Plant Physiol. (1983) 73, 630-6350032-0889/83/73/0630/06/$00.50/0

Effects of SO2 and O3 on Allocation of '4C-LabeledPhotosynthate in Phaseolus vulgaris'

Received for publication November 8, 1982 and in revised form June 20, 1983

SAMUEL B. MCLAUGHLIN AND RONALD K. MCCONATHYEnvironmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37830

ABSTRACT

A series of laboratory exposures of two varieties of bush bean (Phas-eolus vulgaris L, var 274 and var 290) was conducted to determine thesensitivity of ['4Cjphotosynthate allocation patterns to alteration by S02and 03. Experiments with the pollution-resistant 274 variety demon-strated short-term changes in both 14C and biomass allocation to roots of'4CO2labeled plants but no significant effect on yield by up to 40 hoursof exposure to SO2 at 0.50 microliters per liter or 4 hours of 03 at 0.40microliters per liter. Subsequent experiments with the more sensitive 290variety demonstrated significant alteration of photosynthesis, transloca-tion, and partitioning of photosynthate between plant parts includingdeveloping pods. Significant increases in foliar retention of photosynthate(+40%) occurred after 8 hours of exposure to SO2 at 0.75 microlitersper liter (6.0 microliters per liter-hour) and 11 hours of exposure to 03at 0.30 microliters per liter-hour (3.3 microliters-hours). Time seriessampling of labeled tissues after '4C02 uptake showed that the disruptionof translocation patterns was persistent for at least I week after exposuresceased. Subsequent longer-term exposures at lower concentrations ofboth 03 (0.0, 0.10, 0.15, and 0.20 microliters per liter) and SO2 (0.0,0.20, and 0.40 microliters per liter) demonstrated that 03 more effectivelyaltered allocation than SO2, that primary leaves were generally moresensitive than trifoliates, and that responses of trifoliate leaves variedwith plant growth stage. Altered rates of allocation of photosynthate byleaves were generally associated with alterations of similar magnitudeand opposite direction in developing pods. Collectively, these experimentssuggest that allocation patterns can provide sensitive indices of incipientgrowth responses of pollution-stressed vegetation.

There is good evidence that air pollutants may exert significantimpacts on plant productivity by altering the partitioning of drymatter between plant parts (10, 19, 24, 25). In addition to alteredpartitioning of carbohydrates between plant parts, the costs ofrepair from air pollution as well as disease-related stress mayreduce carbohydrates available for growth by increasing the costsof repair ofdamage to cellular or metabolic systems (11). Studieswith several plant species have indicated that the internal costsof maintaining leaf functions are high (11). These maintenancecosts would be expected to be enhanced by exposure to pollutantsand associated metabolic or cytologic injury.

Several recent studies under both laboratory (8, 18, 22, 24)and field (14, 15) conditions have indicated that the processes ofcarbohydrate translocation may be both susceptible to exposureto air pollutants and useful as general indicators of pollution-related stress.

In general, translocation has been reduced by exposure to airpollutants, however, with very low SO2 concentrations (0.08 ,ulI-') Milchunas et al. (15) found translocation to have beenstimulated. In studies by Noyes (8) in the laboratory and Mc-Laughlin et al. (14) in the field, altered translocation of ['4C]photosynthate occurred in the absence of significant changes inphotosynthesis.The research reported here was undertaken to examine a

number of critical questions regarding the air pollution effectson 14C allocation patterns in plants. Among these were: (a) Whatwere the relative effects of SO2 and 03 on allocation? (b) Whatrelationship did differential sensitivity to yield effects have todifferential responses of plants to disruption of allocation pat-terns? (c) What relationship did altered patterns of retention of14C-labeled carbohydrates by foliage bear to altered levels ofincorporation of these products into other plant parts?

Physiological research aimed at defining the physiological basisfor plant responses to air pollutants has generally focused oneither (a) defining mechanisms of response to pollution-inducedstress, or (b) developing indicators of pollutant effects on plantgrowth and yield. Most efforts to date have focused on photosyn-thetic or respiratory exchange of C02, while little emphasis hasbeen directed toward other potentially useful indices of carbonmetabolism such as transport and metabolism of photosynthate.The importance of balanced consideration of the energetic costsof maintenance metabolism and the processes of translocationand biosynthesis as well as photosynthesis were stressed by Evans(2) as critical to understanding plant growth processes.

