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1 UC Agriulture & Nturl Resoures Cliforni Agriulture Title As ron dioxide rises, food qulity will deline without reful nitrogen mngement Permlink Journl Cliforni Agriulture, 63(2 ISSN Author Bloom, Arnold J Pulition Dte Peer reviewed esholrship.org Powered y the Cliforni Digitl Lirry University of Cliforni
2 RevIeW ARTICLe t As ron dioxide rises, food qulity will deline without reful nitrogen mngement y Arnold J. Bloom Rising tmospheri onentrtions of ron dioxide ould drmtilly influene the performne of rops, ut experimentl results to dte hve een highly vrile. For exmple, when C 3 plnts re grown under ron dioxide enrihment, produtivity inreses drmtilly t first. But over time, orgni nitrogen in the plnts dereses nd produtivity diminishes in soils where nitrte is n importnt soure of this nutrient. We hve disovered phenomenon tht provides reltively simple explntion for the ltter responses: in C 3 plnts, elevted ron dioxide onentrtions inhiit photorespirtion, whih in turn inhiits shoot nitrte ssimiltion. Agriulture would enefit from the reful mngement of nitrogen fertilizers, prtiulrly those tht re mmonium sed. Atmospheri ron dioxide (CO 2 hs inresed out 35% sine 18 (from 28 to 38 prts per million [ppm], nd omputer models predit tht it will reh etween 53 nd 97 ppm y the end of the entury (IPCC 7. This rise in ron dioxide ould potentilly e mitigted y rop plnts, in whih photosynthesis onverts tmospheri ron dioxide into rohydrtes nd other orgni ompounds. The extent of this mitigtion remins unertin, however, due to the omplex reltionship etween ron nd nitrogen metolism in plnts (Finzi et l. 7; Johnson 6; Reih et l. 6. Cron metolism provides the energy nd ron moleules to synthesize orgni nitrogen ompounds in plnts, wheres nitrogen metolism provides the mino groups for ll proteins (fig. 1. Proteins inlude ll enzymes tht tlyze (filitte iohemil retions in plnts, inluding The rise in tmospheri ron-dioxide levels out 35% sine 18 hnges how plnts metolize importnt nutrients, whih in turn lters food qulity nd nutrition, influenes where plnts nd rops n grow, nd ffets pest mngement nd other ultivtion prties. Lesley Rndll of the UC Dvis Deprtment of Plnt Sienes ttends to plnts growing in hydroponi ulture under elevted ron-dioxide tmospheres, in environmentl hmers t the UC Dvis Controlled Environment Fility. Industril fixtion 1 Nylon prodution #s = tergrms N/yer Soil miroes Nitrous oxide (N 2 O Shoot ssimiltion Immoiliztion Voltiliztion 1 Ammoni (NH 3 Root sorption 1, Atmospheri nitrogen (N 2 Biologil fixtion Free-living N Plnt & 2 fixers niml wstes Symioti N 2 fixers Deying orgni mtter Ammonifition Nitrifition Ammonium (NH 4+ Biologil fixtion 228 Denitrifition 193 Atmospheri fixtion 5 Nitrous oxide (N 2 O Nitri oxide (NO Nitrte (NO 3 Nitrite (NO 2 Lehing 36 Groundwter Fig. 1. Mjor proesses of the iogeohemil nitrogen yle. Fluxes (red numers re in tergrms (Tg = 1 12 g N/yer. Terrestril orgnisms nd soils ontin orgni nitrogen tht is tive in the yle. Assuming tht the mount of tmospheri moleulr nitrogen remins onstnt (inputs = outputs, the men residene time of nitrogen in orgni forms is out 37 yers. Soure: Bloom 9. AprilJune 9 67
