Plant Physiol. (1986) 80, 211-2150032-0889/86/80/0211/05/$0 1.00/0

Relationship between Photosynthesis and Protein Synthesis inMaizeI. KINETICS OF TRANSLOCATION OF THE PHOTOASSIMILATED CARBON FROM THE EAR LEAFTO THE SEED

Received for publication May 6, 1985 and in revised form September 17, 1985

FRANgOIS MOUTOT, JEAN-CLAUDE HUET, JEAN-FRAN(OIS MOROT-GAUDRY, AND JEAN-CLAUDE PERNOLLET*Laboratoire du Metabolisme et de la Nutrition des Plantes (F.M., J-F.M-G.) and Laboratoire d'Etude desProteines (J-C.H., J.-C.P.), Departement de Physiologie et Biochimie Vegetales, Centre LN.R.A, route deSt-Cyr, 78000 Versailles, France

ABSTRACT

To gain a better understanding of the biochemical basis for partitioningof photosynthetically fixed carbon between leaf and grain, a '4C02labeling study was conducted with field-grown maize plants 4 weeks afterflowering. The carbon flow was monitored by separation and identificationof '4C assimilates and '4C storage components within each tissue duringthe chase period (from 4 to 96 hours) following a 5 minute '4CO2 pulse.In the labeled ear leaf, the radioactivity strongly decreased to reach, atthe end of the experiment, about 12% of the total incorporated radioac-tivity, mostly associated with sucrose and proteins. Nevertheless, anunexpected reincorporation of radioactivity was observed either in leafstarch or proteins, the day following the pulse. Conversely, the radioac-tivity in the grain increased to attain 66% of the total incorporated '4Cafter a 96 hour chase. The photosynthates, mostly sucrose, organic andfree amino acids, rapidly translocated towards the developing seeds,served as precursors for the synthesis of seed storage compounds, starch,and proteins. They accumulate in free form for 24 hours before beingincorporated within polymerized storage components. This delay is inter-preted as a necessary prerequisite for interconversions prior to thepolycondensations. In the grain, the labeling of the storage molecules,either in starch or in storage protein groups (salt-soluble proteins, zein,and glutelin subgroups), was independent of their chemical nature butdependent on their pool size.

Maize is known for its high capacity for dry matter productionassociated with a high potential photosynthesis (10). Whereaselementary processes of carbon assimilation (7, 9), sucrose syn-thesis (5), phloem loading and unloading (3, 6, 27) have beenextensively described, little information is available regarding therelationships between leaf and seed during grain filling, exceptthat the developing ear is rapidly supplied with the assimilatesoriginating from the ear leaf (4, 11, 17, 28). Before being used inthe synthesis of grain compounds, photosynthetic intermediates,especially sugars, may be temporarily stored in the stem tissue(4, 26). The effect of sink strength on the partitioning of assimi-lates in source leaves and their subsequent distribution in theplant has been approached by Koch et al. (13). These studies,focused on the export of carbon from the source leaf, do notassess the contribution of current photosynthates to the nutri-tional demand of seed formation. Only Tsai et al (29) have

suggested that seed storage proteins serve as a sink to regulatethe movement of photosynthates into the grain. To gain a betterunderstanding of the biochemical basis for partitioning of pho-tosynthetically fixed carbon between leaf and grain a '4C02labeling kinetic study was carefully conducted with field-grownplants at mid-development stage of the grain (milky stage).Beginning with early translocation steps, carbon flow was fol-lowed by separation and identification of 14C assimilates and 14Cstorage components within the tissues involved in this process,during short and longer chase times (4, 10, 19, 24, 30, 48, 72,and 96 h) following a 5 min 14C02 pulse.

MATERIALS AND METHODS

Plant Material. Zea mays L. var INRA 180 (Brulouis) wasgrown at INRA, Versailles, between May and August 1982. At28 ± 3 d after flowering, 36 plants were labeled with 14C02directly in the field.