' Research sponsored jointly by the United States EnvironmentalProtection Agency under interagency agreement EPA 82-D-X0533 andby the Office of Health and Environmental Research, United StatesDepartment of Energy under contact W-7405-eng-26 with Union Car-bide Corporation. Publication No. 2205, Environmental Sciences Divi-sion, Oak Ridge National Laboratory.

MATERIALS AND METHODS

A series of individual experiments with the same generalprotocol was performed during the course of this study. Seedswere planted in the greenhouse in 10- to 15-cm pots in acommercially available potting soil (Promix), thinned to one perpot after emergence, and watered as needed. Greenhouse airtemperatures were 25 ± 6°C and the air supply was filtered byactivated charcoal to remove pollutants. The general protocolfor evaluating plant responses involved exposure of groups offour to twelve greenhouse-grown bush beans (Phaseolus vulgarisvar 274 or 290) to SO2 or 03 in a set of eight continuously stirredexposure chambers described previously by McLaughlin andTaylor (13). These exposures, which varied in duration from 3to 40 h were distributed over total time intervals of from 1 d to4 weeks. Pollutant exposures were followed by short-term (2min) treatment of plants with 30 ,uCi of "4C02 in an internallystirred, Teflon-coated greenhouse chamber. Activity in eachtagged plant was determined immediately after tagging and atvarious subsequent times by removing a total of ten 8-mm discs

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EFFECTS OF SO2 AND 03 ON ['4C]PHOTOSYNTHATE ALLOCATION

from fully expanded leaves distributed over the entire plant.Where comparative photosynthetic measurements were needed,single plants from each treatment were labeled simultaneouslyand relative comparisons of incorporated '4CO2 were made.These discs were immediately frozen in liquid N2 as were otherplant parts collected subsequently at whole plant harvest. Dupli-cate leaf disc samples were collected for determination ofthe dryweight:fresh weight ratio and dry weight per unit of leaf surfacearea (one side only). Tagged samples were analyzed for '4Cactivity using a Packard model 306 Tri-Carb sample oxidizer tooxidize approximately 1 g of oven-dried, pelletized tissues. Re-leased '4CO2 was automatically trapped and dissolved in scintil-lation cocktail and counted in a Packard Tri-Carb 460C auto-matic liquid scintillation counting system. Activity per unit leafarea determined immediately after tagging was multiplied byestimating total leaf area to determine total plant activity. Thelength x width product of all trifoliate center leaflets was re-gressed against total plant leaf area at various harvest times to

develop a surface area regression based on easily measured leafdimensions. This regression allowed a nondestructive estimationof total plant area whenever required. Activity budgets andallocation trends were determined by comparing the amountand distribution of 14C activity in plant parts with total activityinitially incorporated into foliage.The identity and details of four experiments utilizing two

varieties of P. vulgaris and varying levels and exposure times to03 and SO2 are shown in Table I. Statistical analyses of differ-ences between treated and control plants was by a Dunnett's(one-tailed) test (20) unless otherwise indicated.

RESULTS

Chronic Exposures to S02-Variety 274. Exposure of var 274to SO2 at 0.0, 0.1, 0.3, and 0.5 l-' SO2 for 20 to 40 h producedno consistent effects on either retention of photosynthate infoliage one day after labeling or in whole-plant weight at harvest.After I d, leaves tagged with 14C retained from 25 to 33 per cent

Table I. Experimental Conditions and Design for Four Studies on the Effects ofAir Pollution Stress onPhotosynthate Allocation

Experiment

Design I II III IV

Plant Material Variety 274 - two weeks

old, one fully expanded

trifol iate

Pollutant

Concentrations

So2 - 0, 0.10, 0.30,

and 0.50 l/l

Variety 290 - five weeks

old, flowering

So2 - 0 and 0.75 l/l

03 - 0 and 0.30 ul/l

Variety 290 - two weeks Variety 290 - seven

old with trifoliate

emerging

So2 - 0, 0.20, and

0.40 1/l;

03 - 0, 0.10, and

0.20 l/l

weeks old, flowers

and pods (< 10 cm)

03 - 0, 0.10, and

0.15 il/l

2 plants x 2 replicates x

2 exposure durations x

4 S02 concentrations

Group 1 - 5 h/d for

2 d/wk, 2 weeks;

Group 2 - sane for

4 weeks

Plants labelled with

14CO after 20 h

(Group 1) or 40 h

(Group 2) of exposure

4 plants per treatnent

x duration harvested

1 week after 14C and

remaining 4 at maturity

(8 weeks old)

3 plants x 2 replicates x

4 exposure durations x

4 concentrations

2-3 h/d for 1,2,3 or 4 d.