3 Moleule: Inger Andersson CH 2 O At elevted ron dioxide onentrtions, C 3 plnts tht rely on nitrte s nitrogen soure suffer severe deprivtion of orgni nitrogen. C 3 ron fixtion NADPH RuBP 2 PGA CO 2 O 2 Ruiso Photorespirtion RuBP PG + PGA NADPH CO 2 PGA NADPH Fig. 2. C 3 ron fixtion nd photorespirtion pthwys in whih the enzyme ruiso (rion model in enter tlyzes retions etween 5-ron sugr, RuBP (riulose-1,5-iphosphte nd either CO 2 or O 2. The first stle produts of C 3 ron fixtion re two moleules of PGA ( 3-ron ompound, 3-phosphoglyerte; the first stle produts of photorespirtion re one moleule of PGA nd one moleule of PG ( 2-ron ompound, 2-phosphoglyolte. High-energy ompounds nd NADPH, generted from photosynthesis, drive these retions. As tmospheri CO 2 inreses, there is n initil inrese in C 3 ron fixtion (nd sugr produtivity, while photorespirtion is inhiited. We hve shown tht inhiiting photorespirtion diminishes nitrte ssimiltion. In plnts tht depend on nitrte s nitrogen soure, this eventully inhiits plnt produtivity nd lowers protein ontent. Nitrogen is prt of the mino groups essentil to ll proteins, nd proteins inlude the enzymes tht filitte iohemil retions. Soure: Bloom 9. CO 2 ron metolism. Any environmentl perturtion tht interferes with nitrogen metolism sooner or lter inhiits ron metolism. Cron dioxide limtion The fol point of rop responses to rising ron dioxide levels is the enzyme ruiso (riulose-1,5-isphosphte roxylse/oxygense. Ruiso is the most prevlent protein on Erth nd ontins s muh s hlf of the nitrogen in plnt leves. It tlyzes two different hemil retions: one retion omines 5-ron sugr RuBP (riulose-1,5-isphosphte with ron dioxide, nd the other retion omines this sme sugr with oxygen. The retion of RuBP with ron dioxide produes 6-ron ompound tht immeditely divides into two moleules of 3-ron ompound (3-phosphoglyerte, hene the nme C 3 ron fixtion (fig. 2. These produts pss through n elorte iohemil yle (Clvin-Benson yle tht eventully forms one moleule of 6-ron sugr (frutose-6-phosphte nd regenertes RuBP. The retion of RuBP with oxygen oxidizes the RuBP, splits it into one moleule of 3-ron ompound (3-phosphoglyerte nd one moleule of Net CO 2 ssimiltion (µmol/m 2 /se ppm CO ppm CO C i (ppm Fig. 3. Net ron dioxide ssimiltion (photosynthesis s funtion of ron dioxide onentrtions within lef (C i for C 3 plnts grown t either mient (365 prts per million [ppm] or elevted (567 ppm tmospheri ron dioxide onentrtions, in free ir CO 2 enrihment (FACe plots, where plnts growing in soil under the open sky re exposed to elevted ron dioxide. Men of 285 studies (Ainsworth nd Rogers 7. Biomss hnge with CO 2 enrihment (% Phoenix, sour ornge Chespeke By, Sirpus Duke, Pinus Ok Ridge, Liquidmr Swiss, mixed deiduous Jsper Ridge, grsslnd Yer of tretment Fig. 4. Eh line shows hnge in iomss over time for speifi plnts grown t elevted (567 ppm nd mient (365 ppm ron dioxide tmospheres, in free ir CO 2 enrihment (FACe plots (Dukes et l. 5; Korner 6 nd open-top hmers (Rsse et l. 5; Kimll et l. 7. Crop yield (28 Tree iomss (19 Grss iomss (13 Plnt iomss (18 Grss nitrogen (13 High N Low N 8 Chnge with CO 2 enrihment (% Fig. 5. Differenes in yield, oveground iomss, lef nitrogen (N onentrtions nd grin protein onentrtions etween C 3 plnts grown t elevted (567 ppm nd mient (366 ppm ron dioxide onentrtions under hevy (high N nd norml N fertiliztion (low N. Symols nd error rs designte mens ± 95% onfidene intervl for rops (Ainsworth nd Long 5, trees (Curtis nd Wng 1998, grsses (Wnd et l. 1999, ll plnt speies (de Grff et l. 6 nd grin protein (Tu et l. 8. Prentheses ontin numer of studies inluded in the met-nlysis. 68 CAliFOrniA AGriCulTure VOLUME 63, NUMBER 2