'4C02 Labeling. Between 10 AM and 2 PM, the median part(200 cm2, i.e. 2-3 g of dry matter) of the attached ear leaf wassealed into a 600-ml Plexiglas '4C02 feeding chamber connectedto a closed gas circuit. From a controlled "4C02 air mixturereserve, a cylinder was filled by pressure adjustment. The 14C02cylinder was connected to the gas flow circuit at the commence-ment of pulse time. This device permitted a very reproducibledelivery of 1.1 MBq 14C02 for each experiment.The chamber was displayed perpendicular to incident sunlight

(irradiance around 700 to 1200 uE m-2 s-'). The leaf wasmaintained at a mean temperature of 27°C in the chamber untiltotal incorporation of the CO2 (i.e. a 5 min pulse), monitoredwith an ADC IR CO2 analyzer to verify the efficiency andreproducibility of ear leafphotosynthesis. The chamber was thenremoved and the plant left under field conditions until sampling:the chase time varied from 5 min (assumed zero time) to 96 h.

Immediately after harvest, plant tissues were separated andfrozen in liquid N2. Tissue samples were defined as follows:14C02 fed leaf area (L), blade below the fed area and sheath (S),node at the leaf and shank (N), husk (H), cob (C), and grains(G). Chase experiments were done in triplicate and the presentedresults correspond to mean values.

Extraction and Separation of 'T( Labeled Products. The liquid-N2 frozen samples were first lyophilized and weighed beforebeing pulverized in a Cyclotec 1092 sample mill at liquid N2temperature. Their radioactivity was determined with a SL4000Intertechnique liquid scintillation counter following both the useof a thixotropic scintillation mixture and combustion with an

211

Plant Physiol. Vol. 80, 1986

Intertechnique Oxymat IN 4101. For leafand intermediary organsamples, the powders were extracted successively in 95, 80, 60%(v/v) ethanol-water and finally with water. Aliquots of extractswere evaporated and dissolved in 10 N H2SO4 for organic acidanalysis and in HCI N/100 for amino acid analysis. For sugardeterminations, the extracts were separated into basic, acidic,and neutral fractions on cation and anion exchange resins. Theradioactivity ofeach fraction was measured by liquid scintillationto verify all subsequent analyses of "1C labeled compounds. Theremaining insoluble material was first treated by a and ,3 amy-lases at 37°C for 12 h to estimate the radioactivity incorporatedin starch. Then, it was treated with pronase in 20 mM Tris HCI(pH 7.4) at 30°C for 24 h to determine the radioactivity incor-porated into proteins. The protein radioactivity was also meas-ured by summation of the radioactivity of the protein aminoacids determined with a Kontron Liquimat III analyzer equippedwith a continuous flow Berthold LB 504 monitor (18).For the grains, the flours were submitted to a sequential

extraction of proteins (14, 18), after defatting in acetone at -10°Cto obtain the lipid fraction. The salt-soluble extract, obtainedwith a 0.5 M NaCl solution, was separated into salt-solubleproteins by TCA precipitation (10% w/v final concentration)and the supernatant split into free amino acids and sugars plusorganic acids by ion exchange chromatography (BioradAG50WX8). The storage proteins were then separated into zein(soluble in 55% v/v isopropanol), G, (soluble in 55% v/v pro-panol with 0.6% 2-mercaptoethanol), G2 (soluble in borateNaOH, 0.5 M [pH 10] in presence of 0.6% 2-mercaptoethanol)and G3 (soluble in the previous buffer added with 0.5% SDS)glutelins. G2 and G3 fractions were dialyzed against 1% aceticacid and evaporated before hydrolysis. The residue was assumedto be starch. The radioactivity ofsamples was measured by liquidand/or solid scintillation. As for leaf proteins, it was verified bysummation of amino acid radioactivity (18). The nitrogenamounts of all nitrogenous samples were determined by themicro-Kjeldahl method. All the results were corrected on ananalytical yield basis and fitted to a standard initial leaf incor-poration of 100 MBq.