Total duration 9 h for

SO2 and 11 h for 03

6 plants per treatment

removed and labelled

with 14C02 after each

day

Plants harvested 7 d

after exposure

3 plants x 2 replicates x 3 plants per treatment

6 concentrations

Initial for one week,

subsequent begins one

week after end of first.

2 h/d for 3 d for So2,

3 h/d for 4 d for 03

6 plants per treatment

labelled with 14coafter each exposure

week

Plants harvested at

maturity 5 weeks after

first exposure, 3 weeks

after second exposure

for 0 and 0.15 PI/I,

6 plants for 0.10 l/l

13 h total over 4 d,

3-4 h/d

All plants labelled

with 14C0C after2fourth day

Plants harvested 7 d

after 03 exposure

Treatment

Design

Exposure

Duration

Exposure

Sequence

Sampl i ng

Protocol

631

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McLAUGHLIN AND McCONATHY Plant Physiol. Vol. 73, 1983

(LSD)

(7.0)

'-5kLEASWTLEAVES A

PODS

ROOTS

PLANT

* 0

* 0

(4 0)°

.- .- a _- _-o- - O

_-° ~ ~~~~ --o _ .... + (3.6)..... ---O(.+.

+I , ,"0 (2.8)

(2.7)0 * *

(1.4)

I I I A-0 0.1 0.3 0.5

B 0". (LSD)

'-O (13.5)

A

'1%"I. .-- .- e.| ...--

0

0

0 0.1 0.3

(8.9)

(6.7)(7.5)

(4.4)

(2.4)

0.5

SO2 EXPOSURE (ML L-1)

FIG. 1. Allocation of ["'C]photosynthate and biomass of P. vulgaris (cv 274) at 1 week (A) and at maturity (B-2 weeks after A) following 4weeks (40 h) of exposure to S02. (*, Significantly different from corresponding control value at -95 per cent confidence.)

28

24

20

16

ORNL-DWG 83-12347

.S02

0 03

0~

..m CONTROL

1 2 3 4

EXPOSURE DAYS

FIG. 2. Effects of 2 h/d S02 (0.75 1 1-') or 03 (0.30 11') on foliarretention of ['4C]photosynthate by P. vulgaris (cv 290) after 1, 2, 3, and4 d of exposure. (*, Significantly different from corresponding controlvalue at >95 per cent confidence.)

of the 14C activity initially assimilated regardless of duration ofSO2 treatment. While total plant biomass was not consistentlyaffected by SO2 exposure, there was evidence of SO2-inducedalteration of distribution of photosynthate between plant parts,particularly after 4 weeks of exposure as shown in Figure 1. Themost consistent response noted was a reduction both in allocationof ['4C]photosynthate to roots and root biomass with increasingSO2 concentration. A comparison of plants treated with 0.50 ,ul

Il' SO2 with controls showed a 47% reduction in 14C activityallocated to roots and a 37% reduction in root biomass for plantsharvested 1 week after exposure. The same comparison made atharvest of mature plants showed 43% reduction of activity anda 25% reduction in biomass of roots. Retention of 14C in leavesexhibited a bimodal response pattern with lowest retention of14C at lower SO2 concentrations and increasing retention at 0.50l 1-' S02.None of the remaining trends were significant at the 95%

confidence level in this experiment, but two responses were ofbiological interest: (a) highest plant biomass (20% above controls)occurred in the highest SO2 treatment, and (b) decreased trans-location of 14C from leaves (Fig. 1B) for mature plants chronicallyexposed to SO2 was accompanied by reduced translocation of14C to both roots and pods and reduced biomass of these tissues.

Sequential Exposure to S02 or 03. The subsequent experi-ments focused on the more pollution-sensitive 290 variety ofP. vulgaris. Results of the initial experiment to define a

dose:response threshold for SO2 and 03 are shown in Figure 2.Foliar retention of initial ["4C]photosynthate following I to 4 dofexposure to SO2 (0.75 ,l 1-') or 03(0.30 I-1') was significantlyincreased by exposure to both pollutants. A Duncan's NewMultiple Range Test (20) of differences between exposed andcontrol plants on each successive day showed a statisticallysignificant (0.05 level) increase (40%) for SO2-treated plants overcontrols after only 2 d of exposure. A maximum increase of73%over controls occurred at day 4. Day 1 foliar retention of 14C by03-treated plants, on the other hand, did not increase signifi-cantly until after 4 d (1 1 h) of exposure to 03.