4 2-ron ompound (2-phosphoglyolte, nd susequently releses ron dioxide, hene the nmes C 2 pthwy or, more ommonly, photorespirtion. In totl, photorespirtion onsumes iohemil energy, ut does not result in ny net prodution of sugr (Foyer et l. 9. Thus, photorespirtion hs een viewed s wsteful proess, vestige of the high ron dioxide tmospheres (over 1, ppm under whih plnts evolved (Wingler et l.. The lne etween C 3 ron fixtion nd photorespirtion depends on the reltive mounts of ron dioxide nd oxygen entering the tive site of ruiso (i.e., portion of the enzyme involved in the primry hemil retions nd the ffinity of the enzyme for eh gs (i.e., degree to whih it ttrts ron dioxide or oxygen. At urrent tmospheri levels of ron dioxide nd oxygen (out 38 nd 9,7 ppm, respetively, photorespirtion in most rops (C 3 plnts inluding whet, rie, rley, ots, legumes, vegetles, nd fruit nd nut trees dissiptes over qurter of the orgni ron produed during ron dioxide ssimiltion (onversion from inorgni to orgni form (Shrkey In ontrst, C 4 rops (suh s orn, sorghum nd sugr ne, whih hve metoli ron dioxide pump tht inreses the onentrtion of this ompound t the tlyti site of ruiso, minimize photorespirtion t the expense of the dditionl energy required for pumping. Elevted levels of tmospheri ron dioxide inhiit photorespirtion in C 3 plnts, mking photosynthesis more effiient. Initilly, this elertes oth their photosyntheti ron dioxide ssimiltion nd their growth y out third. After few dys or weeks, however, ron dioxide ssimiltion nd growth oth slow down until they re elerted in the long term y only out 12% nd 8%, respetively (figs. 3 nd 4. Moreover, lef nitrogen nd protein onentrtions ultimtely derese more thn 12% under ron dioxide enrihment (fig. 5. Suh loss of nitrogen nd protein signifintly diminishes the vlue of this plnt mteril s food for nimls nd humns. Whet ws grown in ontrolled environmentl hmer t elevted ron dioxide (7 ppm. Plnts in the three ontiners on the left reeived mmonium (NH 4 + s the sole nitrogen soure, wheres those on the right reeived nitrte (NO 3. Plnts grown t mient ron dioxide under mmonium nd nitrte nutrition were indistinguishle (not shown. Together these trends re known s ron dioxide limtion. CO 2 limtion hypotheses Severl hypotheses hve een put forwrd to explin ron dioxide limtion. Crohydrte sink limittion. Aording to this hypothesis, plnts under ron dioxide enrihment initilly ssimilte more ron dioxide into rohydrtes thn they n inorporte into their growing tissues. In response, they diminish ron dioxide ssimiltion y deresing their ruiso levels (Long et l. 4. This hnge in ruiso levels, however, is not neessrily seletive; the derese my insted just e prt of the overll deline in protein nd nitrogen onentrtions (Ainsworth nd Long 5; Mkino nd Me Progressive nitrogen limittion. Another hypothesis for ron dioxide limtion is tht shoots umulte rohydrtes fster thn roots n sor nitrogen from soils, mking lef nitrogen onentrtions derese (Hungte et l. 3; Luo et l. 4; Nory et l. 1; Reih et l. 6. As these leves senese nd drop to the ground, (1 plnt litter qulity delines, (2 miroil immoiliztion of soil nitrogen inreses euse of the high ron-to-nitrogen rtios in the litter, (3 soil nitrogen vilility to plnts further diminishes euse more soil nitrogen is tied up in miroorgnisms, (4 plnts eome even more nitrogen limited, (5 plnt protein levels deline Chnge in PS with CO 2 enrihment (% Hers Trees Shrus Chnge in N with CO 2 enrihment (% Fig. 6. Differenes in lef ron fixtion pity (photosynthesis [PS] versus totl nitrogen onentrtion (N etween C 3 plnts grown t elevted (567 ppm nd mient (366 ppm ron dioxide onentrtions. Eh symol designtes the men rtio for speies. Shown re the regression line (solid, slope =.815, r =.71 nd 1:1 line (dotted. This dt suggests tht hnges in photosynthesis from ron dioxide enrihment derive from hnges in plnt nitrogen levels under ron dioxide enrihment (Ellsworth et l AprilJune 9 69