RESULTS

"1C Incorporation and Partitioning in the Plant Organs. At theconsidered stage of plant development, the apparent photosyn-thesis was maximal (30-40 ,umol m-2 s-' of C02) and in agree-ment with previously observed values (1, 10). After "'CO2 incor-poration, about 90% of the "1C was recovered in the ear leafblade, cob, and intermediate organs between the leaf source andgrains. Losses by respiration and translocation into other partsof the plant (unloaded leaves, sheaths, and roots) were negligibleduring the experiment and discrepancies in radioactivity recoverylower than 5%.The kinetics of distribution of radioactivity are reported in

Figure 1. During the chase period, the initial radioactivitystrongly decreased in the "'CO2 fed leaf area. Half of the totalincorporated "1C was exported in 5 h and only 10 to 12%remained after 96 h. Whereas no significant radioactivity wasfound in the distal part of the ear leaf, appreciable "1C amounts(20-25%) were recovered in the intermediate organs and stayedroughly constant during the chase period. Conversely the radio-activity increased rapidly in the grains and reached two-thirds ofthe total incorporated "'C at the end of the experiment.

"1C Distribution in Different Compounds of the AssimilatingEar-leaf. The kinetics of distribution of radioactivity in the maincompounds of the leaf are reported in Table I. After a 5 min14CO2 feeding, the major part of radioactivity (98%) was re-covered in the water-ethanol extracts. The labeling of organic,amino acids, and neutral sugars of the leaf is roughly similar.During the first hours of the chase period, the radioactivity of

the organic and amino acids strongly decreased. The radioactivityof the free amino acids dropped to a negligible value after 10 hof chase, while the radioactivity of the organic acids dropped to1.5% of the total incorporated "'C at time zero, i.e. 8% of theremaining radioactivity in the leaf. Nevertheless the organic acidradioactivity showed two maxima (about 4% ofthe total initiallyincorporated radioactivity, i.e. 25% of the remaining radioactiv-ity in the leaf) at 24 and 48 h of chase. Likewise, the radioactivityof the free sugars decreased quickly during the first 10 h. From10 to 30 h, the radioactivity of the free sugars decreased moreslowly and remained steady during the rest of the experiment.Sucrose represented the most labeled compound (over 70%)among the free sugars (8).The insoluble material was rapidly labeled during the chase.

The radioactivity recovered in starch and proteins just after a 5min pulse accounted for 2% ofthe total incorporated radioactiv-ity (Table I). In the course of the chase, the proportion of 14C ininsoluble fraction varied from 3 to 10% ofthe total initially fixed14C. Its distribution between starch and proteins varied consid-erably as the chase proceeded. After 96 h, almost all the radio-activity of the leaf remained, equally distributed, in sucrose andin proteins with a lesser amount in organic acids.

"'C Distribution in Different Compounds of the IntermediatePlant Organs. The radioactivity ofthe intermediate plant organsaccounted for one-fifth to one-fourth of the total assimilated 14Cand remained nearly constant during the chase period (Fig. 1).In the node and shank (Table II), the soluble sugars were themost labeled components, in which sucrose represented nearly90% of the radioactivity of this compartment. Basic and acidicfractions comprised only 10% ofthe total radioactivity recoveredin node and shank. The radioactivity found in all the freesubstances slightly varied all along the chase, reaching a maxi-mum between 24 and 72 h, and was slowly decreasing at the endof the experiment. The insoluble compounds represented 3% ofthe radioactivity at 24 h of chase, 11% at 48 h, 15% at 72 h, andthen decreased to 10% at the end of the experiment.

"'C Distribution in Different Compounds of the Grain. Thekinetics of distribution of radioactivity in the main compoundsof the grain are shown in Figure 2. During the first 24 h of thechase period, the radioactivity recovered in the free solublecompounds rapidly increased to comprise half of the finallyincorporated radioactivity in the grain. During the rest of theexperiment, the radioactivity of the soluble compounds of thegrain drastically decreased while starch became the major labeledcompound, representing more than two-thirds ofthe grain radio-activity.The radioactivity recovered in proteins and lipids increased

regularly to reach an equal value (10% of the radioactivityrecovered in the grain) at the end ofthe experiment. As illustratedin Figure 3, among seed storage proteins, zein, the major storageprotein was the most quickly labeled compound and accountedfor the most labeled protein. GI, G2, G3 glutelins and salt-solubleproteins were more slowly labeled during the chase period. The14C amount in seed storage compounds appears to be propor-tional to the pool size ofeach compound, as determined throughnitrogen measurements for proteins (results not shown).