Chronic Exposure to SO2 and 03-Variety 290. Subsequentexperiments with the 290 variety were calculated to provide a

weekly exposure dose (concentration x time) below that required

632

A

_

ORNL-DWG 82-18379

4030

.

* 25

I-w

cc

,_ 20

15

-

: 10

U-0

I-.IW 5

0

I-

I-

zC:j

1-J

I-.

~-.

Co

30 -a

CDw

20 CAI-20L.

F-wL.)w

10

0

a

a

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EFFECTS OF S02 AND 03 ON ['4C]PHOTOSYNTHATE ALLOCATION

ORNL-DWG 83-12346

250

200

-i

150

100

50 L

03 0

SO2 0

PRIMARY LEAVES

S°2 9 EXPOSURE H

03 11 EXPOSURE H

0

0*

03~~~ ~SO2I~~~~~~~~~~~~~~I0-l S02

----0~~

10

20

100

90

80

8 70

C-

C--

C=./C)

0

&4

20

40

EXPOSURE CONCENTRATION (UL L-)

FIG. 3. Effects of SO2 and 03 on photosynthesis and photosynthateallocation by P. vulgaris (cv 290). See Table II for corresponding indicesof allocation to other tissues. (*, Significantly different from correspond-ing control value at 299 per cent confidence.)

to initiate altered foliar retention of ["'C]photosynthate in theprevious experiment. The effects of a 1-week exposure to SO2 at0.20 Ml I` and 0.40 I`l and 03 at 0.10 and 0.20 l I`l on 2-week-old plants are shown in Figure 3. Both foliar retention of["4C]photosynthate (day 1:initial, as a percent of controls) andnet photosynthetic rate (determined from levels of 14C uptakecompared to controls) are plotted. Ozone-treated plants showeda highly significant increase in foliar retention of ["4C]photosyn-thate accompanied by depression of net photosynthesis. SO2 didnot affect either parameter significantly. An examination oftreatment effects on weight of plant parts at harvest 6 weeks latershowed no effect of SO2, but 03 treatment produced a pattern ofincreasing biomass of leaves and stems and decreasing biomassof pods. The magnitude of increases .in assimilate retention inleaves at 0.10 and 0.20 Ml I' (6 and 24%, respectively) comparedwell with increases in stem retention (8 and 25%) and decreases

in allocation of assimilates to pods (-6 and -22%); however,differences were not statistically different at the 95% level.The changes in assimilate partitioning noted in this experiment

were accompanied by some visual symptoms of pollutant injuryon the fully expanded primary leaves. After 4 d of exposure,ozone at 0.10IO ul' produced a light uniform chlorotic stippleon nearly all primary leaves, while 03 at 0.20 ,l 1' produced amore uniform level of chlorosis, accompanied by light bifacialbleaching of some of the chlorotic stipple. SO2 produced noobvious visual injury symptoms.

In the second weekly exposure in this series, both primary andtrifoliate leaves were present and allocation and photosyntheticresponses were analyzed separately (Table II). Whereas measure-ments of 14C uptake indicated that photosynthetic rates of trifo-liate leaves were about twice those of primary leaves, photosyn-thesis was similarly affected by both pollutants regardless of leafage. Maximum photosynthetic depression following SO2 expo-sure was approximately 8 per cent and occurred at 0.40 Al 1' ofSO2. Ozone (20 g 1-') more actively inhibited photosynthesiswith a 40% depression in trifoliates and 60% depression in theprimary leaves; however, there was only one plant in the high O3group in which primary leaves had not already senesced at theend of this exposure. Premature senescence had not occurred inother treatments. Leaf retention of '4C was generally unaffectedby SO2 at all sampling intervals, while O3 at both 0.10 and 0.20gl 1' significantly reduced retention during the first 7 d afterlabeling. Subsequent relative movement of 14C from foliageduring the day 7 to harvest interval was also significantly reducedat the highest 03 level.