5 nd (6 plnt proesses inluding photosynthesis slow down (fig. 6. This hypothesis, however, hs diffiulty in explining the vrition in ron dioxide limtion mong sites (Finzi et l. 7 nd mong methods of ron dioxide enrihment (Ainsworth nd Long 5. Role of photorespirtion We hve disovered nother explntion for ron dioxide limtion: in C 3 plnts, shoot ssimiltion of nitrte into orgni nitrogen ompounds depends on photorespirtion, so ny ondition tht inhiits photorespirtion (elevted ron dioxide or low oxygen onentrtions lso inhiits shoot nitrte ssimiltion (figs. 7 nd 8. Thus, t elevted ron dioxide onentrtions, C 3 plnts tht rely on nitrte s nitrogen soure suffer severe deprivtion of orgni nitrogen ompounds suh s proteins. The resulting deline in orgni nitrogen ompounds redues the plnts yield nd iomss prodution. While high pplitions of nitrogen fertilizer my prtilly ompenste for this, the plnts nitrogen nd protein onentrtions still diminish (fig. 5. Ammonium nd nitrte re the two min soures of nitrogen tht re essile to plnts from the soil. Plnts show wide rnge of responses to ron dioxide enrihment euse the lne etween nitrte nd mmonium vilility vries over sesons, yers, lotions nd plnt speies. In n nnul Cliforni grsslnd where nitrte ws the predominnt nitrogen soure, net primry produtivity diminished under ron dioxide enrihment (fig. 4 (Dukes et l. 5. This ws presumly euse elevted ron dioxide inhiited plnt nitrte ssimiltion (y oth shoots nd roots, nd the grsses eme deprived of orgni nitrogen. In ontrst, mmonium is the mjor form of nitrogen ville to plnts in mrshes euse wet, neroi soils promote denitrifition (the onversion of nitrte into nitrous oxide nd dinitrogen gs nd nitrte lehing (the removl of dis- solved nitrte into deep groundwter or surfe wter. For exmple, the dominnt C 3 plnt in the Chespeke By mrsh (Sirpus olneyi showed little ron dioxide limtion (fig. 4; even fter dede of tretment, photosynthesis nd growth remined out 35% greter under ron dioxide enrihment (Rsse et l. 5, with little hnge in nitrogen onentrtions (Erikson et l. 7. In whet, nother C 3 plnt, elevted ron dioxide tmospheres stimulted less growth under nitrte thn under mmonium nutrition (fig. 9; see photo, pge 69. Physiologil mehnisms Severl physiologil mehnisms pper to e responsile for the dependeny of nitrte ssimiltion on photorespirtion. First, the initil iohemil step of nitrte ssimiltion is the onversion of nitrte to nitrite in leves. This step is powered y the high-energy ompound NADH (redued niotinmide denine dinuleotide, nd photorespi-.3.6 A (Aridopsis B (whet Reltive nitrte ssimiltion.2.1. C 3 plnts C 4 plnts 6 8 1, C i (ppm Fig. 7. Response of nitrte (NO 3 ssimiltion in C 3 nd C 4 plnts s funtion of ron dioxide onentrtions inside lef (C i. Reltive NO 3 ssimiltion ws ssessed from hnges in CO 2 -O 2 fluxes with shift from NH 4 + to NO 3 nutrition ( AQ. The C 3 speies inluded rley (Bloom et l. 1989, whet (Bloom et l. 2, tomto (Serles nd Bloom 3, Aridopsis (Rhmilevith et l. 4 nd Flveri pringlei nd gint redwood (Bloom, unpulished dt. The C 4 speies inluded mize (Cousins nd Bloom 3, 4 nd Flveri identis nd Amrnthus retroflexus (Bloom, unpulished dt. Rte (µmol nitrte /plnt grm/min Uptke m n mn Assimiltion 36 ppm CO 2 nd 21% O 2 7 ppm CO 2 nd 21% O 2 36 ppm CO 2 nd 2% O 2 s s Uptke s w x x Assimiltion Fig. 8. Nitrte (NO 3 uptke