Carbohydrate Level and Growth ofTomatoPlants · GENT PlantPhysiol. Vol. 76, 1984 Table I. AverageGrowthConditionsandRelativeGrowthRatesforTomatoPlantsunderDifferent Growth Regimensin

Plant Physiol. (1984) 76, 694-6990032-0889/84/76/0694/06/$01.00/0

Carbohydrate Level and Growth of Tomato PlantsI. THE EFFECT OF CARBON DIOXIDE ENRICHMENT AND DIURNALLY FLUCTUATINGTEMPERATURES

Received for publication May 8, 1984 and in revised form July 17, 1984

MARTIN P. N. GENT*Department ofForestry and Horticulture, The Connecticut Agricultural Experiment Station, New Haven,Connecticut 06504

ABSTRACT

To what extent can the influence ofenvironment on greenhouse tomatoplants (Lycopersicoe escukxtwm L.) be explained by a linear response ofthe growth rate to carbohydrate level? To answer this questfon, youngtomato plnts were trasplanted in January and March ad grown forone-month periods under natural light either with or without C02 enrich-ment to 1000 microliters per liter and either under a constant iimumtemperature of 15°C or a minimum temperature that fluctuated between20°C for 12 hours inclu the photoperiod and 100C for the remaining12 hours. The carbohydrate levels were measured for plants under allgrowth conditions at several times in the diurnal cycle.

At the average irnc in January, 23 megujoules per square meterper day, plants under C02 enrichment grew 15% faster and had, onaverage, total nonstrtl carbohydrate levels 27 milims per gramgreater and soluble carbohydrates 3 milligms per gram greater at allhours of the day than did plants grown under ambient C02. Phlat grownunder fluctuating diurnal temperature grew slghtly faster and had totalnonstucal carbohydrte levels on average 8 milliams per gramgreater than plants grown under a more constant temperture. At theaverage irradiance in March-ApriL 4.3 megajoules per square meter perday, growth and carbohydrate level increased with CO2 enrichment underthe control temperature regime but not under fluctuting temperatures.Plants in all growth regimens grew faster than in January.

Over all plantings and growth regimens, relative growth rates weremore highly correlated to total nonstructural carbohydrate levels thanthey were to irrdiance, C02, or temperature.

The rate of growth of tomato in a greenhouse varies with thedaily integrated irradiance (12), the CO2 level (2, 24), and thediurnal variation in temperature (1, 6). These factors interact.Irradiance affects the growth response of tomato to CO2 level inthe greenhouse (18) and under controlled conditions (10). Diur-nal temperature fluctuations affect the response of tomato fruityield to C02 enrichment (1). Irradiance and diurnal temperaturefluctuations interact to govern the growth response of otherplants (20).The combined effects of daily integrated irradiance and CO2

level on the RGRI of tomato plants was explained by a wholeplant model relating net CO2 assimilation to production ofstructural dry matter (23). A centrl assumption of the modelwas that a linear relation exists between TNC and RGR (22 andreferences therein). The limited experimental evidence to support

' Abbreviations: RGR, relative growth rate; EST, eastern standardtime; TNC, total nonstructural carbohydrate level.

this hypothesis was that the starch level of tomato leaves at theend of the photoperiod was highly correlated to RGR, althoughthe soluble sugars level was not (23). If it is assumed that the rateof translocation is proportional to RGR, then the linear relationobserved between the level ofsucrose or starch in mature tomatoleaves and the rate oftanslocation (7) also supports this hypoth-esis. This linear relation was observed whether iradiance or C02level was used to vary photosynthesis and the carbohydrate level(8). In addition, an approximately linear relation was observedbetween the leaf extension rate and the carbohydrate content ofcereals (19).The effect of diurnally fluctuating temperature on growth of

tomato plants has also been explained in terms of a whole plantmodel ofCO2 assimilation and carbohydrate metabolism (5). Inthis case the diurnal fluctuation in TNC was defined explicitlysince the instantaneous rate of growth was assumed to dependexponentially on temperature (15, 19) as well as linearly on TNC.Although models based on whole plant CO2 assimilation andcarbohydrate metabolism did predict the effects of irradianceand CO2 level (23) and diurnal temperature fluctuations (5, 16)on vegetative growth, they may not simulate accurately thecarbohydrate status of the plant. This is because these modelswere based largely on observations relating the rates ofphotosyn-thesis and respiration to growth (15, 17, 22 and referencestherein) rather than on observations relating TNC to growth.

Is the influence of the environment on the growth of green-house tomato plants accounted for by a linear response ofRGRto the level of carbohydrate? To test this hypotheis, tomatoplants were grown for 1-month intervals in a greenhouse inwinter and spring with or without CO2 emichment and with orwithout diurnal temperature fluctuation, and their carbohydratelevels were measured. The observed diurnal variation in TNCwas compared to predictions of a whole plant model of carbo-hydrate metabolism based on this hypothesis (5).The hypothesis suges that TNC of plants in exponential

growth, with a constant RGR, does not vary with plant size.However, in cereals it was found that the leaf extension rate diddecrease for larger plants at a given level ofTNC (19). TNC levelof tomato plants growing at a constant RGR were measured onseveral dates to see if plant size affected the level ofTNC.

Diurnally fluctuating temperatures may change the ratio ofsoluble to storage forms of carbohydrate and thus the relationbetween TNC and RGR. The major component ofTNC, starch,must be transformed to sucrose or glucose before being trans-ported and metabolized at the growing points, and the activityof starch synthetase is temperature sensitive (4). The variouscomponents of TNC were examined to determine if the level ofa particular carbohydrate was more closely related to RGR thanwas TNC.

