splits it into one mol- of the amino groups essential to all proteins, and proteins include the enzymes that facilitate ecule of a 3-carbon compound (3-phos- biochemical reactions. Source: Bloom 2009. phoglycerate) and one molecule of a

50 100 Phoenix, sour orange Crop yield (28) Chesapeake Bay, Scirpus Duke, Pinus /sec)

2 365 ppm CO Oak Ridge, Liquidambar 40 2 Tree biomass (19) 80 Swiss, mixed deciduous 567 ppm CO2 Jasper Ridge, grassland Grass biomass (13) 30 60 enrichment (%)

2 Plant biomass (18) 20 High N 40 Grass nitrogen (13) Low N assimilation (µmol/m assimilation 2 10 –40 0 40 80 20 Change with CO2 enrichment (%) Net CO Net 0 0 200 400 600 800 C (ppm) 0 Fig. 5. Differences in yield, aboveground i biomass, leaf nitrogen (N) concentrations Biomass change with CO and grain protein concentrations between Fig. 3. Net carbon dioxide assimilation –20 C3 plants grown at elevated (567 ppm) (photosynthesis) as a function of carbon 0 2 4 6 8 10 12 and ambient (366 ppm) carbon dioxide dioxide concentrations within a leaf (C i) Year of treatment concentrations under heavy (high N) and for C3 plants grown at either ambient normal N fertilization (low N). Symbols and (365 parts per million [ppm]) or elevated Fig. 4. Each line shows change in biomass over error bars designate means ± 95% confi dence (567 ppm) atmospheric carbon dioxide time for specifi c plants grown at elevated (567 interval for crops (Ainsworth and Long 2005), concentrations, in free air CO2 enrichment ppm) and ambient (365 ppm) carbon dioxide trees (Curtis and Wang 1998), grasses (Wand (FACe) plots, where plants growing in soil atmospheres, in free air CO2 enrichment et al. 1999), all plant species (de Graaff et al. under the open sky are exposed to elevated (FACe) plots (Dukes et al. 2005; Korner 2006) 2006) and grain protein (Taub et al. 2008). carbon dioxide. Mean of 285 studies and open-top chambers (Rasse et al. 2005; Parentheses contain number of studies (Ainsworth and Rogers 2007). Kimball et al. 2007). included in the meta-analysis.