DISCUSSION14C losses during the experiment were negligible. They are

attributed to technical difficulties in measuring radioactivity byliquid scintillation and to respiration processes. After 48 h, amajor part of 14C was recovered in grain starch which is consid-ered as an important quenching factor of the ,Bemission of 14C,as we found by comparing radioactive measurements using thix-otropic scintillation mixture to combustion. Maize is also knownto exhibit a very limited carbon loss by respiration throughoutgrowth (I17) when compared with wheat, a C3 plant that respires

212 MOUTOT ET AL.

PHOTOSYNTHETIC SUPPLY OF MAIZE SEED

FIG. 1. Kinetics of partitioning of 14CO2 radioactiv-ity from the ear leaf to the grain. Values (mean of 3samples) have been calculated for a 100 MBq standardintital incorporation in the plant. L(A), 4CO2 fed leafarea; S(A), sheath and proximal leaf moiety; N(E),node and shank; C(O), cob; H(O), husk; G(-), grains.

G

72CHASE (h)

Table I. Kinetics ofPartitioning ofRadioactivity in the Ear LeafFed AreaRadioactivity. expressed in kBq per g of dry matter, has been calculated for a 100 MBq standard 4C02

incorporation and corrected for extraction yields.Chase (h)

Compounds0 4 10 19 24 30 48 72 96

Free amino acids 14150 380 168 185 80 120 55 42 70Organic acids 11050 1300 848 655 1910 1040 1720 598 770Free sugars 17410 15480 6904 5550 4610 2070 2250 1840 1760Phosphorylated com-pounds 7740 690 0 0 0 0 0 0 0

Total of free com-pounds 50350 17850 7920 6390 6600 3230 4025 2480 2600

Starch 600 3490 1820 1615 400 3260 1670 430 260Proteins 550 510 1040 595 950 1100 960 920 1550

Starch + proteins 1150 4000 2860 2210 1350 4360 2630 1350 1810

Total of free + poly-merized com-pounds 51500 21850 10780 8600 7950 7590 6655 3830 4410

40 to 50% of the photoassimilated carbon (16).The translocation from the leafto the intermediate and storage

plant organs of recently assimilated "1C occurred very soon afterthe pulse. Troughton et al. (27) have demonstrated that thephotosynthates moved very rapidly with water by the mass flowin sieve tubes. The resulting osmotically generated pressure mightbe the driving force for movement of substances in the plant.Theblade below the fed area, node, shank, and cob are considered asconduits and as temporary storage reservoirs for carbon skeletonsused thereafter as precursors in the synthesis of starch, proteins,and lipids for the developing grain (2, 4, 17, 26). The accumu-lation of a limited but significant fraction of radioactivity in theinsoluble components of the intermediary organs is in accord-ance with the results showing that photosynthates temporarilyaccumulate in the cell wall of vascular bundles as structuralcarbohydrates and proteins (2, 8). Besides, we confirm here thelarge size of the conduit compartment which retains 20% of the

photoassimilated carbon for at least 4 d.The patterns of "4C distribution between plant organs reveal

that developing ear and specifically grains were major sinks for14C photoassimilated by ear leaf blade, 28 d after silk emergence.Other previous works have shown that the development of grainwas the main process determining the fate of photosyntheticcarbon after flowering in maize (4, 7, 17). Nevertheless we showthat only two-thirds of the photosynthetic carbon is trappedwithin the grain. This is explained not only by the size of theconduits but also by the relatively high amount of radioactivityremaining in the leaf.

14C free sugars (mainly sucrose) are exported rapidly duringthe first 10 h of the chase as previously observed by Hofstra andNelson ( 11) and Prioul and Rocher (20). Exported sucrose pro-vides carbon skeletons and energy for organic synthesis in thedark; this movement persists as long as reserves are available,but after 30 h there is no significant export of 14C sucrose. We

213

Plant Physiol. Vol. 80, 1986

Table II. Kinetics ofPartitioning ofthe Radioactivity in the Node and ShankRadioactivity, expressed in kBq per g of dry matter, has been calculated for a 100 MBq standard 4C02

incorporation.