s the mount of NO 3 depleted from medium, nd nitrte ssimiltion s the differene etween the rtes of net NO 3 uptke nd net umultion of free NO 3 in plnt tissues: (A 36-dy-old Aridopsis or (B 1-dy-old whet were exposed to 36 ppm ron dioxide (CO 2 nd 21% O 2, 7 ppm ron dioxide nd 21% O 2, or 36 ppm CO 2 nd 2% O 2. Shown re the men ± SE (n = Tretments leled with different letters differ signifintly (P.5. Light levels were 5 nd 1, miromoles of qunt per meter squred per seond for Aridopsis nd whet, respetively (Rhmilevith et l CALIFORNIA AGRICULTURE VOLUME 63, NUMBER 2
6 Environmentl hmers in the UC Dvis Controlled Environment Fility re helping sientists to understnd how plnts ret to hnges in tmospheri ron, oxygen nd other greenhouse gses. Twelve whet seedlings were sujet to tmospheres ontining vrious onentrtions of ron dioxide nd oxygen. The ules re thin wter lyer tht lines the top of the hmer to ontrol its temperture. rtion inreses the vilility of this ompound (Bkhusen et l. 1998; Igmerdiev et l. 1. In ontrst, C 4 plnts generte mple mounts of NADH in leves vi different iohemil pthwy. This explins why shoot nitrte ssimiltion is reltively Biomss (g Whet + NH 4 nd 36 ppm CO 2 + NH 4 nd 7 ppm CO 2 NO 3 nd 36 ppm CO 2 NO 3 nd 7 ppm CO 2 Shoot Stem Root Lef re d d 6 Lef re (m 2 Fig. 9. Biomss (grms dry mss nd lef re (m 2 per plnt of whet seedlings grown for 14 dys in ontrolled environment hmers t 36 or 7 ppm ron dioxide nd under NH 4 + or NO 3 nutrition. Shown re men ± SE for four replite experiments, eh with 8 to 1 plnts per tretment. Tretments leled with different letters differ signifintly (P <.5 (Bloom et l. 2. independent of ron dioxide onentrtions in C 4 plnts (fig. 7. Seond, the susequent iohemil step of nitrte ssimiltion is the onversion of nitrite to mmonium in the hloroplsts of lef ells, whih requires the trnsport of nitrite into the hloroplst. Elevted ron dioxide inhiits this trnsport (Bloom et l. 2. Third, this susequent step lso requires hemil energy from the oxidtion of different high-energy ompound lled ferredoxin. Severl other proesses in prtiulr, ron dioxide ssimiltion depend on the sme energy soure nd seem to hve priority in using it. Ferredoxin eomes involved in nitrte ssimiltion only when ron dioxide vilility limits C 3 photosynthesis (Bkhusen et l. ; Peirson nd Elliott Cron dioxide nd food qulity Mny rops in Cliforni depend on nitrte s their primry nitrogen soure. As tmospheri ron dioxide onentrtions rise nd nitrte ssimiltion diminishes, these rops will e depleted of orgni nitrogen, inluding protein, nd food qulity will suffer (Tu et l. 8. Whet, rie nd potto provide 21%, 14% nd 2%, respetively, of protein in the humn diet (FAOSTAT 7. At elevted ron dioxide nd stndrd fertilizer levels, whet hd 1% less grin protein (Fngmeier et l. 1999; Kimll et l. 1. Similrly, grin protein in rie (Tero et l. 5 nd tuer nitrogen in potto (Fngmeier et l. 2 delined y out 1% t elevted ron dioxide onentrtions. Severl pprohes ould mitigte these delines in food qulity under ron dioxide enrihment. Inresed yields my ompenste to some degree for totl protein hrvested (fig. 5. Severl-fold inreses in nitrogen fertiliztion ould eliminte delines in food qulity (Kimll et l. 1, ut suh fertiliztion rtes would not e eonomilly or environmentlly fesile given the ntiipted higher fertilizer pries nd striter regultions on nitrte lehing nd nitrous oxide emissions. Greter reline on mmonium fertilizers nd inhiitors of nitrifition (miroil onversion of mmonium to nitrte might ountert food qulity dereses. Nevertheless, the widespred doption of suh prties would require sophistited mngement to void mmonium toxiity, whih ours when plnts sor more of this ompound thn they n ssimilte into mino ids nd free mmonium then umultes in their tissues (Epstein nd Bloom 5. AprilJune 9 71