Total plant dry weight at harvest was reduced at highest levelsof SO2 (16%) and O3 (24%); however, differences were notstatistically significant. Partitioning of dry matter was not sig-nificantly affected by O3; however, reduced allocation to leaves(-95% significance) and increased allocation to pods (NS) oc-

curred at the highest SO2 level. These responses were accompa-nied by a generalized chlorosis of the two oldest age classes oftrifoliate leaves in the high O3 treatment, but only the oldesttrifoliates were chlorotic (lightly) with the 0.10 l1 1' treatment.The results of one final exposure of a subset of unexposed

plants from the previous experiment to 18 h of 0, 0.10, or 0.15Al I-' of 03 are shown in Table III. These plants were approxi-mately 5 weeks old and in the active pod-filling stage at the timeof this experiment, with both flowers and pods up to 10 cm longpresent. They experienced decreased photosynthetic uptake of'4C, increased foliar retention of '4C-assimilates in foliage, in-

Table II. Effects ofa 2nd Week ofExposure at Varying Levels ofSO2, and 03 on Photosynthesis, 14C Allocation, and Partitioning ofPhotosynthateby Bush Beans (P. vulgaris-290)

Plants were approximately 3 weeks old at exposure.

Sulfur Dioxide Concn. (A1/1) Ozone Concn. (A1/1)Allocation Indices

0.0 0.2 0.4 0.0 0.1 0.2

Photosynthesis[Relative 14C uptake (%)]Primary leaves 100 110 ± 22 95 ± 26 100 99 ± 48 41'Trifoliate leaves 100 97 ± 29 91 ± 8 100 93 ± 17 61 ± 12c

Leaf retention of 14CDay H:initialPrimary leaves 0.42 ± 0.12 0.46 ± 0.11 0.53 ± 0.15 0.34 ± 0.06 0.28 ± 0.08 0.45aTrifoliate leaves 0.31 ± 0.09 0.35 ± 0.15 0.29 ± 0.14 0.36 ± 0.17 0.25 ± 0.09 0.25 ± 0.07

Day 7:initial (trifoliate) 0.19 ± 0.10 0.26 ± 0.18 0.20 ± 0.13 0.21 ± 0.06 0.15b ± 0.06 0.12b ± 0.04Harvest:day 7 0.38 ± 0.17 0.41 ± 0.12 0.43 ± 0.18 0.35 ± 0.11 0.44 0.17 0.71c ±0.12

Total plant dry wt (g) at harvest 15.9 ± 2.1 15.9 ± 1.5 13.4 ± 2.3 18.0 ± 3.1 15.9 3.9 13.7 2.2a Only one plant with live primary leaves. All other values are means of six plants (± I SD).b Values significantly different from controls at 295%.c Values significantly different from controls at 299%.

LL.

CL

-1

r-M

633

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Table III. Effects of 18 Hours ofExposure to Varying Levels of03 on Photosynthate Allocation by Bush Beans (P. vulgaris-290)Plants were 5 weeks old and flowering during exposure. Zero- and 0.1 5-,u/I values are means for three plants, 0.10 M1/1 for six plants (±SD).

Ozone synlthesis(P4C Foliar Retention of Pod Activity at Harvest Activity Apportionment at Harvest

Level sUptake) C 4C (Day 1:Initial) Small Large Leaves Small pods Large pods

M1/1 % ofcontrol (dpm/g)(103) % oftotal0.00 100 0.19±0.09 22.8± 11.9 13.2±20.8 36.2± 11.7 1.1 ± 1.0 62.7± 11.70.10 90 ± 20 0.23 ± 0.06 37.3 ± 32 13.0 ± 27.8 38.1 ± 9.0 1.1 ± 1.2 60.9 ± 9.00.15 80 ± 15 0.33 ± 0.09 95.2 ± 48.2 99.1 ± 30.4 56.7a ± 10.0 3.7 ± 2.0 39.6a + 11.8

a Significantly different from controls at 295% confidence.

creased allocation of 14C-assimilates to small pods, and decreasedallocation to large pods with increasing 03 concentration. Anexamination of the distribution of activity between leaves andpods of the two size classes showed that the increased retentionof assimilates in leaves (+5 and +57% at 0. 10 and 0.15I,l 1' 03,respectively) and was accompanied by decreased allocation tolarge pods (-3 and -37%). Small pods, while experiencing adramatic increase in 14C allocation at the highest 03 level, rep-resented only a small fraction ofthe total sink for '4C-assimilates.