68 CAliFOrniA AGriCulTure • VOLUME 63, NUMBER 2 2-carbon compound (2-phosphoglyco- late), and subsequently releases carbon dioxide, hence the names C2 pathway or, more commonly, photorespiration. In total, photorespiration consumes bio- chemical energy, but does not result in any net production of sugar (Foyer et al. 2009). Thus, photorespiration has been viewed as a wasteful process, a vestige of the high carbon dioxide atmospheres (over 1,000 ppm) under which plants evolved (Wingler et al. 2000). The balance between C3 carbon fixa- tion and photorespiration depends on the relative amounts of carbon dioxide and oxygen entering the active site of rubisco (i.e., portion of the enzyme involved in the primary chemical reac- tions) and the affinity of the enzyme for each gas (i.e., degree to which it attracts carbon dioxide or oxygen). At current Wheat was grown in a controlled environmental chamber at elevated carbon dioxide (700 atmospheric levels of carbon dioxide + ppm). Plants in the three containers on the left received ammonium (NH4 ) as the sole – and oxygen (about 380 and 209,700 nitrogen source, whereas those on the right received nitrate (NO3 ). Plants grown at ambient ppm, respectively), photorespiration in carbon dioxide under ammonium and nitrate nutrition were indistinguishable (not shown). most crops (C3 plants including wheat, rice, barley, oats, legumes, vegetables, Together these trends are known as nitrogen increases because of the high and fruit and nut trees) dissipates carbon dioxide acclimation. carbon-to-nitrogen ratios in the litter, over a quarter of the organic carbon (3) soil nitrogen availability to plants CO acclimation hypotheses produced during carbon dioxide as- 2 further diminishes because more soil similation (conversion from inorganic to Several hypotheses have been put nitrogen is tied up in microorganisms, organic form) (Sharkey 1988). forward to explain carbon dioxide ac- (4) plants become even more nitrogen In contrast, C4 crops (such as corn, climation. limited, (5) plant protein levels decline and sugar cane), which have Carbohydrate sink limitation. Ac- a metabolic carbon dioxide pump that cording to this hypothesis, plants under increases the concentration of this com- carbon dioxide enrichment initially as- 40 pound at the catalytic site of rubisco, similate more carbon dioxide into carbo- minimize photorespiration at the ex- hydrates than they can incorporate into 20 pense of the additional energy required their growing tissues. In response, they enrichment (%) for pumping. diminish carbon dioxide assimilation by 2 0 Elevated levels of atmospheric car- decreasing their rubisco levels (Long et bon dioxide inhibit photorespiration in al. 2004). This change in rubisco levels, Herbs –20 Trees C3 plants, making photosynthesis more however, is not necessarily selective; the Shrubs efficient. Initially, this accelerates both decrease may instead just be part of the their photosynthetic carbon dioxide overall decline in protein and nitrogen –40 assimilation and their growth by about concentrations (Ainsworth and Long Change in PS with CO –40 –20 0 20 40 a third. After a few days or weeks, 2005; Makino and Mae 1999). Change in N with CO2 enrichment (%) however, carbon dioxide assimilation Progressive nitrogen limitation. An- Fig. 6. Differences in leaf carbon fixation and growth both slow down until they other hypothesis for carbon dioxide capacity (photosynthesis [PS]) versus total are accelerated in the long term by acclimation is that shoots accumulate nitrogen concentration (N) between C3 plants only about 12% and 8%, respectively carbohydrates faster than roots can grown at elevated (567 ppm) and ambient (366 ppm) carbon dioxide concentrations. (figs. 3 and 4). Moreover, leaf nitrogen absorb nitrogen from soils, making Each symbol designates the mean ratio for and protein concentrations ultimately leaf nitrogen concentrations decrease a species. Shown are the regression line decrease more than 12% under carbon (Hungate et al. 2003; Luo et al. 2004; (solid, slope = 0.815, r = 0.71) and 1:1 line dioxide enrichment (fig. 5). Such a loss Norby et al. 2001; Reich et al. 2006). As (dotted). This data suggests that changes in photosynthesis from carbon dioxide of nitrogen and protein significantly these leaves senesce and drop to the enrichment derive from changes in plant diminishes the value of this plant ma- ground, (1) plant litter quality declines, nitrogen levels under carbon dioxide terial as food for animals and humans. (2) microbial immobilization of soil enrichment (Ellsworth et al. 2004).