7 Severl of these issues might e simultneously ddressed y fertigtion, or frequent dditions of smll mounts of mmonium-sed fertilizers in wter delivered through miroirrigtion. These findings hve rod implitions for the future of plnt distriutions nd food prodution. Enrihed ron dioxide tmospheres will not enhne the performne of C 3 plnts to the extent originlly envisioned. A 1% deline in food protein ontent will further urden regions of the world lredy ffeted y hunger. With etter understnding of mmonium nd nitrte use y rops nd reful nitrogen mngement, we n turn these phenomen to our dvntge. A.J. Bloom is Professor, Deprtment of Plnt Sienes, UC Dvis. Referenes Ainsworth EA, Long SP. 5. Wht hve we lerned from 15 yers of free-ir CO 2 enrihment (FACE? A met-nlyti review of the responses of photosynthesis, nopy. New Phytolog 165: Ainsworth EA, Rogers A. 7. The response of photosynthesis nd stomtl ondutne to rising [CO 2 ]: Mehnisms nd environmentl intertions. Plnt Cell Env 3:2587. Bkhusen JE, Emmerlih A, Holtgrefe S, et l Trnsgeni potto plnts with ltered expression levels of hloroplst NADP-mlte dehydrogense: Intertions etween photosyntheti eletron trnsport nd mlte metolism in leves nd in isolted intt hloroplsts. Plnt 7:1514. Bkhusen JE, Kitzmnn C, Horton P, et l.. Eletron eptors in isolted intt spinh hloroplsts t hierrhilly to prevent over-redution nd ompetition for eletrons. Photosynth Res 64:113. Bloom AJ. 9. Glol Climte Chnge: A Convergene of Disiplines. Sunderlnd, MA: Sinuer Asso. In press. Bloom AJ, Cldwell RM, Finzzo J, et l Oxygen nd ron dioxide fluxes from rley shoots depend on nitrte ssimiltion. Plnt Physiol 91:3526. Bloom AJ, Smrt DR, Nguyen DT, Serles PS. 2. Nitrogen ssimiltion nd growth of whet under elevted ron dioxide. PNAS 99:1735. Cousins AB, Bloom AJ. 3. Influene of elevted CO 2 nd nitrogen nutrition on photosynthesis nd nitrte photossimiltion in mize (Ze mys L.. Plnt Cell Env 26: Cousins AB, Bloom AJ. 4. Oxygen onsumption during lef nitrte ssimiltion in C 3 nd C 4 plnt: The role of mitohondril respirtion. Plnt Cell Env 27: Curtis PS, Wng XZ A met-nlysis of elevted CO 2 effets on woody plnt mss, form nd physiology. Oeologi 113: De Grff MA, vn Groenigen KJ, Six J, et l. 6. Intertions etween plnt growth nd soil nutrient yling under elevted CO 2 : A met-nlysis. Glol Chnge Biol 12:7791. Dukes JS, Chiriello NR, Clelnd EE, et l. 5. Responses of grsslnd prodution to single nd multiple glol environmentl hnges. PLoS Biol 3: Ellsworth DS, Reih PB, Numurg ES, et l. 4. Photosynthesis, roxyltion nd lef nitrogen responses of 16 speies to elevted pco 2 ross four free-ir CO 2 enrihment experiments in forest, grsslnd nd desert. Glol Chnge Biol 1: Epstein E, Bloom AJ. 5. Minerl Nutrition of Plnts: Priniples nd Perspetives, 2nd Edition. Sunderlnd, MA: Sinuer Asso. 415 p. Erikson JE, Megonigl JP, Perest G, Drke BG. 7. Slinity nd se level medite elevted CO 2 effets on C 3 -C 4 plnt intertions nd tissue nitrogen in Chespeke By tidl wetlnd. Glo Chnge Biol 13:25. Fngmeier A, De Temmermn L, Blk C, et l. 2. Effets of elevted CO 2 nd/or ozone on nutrient onentrtions nd nutrient uptke of pottoes. Eur J Agron 17: Fngmeier A, De Temmermn L, Mortensen L, et l Effets on nutrients nd on grin qulity in spring whet rops grown under elevted CO 2 onentrtions nd stress onditions in the Europen, multiple-site experiment ESPACE-whet. Eur J Agron 1: Finzi AC, Nory RJ, Clfpietr C, et l. 7. Inreses in nitrogen uptke rther thn nitrogen-use effiieny support higher rtes of temperte forest produtivity under elevted CO 2. PNAS 14:1149. [FAOSTAT] Food nd Agriulture Orgniztion Sttistis. 