DISCUSSION

These experiments were designed to examine a variety ofindices of potential disruption of photosynthate allocation path-ways by air pollutants. Initial experiments with the more tolerant274 variety of Phaseolus vulgaris demonstrated no effect on totalplant yield or short-term photosynthate retention by foliagefollowing up to 40 h ofexposure to c0.50 ppm SO2 (20 1u I-'-h),however. By comparison, significant alteration of foliar alloca-tion of the more sensitive 290 variety occurred after only 8 h ofexposure to 0.75 p.l I' (6.0 sl l-'-h). With the 274 variety,analysis of both activity and biomass distribution at harvest,however, indicated that changes in allocation patterns had oc-curred principally in pods and roots and principally after longer-term exposures. Changes in 14C allocation patterns both I weekafter pollutant exposures to 40 h of SO2 and 2 weeks later whenplants were mature were similar and generally mirrored changesin partitioning of biomass. Thus, the analysis of photosynthatedistribution prior to harvest provided an early indication ofsubsequent changes in the distribution of subsequent growth.The series of experiments with the more sensitive 290 variety

demonstrated rather dramatic alterations in photosynthetic as-similation of '4C02, patterns of movement of ['4C]photosynthatefrom foliage, and allocation to developing pods, induced primar-ily by 03 exposure. Of particular interest in the experiments with03 was the concurrent decrease in both assimilation of '4CO2and reduced translocation of ['4C]photosynthate away from pol-lutant-stressed foliage (Figs. 2 and 3, and Table III). Leaf age andleaf type also exerted a strong influence on the effects of both 03and SO2 on translocation patterns. Primary leaves generallyexperienced reduced translocation in response to pollution stress;however, responses of trifoliate leaves were variable. On plantsat the flowering stage (Fig. 2; Table II), trifoliate leaves experi-enced reduced translocation of assimilates while plants exposedat an intermediate growth stage (Table II) showed the oppositeresponse. It should be noted that plants in this latter conditionwere from an exposure series in which (in the case of 03) primaryleaves had already been impaired in both photosynthetic andtranslocation potential. Thus, one might expect alteredsource:sink relations and a greater demand on trifoliate leavesfor assimilates under this condition.An examination of time series sampling in these experiments

(initial:day 1-day 7:harvest) provides a good indication of dis-ruption of allocation patterns by stress from either SO2 or 03;however, 03 can alter these processes at much lower concentra-

tions than SO2 (including 03 levels below the existing NationalAmbient Air Quality Secondary Standard of 0.12 ,l 1'). It isalso apparent that changes in allocation patterns observed within1 d after cessation of exposure to pollutants may be persistentfor several days to several weeks after cessation of pollutantexposure. Jones and Mansfield (8) also found persistent effectsof SO2 on translocation of P. pratense. Of particular significanceto air pollution studies, where altered yield is of primary interest,was the good relationship between altered short-term movementof ['4C]photosynthate away from leaves and its appearance indeveloping pods.The identification of a range of parameters of general use in

documenting stress-induced alteration of photosynthate alloca-tion patterns is important to physiological ecologists; however,identifying the mechanisms by which these alterations occurredis also important to understanding the relevance of observedresponses to whole-plant physiological function. In our studies,increased retention of assimilates in foliage was accompanied byreduced transfer of these materials to other plant tissues. Theexact mechanism by which this occurs is not known but severalpossibilities can be suggested. These include decreased phloemloading due to either a physical or biochemical blockage; in-creased allocation to repair within the leaf itself due to damageto leaf tissues; and altered balance of sources and sinks occa-sioned by reduced assimilation and a greater relative demand ofleaves for the limited pool of photosynthate produced.The transfer ofphotosynthate from source leaves to the phloem

and the translocation stream is a complex process which requiresmetabolic energy and is dependent on the balance of nutrients,carbon, water, and hormones of both source and sink regions (5,6, 23, 26). Radiochemical experiments with soybean and morn-ing glory (4) indicated that the rate of translocation was limitedlargely by the rate of tracer entry into the sieve tubes of thesource leaf. The experiments of Noyes (18) with Phaseolusvulgaris indicated that reduced translocation following exposureto SO2 was accompanied by increased loading of small veins ofsource leaves with ['4C]sucrose and an apparent decrease inloading or transport at the sieve tubes. A number of possiblemechanisms related to the known metabolic effects of air pollu-tants can be postulated for these responses. They include bothreduced photosynthetic production (reduced energy) and inhi-bition of enzymic pathways (7, 16, 27, 28) as well as a variety ofpotential secondary reactions associated with alteration of theintegrity of cellular membranes.