http://CaliforniaAgriculture.ucop.edu • April–June 2009 69 and (6) plant processes including pho- partially compensate for this, the plants’ solved nitrate into deep groundwater tosynthesis slow down (fig. 6). This nitrogen and protein concentrations still or surface water). For example, the hypothesis, however, has difficulty in diminish (fig. 5). dominant C3 plant in the Chesapeake explaining the variation in carbon di- Ammonium and nitrate are the two Bay marsh (Scirpus olneyi) showed oxide acclimation among sites (Finzi et main sources of nitrogen that are ac- little carbon dioxide acclimation (fig. al. 2007) and among methods of carbon cessible to plants from the soil. Plants 4); even after a decade of treatment, dioxide enrichment (Ainsworth and show a wide range of responses to photosynthesis and growth remained Long 2005). carbon dioxide enrichment because the about 35% greater under carbon diox- balance between nitrate and ammo- ide enrichment (Rasse et al. 2005), with Role of photorespiration nium availability varies over seasons, little change in nitrogen concentrations We have discovered another explana- years, locations and plant species. In (Erickson et al. 2007). In wheat, an- tion for carbon dioxide acclimation: in C3 an annual California grassland where other C3 plant, elevated carbon dioxide plants, shoot assimilation of nitrate into nitrate was the predominant nitro- atmospheres stimulated less growth organic nitrogen compounds depends gen source, net primary productivity under nitrate than under ammonium on photorespiration, so any condition diminished under carbon dioxide nutrition (fig. 9; see photo, page 69). that inhibits photorespiration (elevated enrichment (fig. 4) (Dukes et al. 2005). Physiological mechanisms carbon dioxide or low oxygen concentra- This was presumably because elevated tions) also inhibits shoot nitrate assimi- carbon dioxide inhibited plant nitrate Several physiological mechanisms lation (figs. 7 and 8). Thus, at elevated assimilation (by both shoots and roots), appear to be responsible for the depen- carbon dioxide concentrations, C3 plants and the grasses became deprived of dency of nitrate assimilation on photo- that rely on nitrate as a nitrogen source organic nitrogen. In contrast, ammo- respiration. suffer severe deprivation of organic nium is the major form of nitrogen First, the initial biochemical step of nitrogen compounds such as proteins. available to plants in marshes because nitrate assimilation is the conversion The resulting decline in organic nitrogen wet, anaerobic soils promote denitri- of nitrate to nitrite in leaves. This step compounds reduces the plants’ yield fication (the conversion of nitrate into is powered by the high-energy com- and biomass production. While high nitrous oxide and dinitrogen gas) and pound NADH (reduced nicotinamide applications of nitrogen may nitrate leaching (the removal of dis- adenine dinucleotide), and photorespi-

0.3 0.6 A (Arabidopsis) B (wheat)

0.2 a 360 ppm CO and 21% O w C plants 2 2 3 720 ppm CO and 21% O a 2 2 C4 plants 0.4 360 ppm CO2 and 2% O2 0.1 b s s s x

0.0 Relative nitrate assimilation m x 0.2

0 200 400 600 800 1,000 mn n Ci (ppm) Rate (µmol nitrate /plant gram/min.) Rate – Fig. 7. Response of nitrate (NO3 ) assimilation in C3 and C4 plants as a function of carbon dioxide concentrations inside a leaf (C ). 0.0 – i Relative NO3 assimilation was assessed from Uptake Assimilation Uptake Assimilation changes in CO2-O fluxes with a shift from – 2 NH + to NO nutrition (∆AQ). The C species 4 3 3 – – included barley (Bloom et al. 1989), wheat Fig. 8. Nitrate (NO3 ) uptake as the amount of NO3 depleted from a medium, and nitrate (Bloom et al. 2002), tomato (Searles and Bloom assimilation as the difference between the rates of net NO – uptake and net accumulation – 3 2003), Arabidopsis (Rachmilevitch et al. 2004) of free NO3 in plant tissues: (A) 36-day-old Arabidopsis or (B) 10-day-old wheat were and Flaveria pringlei and giant redwood exposed to 360 ppm carbon dioxide (CO2) and 21% O2 , 720 ppm carbon dioxide and (Bloom, unpublished data). The C4 species 21% O2 , or 360 ppm CO2 and 2% O2. Shown are the mean ± SE (n = 13–16). Treatments included (Cousins and Bloom 2003, labeled with different letters differ significantly (P ≤ 0.05). Light levels were 500 and 1,000 2004) and Flaveria bidentis and Amaranthus micromoles of quanta per meter squared per second for Arabidopsis and wheat, respectively retroflexus (Bloom, unpublished data). (Rachmilevitch et al. 2004).