Chase (h)Compounds

4 10 19 24 30 48 72 96Free amino acids 6.3 17.4 12.1 12.7 11.3 12.9 6.0 3.4Organic acids 32.1 26.0 32.0 35.4 33.8 38.3 62.7 13.2Free sugars 512 538 456 601 588 684 549 476

Total solubles 550 581 500 649 633 735 618 493

Insoluble compounds 11 33 70 19 60 93 112 53

Total recovered ra-dioactivity 561 614 570 668 693 828 730 546

00

4c0

a4C

5_C)4

0

a4rcca

o

o0

C)z

-J

I-.C

0 24 48 72 96CHASE (h)

FIG. 2. Kinetics of "4CO2 radioactivity of the major biochemicalcomponents of the grain. Values have been calculated for a 100 MBqstandard initial incorporation in the plant. (*), Total radioactivity of thegrain; (0), free sugars (and organic acids); (0), starch; (U), proteins; (A),lipids; (E), free amino acids.

show that, in the leaf at the end of the chase, free sugars (mainlysucrose) still represent more than 3% ofthe initially incorporatedradioactivity, i.e. 40% of the remaining radioactivity. They forma storage pool not directly accessible to translocation, in agree-ment with the results of Prioul and Rocher (20) who haveprovided evidence of such a sucrose pool in the leaf vacuoles.The rate of sucrose synthesis and translocation indirectly reg-

ulates the rate of starch formation which is associated with thephotosynthate demand. The partitioning of carbon between su-crose and starch is controlled by fructose 2,6-bisP, phosphatetranslocator, Pi, and triose-P concentrations and an importantdeterminant of carbon partitioning into starch may be the rateof sucrose synthesis and the related generation of Pi into cytosol(12, 19, 21, 24, 25). Transient starch in the leaf is well known tobe a response to a temporary oversupply of carbohydrates fromphotosynthesis. In fact, after a rapid depletion from 4 to 10 h ofchase, we have observed only a slight decrease of the starchradioactivity during the night, the rest of the degradation takingplace early in the morning. Nevertheless this is in agreement withstarch hydrolysis in chloroplast into exportable triose-P by thereactions of the glycolytic sequence (15). It is worth emphasizing

8 ZEIN

2

C) FREE AMINO ACIDS42

O1.58 72 9

SALT sdLUBLE PROTEINS

(A),443glutelins.0z

0 24 48 72 96CHASE (h)

FIG. 3. Kinetics of rC02radioactivity accumulation in the nitroge-nous compounds of the grain. Values have been calculated for a 100MBq standard initial incorporation in the plant. (0), Free amino acids;(J), salt-soluble proteins; (0), zein; (U) GI glutelins; (A), G2 glutelins;(A), G3 glutelins.

that the second labeling of starch occurring after 24 h of chase,resulting from the incorporation of the '4C02released during thefirst night and early in the next mor ing. This original resultsupports the contention that the maize leaf is able to reincorpo-rate secondarym 4C02 issued from general metabolism to synthe-size starch again.

Leaf proteins are also quickly labeled after a briefcaCO2apulse.Their radioactivity increases during the chase to reach nearly 3%of the initially incorporated radioactivity at the end of theexperiment while the labeling of starch dropped to zero. Photo-synthetic carbon is stored temporarily in leaf proteins which arealso considered as the main reservoir of nitrogen for the maizegrain from pollination to maturity (2). As for starch, the radio-activity in leaf proteins obeys a nyctemeal period, characterizedby a depletion during the first night and a secondary increase inthe course ofthe 2nd d. This can only be explained by a relativelyrapid turnover of at least half of the leaf proteins, involvingproteins different from ribulose- l,5-bisP carboxylase, which isknown to have a 7-d half-life (23).Another new observation is that the photoassimilated carbon,

translocated to developing grains, appears temporarily in freemolecules, mainly sucrose, amino and organic acids. These mol-ecules set up a large transient reservoir of precursors used there-