7. Agriulturl Dt. Food nd Agriulturl Orgniztion of the United Ntions. Foyer CH, Bloom AJ, Quevl G, Notor G. 9. Photorespirtory metolism: Genes, mutnts, energetis nd redox signling. Annu Rev Plnt Biol 6. In press. Hungte BA, Dukes JS, Shw MR, et l. 3. Nitrogen nd limte hnge. Siene 32: Igmerdiev AU, Bykov NV, Le PJ, Grdestrom P. 1. The role of photorespirtion in redox nd energy lne of photosyntheti plnt ells: A study with rley mutnt defiient in glyine deroxylse. Physiologi Plntrum 111: [IPCC] Intergovernmentl Pnel on Climte Chnge. 7. Climte Chnge 7: The Physil Siene Bsis. Contriution of Working Group I to the Fourth Assessment Report of the IPCC. Solomon S, Qin D, Mnning M, et l. (eds.. Cmridge, UK, nd New York, NY: Cmr Univ Pr. 996 p. Johnson DW. 6. Progressive N limittion in forests: Review nd implitions for long-term responses to elevted CO 2. Eology 87:6475. Kimll BA, Idso SB, Johnson S, Rillig MC. 7. Seventeen yers of ron dioxide enrihment of sour ornge trees: Finl results. Glo Chnge Biol 13: Kimll BA, Morris CF, Pinter PJ, et l. 1. Elevted CO 2, drought nd soil nitrogen effets on whet grin qulity. New Phytol 15: Korner C. 6. Plnt CO 2 responses: An issue of definition, time nd resoure supply. New Phytol 172: Long SP, Ainsworth EA, Rogers A, Ort DR. 4. Rising tmospheri ron dioxide: Plnts fe the future. Ann Rev Plnt Biol 55: Luo Y, Su B, Currie WS, et l. 4. Progressive nitrogen limittion of eosystem responses to rising tmospheri ron dioxide. Biosiene 54:7319. Mkino A, Me T Photosynthesis nd plnt growth t elevted levels of CO 2. Plnt Cell Physiol : Nory RJ, Cotrufo MF, Ineson P, et l. 1. Elevted CO 2, litter hemistry nd deomposition: A synthesis. Oeologi 127: Peirson DR, Elliott JR Effet of nitrite nd ironte on nitrite utiliztion in lef tissue of ush en (Phseolus vulgris. J Plnt Physiol 133:4259. Rhmilevith S, Cousins AB, Bloom AJ. 4. Nitrte ssimiltion in plnt shoots depends on photorespirtion. PNAS 11: Rsse DP, Perest G, Drke BG. 5. Seventeen yers of elevted CO 2 exposure in Chespeke By wetlnd: Sustined ut ontrsting responses of plnt growth nd CO 2 uptke. Glo Chnge Biol 11: Reih PB, Hungte, BA, Luo YQ. 6. Cronnitrogen intertions in terrestril eosystems in response to rising tmospheri ron dioxide. Ann Rev Eol Evolu Syst 37: Serles PS, Bloom AJ. 3. Nitrte photossimiltion in tomto leves under short-term exposure to elevted ron dioxide nd low oxygen. Plnt Cell Env 26: Shrkey TD Estimting the rte of photorespirtion in leves. Physiologi Plntrum 73: Tu DR, Miller B, Allen H. 8. Effets of elevted CO 2 on the protein onentrtion of food rops: A met-nlysis. Glo Chnge Biol. doi:1.1111/ j x. Tero TS, Miur T, Yngihr T, et l. 5. Influene of free-ir CO 2 enrihment (FACE on the eting qulity of rie. J Si Food Ag 85: Wnd SJE, Midgley GF, Jones MH, Curtis PS Responses of wild C 4 nd C 3 grss (Poee speies to elevted tmospheri CO 2 onentrtion: A metnlyti test of urrent theories nd pereptions. Glol Chnge Biol 5: Wingler A, Le PJ, Quik WP, Leegood RC.. Photorespirtion: Metoli pthwys nd their role in stress protetion. Philosophil Trnstions of the Royl Soiety of London Series B-Biologil Sienes 355: CALIFORNIA AGRICULTURE VOLUME 63, NUMBER 2
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