70 CALIFORNIA AGRICULTURE • VOLUME 63, NUMBER 2 Environmental chambers in the UC Davis Controlled Environment Twelve wheat seedlings were subject to atmospheres containing various Facility are helping scientists to understand how plants react to concentrations of carbon dioxide and oxygen. The bubbles are a thin changes in atmospheric carbon, oxygen and other greenhouse gases. water layer that lines the top of the chamber to control its temperature. ration increases the availability of this independent of carbon dioxide concen- carbon dioxide and standard fertilizer compound (Backhausen et al. 1998; trations in C4 plants (fig. 7). levels, wheat had 10% less grain pro- Igamberdiev et al. 2001). In contrast, Second, the subsequent biochemical tein (Fangmeier et al. 1999; Kimball et C4 plants generate ample amounts of step of nitrate assimilation is the con- al. 2001). Similarly, grain protein in rice NADH in leaves via a different bio- version of nitrite to ammonium in the (Terao et al. 2005) and tuber nitrogen in chemical pathway. This explains why of leaf cells, which requires potato (Fangmeier et al. 2002) declined shoot nitrate assimilation is relatively the transport of nitrite into the chloro- by about 10% at elevated carbon diox- plast. Elevated carbon dioxide inhibits ide concentrations. Wheat this transport (Bloom et al. 2002). Several approaches could mitigate + NH4 and 360 ppm CO2 Third, this subsequent step also these declines in food quality under + NH4 and 700 ppm CO2 – requires chemical energy from the carbon dioxide enrichment. Increased NO3 and 360 ppm CO2 – oxidation of a different high-energy yields may compensate to some de- NO3 and 700 ppm CO2 compound called ferredoxin. Several gree for total protein harvested (fig. 0.3 60 b b other processes — in particular, carbon 5). Several-fold increases in nitrogen d dioxide assimilation — depend on the fertilization could eliminate declines same energy source and seem to have in food quality (Kimball et al. 2001), c c priority in using it. Ferredoxin becomes but such fertilization rates would not 0.2 40 ) a 2 involved in nitrate assimilation only be economically or environmentally a b a d when carbon dioxide availability limits feasible given the anticipated higher b C3 photosynthesis (Backhausen et al. fertilizer prices and stricter regula- c c Biomass (g) 0.1 20 2000; Peirson and Elliott 1988). tions on nitrate leaching and nitrous a Leaf area (cm a a oxide emissions. Greater reliance on Carbon dioxide and food quality ammonium fertilizers and inhibitors Many crops in California depend of nitrification (microbial conversion of 0.0 0 on nitrate as their primary nitrogen ammonium to nitrate) might counteract Shoot Stem Root Leaf area source. As atmospheric carbon diox- food quality decreases. Nevertheless, ide concentrations rise and nitrate the widespread adoption of such Fig. 9. Biomass (grams dry mass) and leaf area (cm2) per plant of wheat seedlings assimilation diminishes, these crops practices would require sophisticated grown for 14 days in controlled environment will be depleted of organic nitrogen, management to avoid ammonium chambers at 360 or 700 ppm carbon dioxide including protein, and food quality toxicity, which occurs when plants ab- + – and under NH4 or NO3 nutrition. Shown will suffer (Taub et al. 2008). Wheat, sorb more of this compound than they are mean ± SE for four replicate experiments, each with 8 to 10 plants per treatment. Treat- rice and potato provide 21%, 14% and can assimilate into amino acids and ments labeled with different letters differ 2%, respectively, of protein in the hu- free ammonium then accumulates in significantly (P < 0.05) (Bloom et al. 2002). man diet (FAOSTAT 2007). At elevated their tissues (Epstein and Bloom 2005).

http://CaliforniaAgriculture.ucop.edu • April–June 2009 71 Several of these issues might be simul- tions and food production. Enriched a better understanding of ammonium taneously addressed by fertigation, or carbon dioxide atmospheres will not and nitrate use by crops and careful ni- frequent additions of small amounts of enhance the performance of C3 plants trogen management, we can turn these ammonium-based fertilizers in water to the extent originally envisioned. A phenomena to our advantage. delivered through microirrigation. 10% decline in food protein content These findings have broad implica- will further burden regions of the A.J. Bloom is Professor, Department of Plant tions for the future of plant distribu- world already affected by hunger. With Sciences, UC Davis.

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