214 MOUTOT ET AL.

PHOTOSYNTHETIC SUPPLY OF MAIZE SEED

after in the synthesis of starch, proteins, and lipids of the grain.This delay may be explained by the well known mechanisms ofunloading and transfer of sucrose from the phloem of interme-diate organs to the endosperm (22), mechanisms involving thepassage through specialized basal endosperm cells prior to move-ment into the starchy endosperm and embryo. The transientstorage of precursors could also be attributed to slow biochemicalconversions of molecules prior to their polymerization into stor-age macromolecules.Although produced since the first hours of chase, the final

storage molecules are more intensively synthesized from theincoming precursors after a 24 h chase. Starch appears as theprincipal carbon sink of the grain, whereas the radioactivityassociated with storage proteins accounts for only 10% of theradioactivity accumulated in the grain. The same level is ob-served in the lipids. In the grain, the labeling of the storagemolecules is independent of their chemical nature but dependenton their pool size.The patterns of 14C distribution reveal that, at mid-develop-

ment stage of the seed, grains are the major, but not the only,sink for the carbon photoassimilated by ear leaf blade. Thephotosynthates, mostly sucrose, organic and amino acids, rapidlytranslocated to the developing seeds, serve as elementary com-ponents for the synthesis of seed storage compounds, starch, andproteins. In the grain, the final storage molecules, either starchor proteins, are not immediately synthesized from the incomingprecursors: a 24 h delay is a necessary prerequisite for theirpolycondensation. On the other hand, about 12% of the pho-toassimilated carbon remained trapped in the assimilation areaof the leaf, mostly in sucrose and proteins.

Reliable information about the translocation processes in-volved in the seed protein synthesis from photosynthates in maizeis presented. Further studies are in progress on the biochemicalinterconversions necessary for the photosynthetic carbon to ac-cumulate in the grain under suitable forms. Only appropriatetechniques of labeling and analysis and a judicious choice of thesampling time in the course of chase after a short "CO2 pulseallow one to properly examine the fate of photoassimilatedcarbon in the source leaf along the translocation path and inassimilation into grain components of maize.

Acknowledgments-We particularly want to thank Dr. J. Mosse for criticalreading of the manuscript and Dr. J. Baudet for helpful advice. We are grateful toM. C. Aubriere, G. Colliere, J. C. Lescure, and S. Wuilleme for their skillfultechnical assistance, and to all colleagues who kindly participated in "CO2 incor-porations.

LITERATURE CITED

1. BETHENOD 0, C JACOB, JC RODE. JF MOROT-GAUDRY 1982 Influence de l'Igesur les caracteistiques photosynthetiques de la feuille de mais, Zea mays L.Agronomie 2: 159-166

2. CRAWFORD TW JR, VV RENDING, FE BROADBENT 1982 Sources, fluxes andsinks of nitrogen during early reproductive growth of maize (Zea mays L.).Plant Physiol 70: 1654-1660

3. EVERT RF, W ESCHRICH, W HEYSER 1978 Leaf structure in relation to solutetransport and phloem loading in Zea mavs L. Planta 138: 279-294

4. FAIREY NA. TB DAYNARD 1978 Assimilate distribution and utilization in

maize. Can J Plant Sci 58: 719-7305. FEKETE MAR, GH VIEWEG 1973 Zur Synthese der Saccharose in Blattern von

Zea mays. Ber Dtsch Bot Ges 86: 227-2316. FRITZ E, RF EVERT, W HEYSER 1983 Microautoradiography studies of phloem

loading and transport in the leaf of Zea mays L. Planta 159: 193-2067. GALMICHE JM 1973 Studies on the mechanism of glycerate 3-phosphate

synthesis in tomato and maize leaves. Plant Physiol 51: 512-5198. GIAQUINTA RT 1980 Translocation ofsucrose and oligosaccharides. In J Preiss,

ed, The Biochemistry of Plant, Vol 3. Academic Press, New York, pp 271-320

9. HATCH MD 1971 The C4-pathway of photosynthesis. Evidence for an inter-mediate pool ofcarbon dioxide and the identity ofthe donor C4 dicarboxylicacid. Biochem J 125: 425-432