Translocation may also be altered by the creation of new sinkswithin the leaf itself as a consequence of disease or injury (1 1).Livne and Daly (9) examined translocation of ['4C]photosynthatein Phaseolus vulgaris and found that rust-infected leaves retainedmore endogenous ['4C]photosynthate than healthy leaves (only2 per cent of the photosynthate moved out of infected leaves).In addition, infected leaves served as sinks drawing photosyn-thate away from adjoining healthy foliage.The reduction of photosynthesis per se can be expected to lead

to altered retention of photosynthate in source leaves. The inter-

634 McLAUGHLIN AND McCONATHY Plant Physiol. Vol. 73, 1983

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EFFECTS OF SO2 AND 03 ON ['4C]PHOTOSYNTHATE ALLOCATION

nal demand for carbon by even mature leaves is rather high ( 13),and it can be expected that this on-site demand would require ahigher fraction of available photosynthate-a demand whichwould be additionally augmented by increased metabolic de-mand of injured tissues. While reduced photosynthesis maycontribute to reduced translocation, it does not appear to be aprerequisite for this process to occur (8, 14).Of particular interest in our study was the response of whole

plant allocation processes to reductions in the supply of photo-synthate. With the sensitive 290 variety, there was good indica-tion that increased retention of photosynthate by leaves occurredat the expense of allocation to pods. In the few cases where SO2increased movement of photosynthate from leaves, we foundincreased transport to pods. Similar enhanced export of carbonwas noted by Milchunas et al. (15) at concentrations of SO2which stimulated growth ofAgropyron smithii.The combined effects of air pollutants on photosynthesis and

translocation noted in this and earlier studies (14, 22) indicatethat subtle alteration of carbohydrate metabolism and distribu-tion can be detected and quantified by radiochemical techniques.With crop plants, considerable information can be gained fromfollowing uptake and partitioning of assimilates between leavesand the reproductive structures which constitute economic yield.Changes in both assimilate transfer to roots and root growthshown here and in other studies (1, 8, 24, 25) may also provideearly indications of important changes in whole plant physiolog-ical function. With perennial species, particularly trees, a morecomplete analysis of the amount and age of foliage, respiratorylosses, photosynthetic rate, and partitioning of photosynthate toboth growth and storage (14) becomes increasingly important inevaluating longer-term growth effects.

LITERATURE CITED

1. BLUM U, DT TINGEY 1977 A study of potential ways in which ozone couldreduce root growth and nodulation of soybeans. Atmos Environ 11: 737-739

2. EVANS LT 1975 Beyond photosynthesis-the role of respiration, translocation,and growth potential in determining productivity. In JB Cooper, ed, Photo-synthesis and Productivity in Different Environments. Cambridge UniversityPress, New York, pp 501-507

3. FELLOWS RJ, DB EGLI, JE LEGGETr 1979 Rapid changes in translocationpatterns in soybeans following source-sink alterations. Plant Physiol 64: 652-655

4. FISCHER DB, TL HOUSLEY, AL CHRISTY 1978 Source pool kinetics for "C-photosynthate translocations in morning glory and soybean. Plant Physiol

61: 291-2955. FONDY BR, DR GEIGER 1981 Regulation of export by integration of sink and

source activity. What's New in Plant Physiol 12: 33-366. GEIGER DR 1979 Control of partitioning and export of carbon in leaves of

higher plants. Bot Gaz 140: 241-2487. HEATH RL 1975 Ozone. In JB Mudd, TS Kozlowski, eds, Responses of Plants

to Air Pollution. Academic Press, New York, pp 23-558. JONES T, TA MANSFIELD 1982 Studies on dry matter partitioning and distri-

bution of "C-labelled assimilates in plants of Phleum pratense exposed toSO2 pollution. Environ Pollut 28: 199-207

9. LiVNE A, JM DALY 1966 Translocation in healthy and rust-infected beans.Phytopathology 56: 170-175

10. MANNING WJ 1978 Chronic foliar ozone injury: Effects on plant root devel-opment and possible consequences. Calif Air Environ 7: 3-4

11. McLAUGHLIN SB, DS SHRINER 1980 Allocation of resources to defense andrepair. In JB Horsfall, EB Cowling, Plant Disease, Vol 5. Academic Press,New York, pp 407-431

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