10. HESKETH JD, DN Moss 1963 Variation in the response of photosynthesis tolight. Crop Sci 3: 107-1 10

11. HOFSTRA G, CD NELSON 1969 The translocation of photosynthetically assim-ilated 14C in corn. Can J Bot 47: 1435-1442

12. HUBER SC, DN ISRAEL 1982 Biochemical basis for partitioning of photosyn-thetically fixed carbon between starch and sucrose in soybean (Glvcine maxMerr.) leaves. Plant Physiol 69: 691-696

13. KOCH KE, CL Tsui, LE SCHRADER, OE NELSON 1982 Source-sink relations inmaize mutants with starch-deficient endosperms. Plant Physiol 70: 322-325

14. LANDRY J, T MOUREAUX 1976 Quantitative estimation of accumulation ofprotein fractions in unripe and ripe maize grain. Qual Plant 25: 343-360

15. LATZKO E, M STEUP, C SCHACHTELE 1981 Starch biosynthesis and degradationin photosynthetic tissues. In G Akoyunoglou, ed, Photosynthesis IV Regu-lation of Carbon Metabolism. Balaban Intern Sci Serv, Philadelphia, pp5 17-528

16. MORGAN CL, RB AUSTIN 1983 Respiratory loss of recently assimilated carbonin wheat. Ann Bot 51: 85-95

17. PALMER AFE, GH HEICHEL, RB MUSGRAVE 1973 Patterns of translocation,respiratory loss, and redistribution of "C in maize labeled after flowering.Crop Sci 13: 371-376

18. PERNOLLET JC, JC HuET, F MOUTOT, JF MORoT-GAUDRY 1986 Relationshipbetween photosynthesis and protein synthesis in maize: II. Interconversionsofthe photoassimilated carbon in the ear leafand in the intermediary organsto synthesize the seed storage proteins and starch. Plant Physiol 80: 216-222

19. PREISS J 1984 Starch, sucrose biosynthesis and partition of carbon in plantsare regulated by orthophosphate and triose-phosphates. Trends Biochem Sci9: 24-27

20. PRIOUL JL, JP ROCHER 1984 Les transports d'assimilats chez le mais: meca-nisme, r6le des facteurs externes, application a des comparaisons intergeno-types. In A Gallais, ed, Physiologie du Mais. INRA, Paris, pp 303-330

21. RuFrY WT, SC HUBER 1983 Changes in starch formation and activities ofsucrose phosphate synthase and cytoplasmic fructose 2,6-bisphosphate inresponse to source-sink alterations. Plant Physiol 72: 474-480

22. SHANNON JC 1972 Movement of "C-labeled assimilates into kernels of Zeamays L. 1. Pattern and rate of sugar movement. Plant Physiol 49: 198-202

23. SIMPSON E, RJ COOKE, DD DAVIES 1981 Measurement of protein degradationin leaves of Zea mays using [3H]acetic anhydride and tritiated water. PlantPhysiol 67: 1214-1219

24. STIrr M, B HERZOG, HW HELDT 1984 Control of photosynthetic sucrosesynthesis by fructose 2,6-bisphosphate. I. Coordination of CO2 fixation andsucrose synthesis. Plant Physiol 75: 548-553

25. STITT M, B KURZEL, HW HELDT 1984 Control of photosynthetic sucrosesynthesis by fructose 2,6-bisphosphate. II. Partitioning between sucrose andstarch. Plant Physiol 75: 554-560

26. SWANK JC, FE BELOW, RJ LAMBERT, RH HAGEMAN 1982 Interaction ofcarbon and nitrogen metabolism in the productivity of maize. Plant Physiol70: 1185-1190

27. THROUGHTON JH, BG CURRIE, FH CHANG 1977 Relations between light level,sucrose concentration, and translocation of carbon 11 in Zea mays leaves.Plant Physiol 59: 808-820

28. TRIPATHY PC, JA EASTIN, LE SCHRADER 1972 A comparison of "C-labeledphotosynthate export from two leafpositions in a corn (Zea mays L.) canopy.Crop Sci 12: 495-497

29. TSAI CY, DM HUBER, HL WARREN 1980 A proposed role of zein and glutelinas N sinks in maize. Plant Physiol 66: 330-333

215