694 www.plantphysiol.orgon October 22, 2020 - Published by Downloaded from

Copyright © 1984 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

CARBOHYDRATE LEVEL AND GROWTH

MATERIAIS AND METHODS

Plant Material and Growth Conditions. Four tomato hybrids(Lycopersicon esculentum L.) were grown. Their common namesand sources were: Early Cascade, Petoseed Co., Saticoy, CA;Michigan-Ohio, Harris Seed Co., Rochester, NY; Sonato, Derui-ter Zonen, Bleiswijk, Holland; and Virosa, Enza Zaden, Enkhu-isen, Holland. Seeds of each hybrid were germinated inpeat:vermiculite at 23°C and grown under 15°C day and 13-Cnight temperatures, an irradiance of 110 w-m-2 PAR, and a 12-h photoperiod until the seedlings had three to four true leavesand attained 0.01 to 0.02 g dry weight. Then uniform seedlingswere selected and transplanted up to the cotyledons into apeat:vermiculite 1:1 v/v mix containing essential nutrients. Fourplants of one hybrid were planted per 8-1 pot. Immediately aftertransplanting, six pots of each hybrid were placed in each of fourdaylit chambers in a greenhouse. These chambers, situated onthe south side of a single pane glasshouse, were separated bydouble walls of 0.05 cm acrylic sheet, and heated and ventilatedindependently. Two chambers had the control temperature reg-imen: a minimum temperature of 15C and a maximum tem-perature of 21C. The other two chambers had a fluctuatingtemperature regimen: a minimum temperature of 21C from0600 to 1800 h EST and 9°C from 1800 to 0600 h EST and amaximum temperature of 27°C. Two chambers, one of eachtemperature regimen, had a CO2 enrichment regimen from 0700to 1700 h EST when ventilation was not required. An IR gasanalyzer in one of these chambers controlled the injection ofCO2 to maintain 1000 ± 100 1-1-'. The other two chambershad an ambient CO2 regimen with CO2 levels that varied from500 ,ul-1- in the dark to 250 Ml-l' on sunny days with noventilation. During ventilation, all chambers had a CO2 level of350 ul-1-'. Pots were spaced 25 cm on center in a square array.They were watered with N:P:K 20:20:20 w/w% at 200 mgml-'N when moisture tension of the root medium fell to -0.2 bar.On January 3, 1983 and March 18, 1983 plants were trans-

planted and placed in the chambers with the four different growthconditions. Twenty-four plants were harvested per chamber atabout 8, 16, and 26 d after transplant. The soil was loosened andone plant per pot was extracted with most of the roots attached.The roots were washed in water at 4°C and the plants frozen at-20°C and freeze dried. Plants were harvested either all at once,at noon, or one per hybrid per chamber at 4-h intervals beginningat noon and continuing to 0800 h EST on the next day. Afterdrying, roots, stems, and leaves were weighed and whole plantswere ground to pass a 20-mesh sieve. During sequential harvestsat 4-h intervals, plants ofall hybrids harvested from one chamberat a given time were combined before grinding.Growth Analysis. The RGR was determined from linear

regression of the natural log of whole plant dry weight versustime. RGR was determined separately for each hybrid in eachchamber. Analysis of variance of RGR indicated no significantdifference between hybrids so the variation in RGR betweenhybrids was used as an estimate of the standard error.Carbohydrate Analysis. Thirty-mg subsamples of ground

whole plant material were rehydrated and digested for 42 h at37°C with 5 mg-ml-' a-amylase (Miles Labs, Elkhardt, IN). Thesolubilized carbohydrates were hydrolyzed and reducing sugarsmeasured colorimetrically through reduction ofK3Fe(CN)6. Thismethod determined TNC in grams of glucose equivilant pergram dry weight (21). The analysis was repeated up to 5 times toreduce the standard error of the estimate for each sample below5 mg-g-' TNC.

Soluble sugars from 100-mg subsamples were repeatedly ex-tracted with 15 ml of 80 v/v% ethanol in a microsoxhlet appa-ratus. The extract was dried at 50°C under reduced pressure, thentaken up in 2 ml water and passed through a 0.22 gm filter. A50 Al subsample was injected onto an aminex HPLC column

(HPX87C, dimensions 300 x 7.8 mm, BioRad, Richmond, CA).The sample was eluted with water at a rate of 1.0 ml.min-'through anion and cation exchange precolumns at 20C and theaminex column at 75C. Sugars were detected by differentialrefractometry and the amounts determined from standardcurves.The statistical significance of the effects of CO2 enrichment

and fluctuating temperature growth regimens on carbohydratelevels were determined by three-way analysis of variance versustime of harvest, CO2 regimen, and temperature regimen. Inter-actions between times of harvest and growth regimens wereexcluded from the analysis.Measurement of Environment. Solar radiation was measured

with a recording pyroheliometer placed in the greenhouse butoutside the chambers. Integrated daily irradiance was determinedfrom the area under the tracing for each day. PAR was assumedto be half of the total. Temperatures in a chamber with thefluctuating temperature regimen and in a chamber with thecontrol regimen were continuously recorded on hydrothermo-graphs. Mean temperatures from 0600 to 1800 h EST and from1800 to 0600 h EST were determined from the areas under thetrace.

RESULTSGrowth Rates and Growth Conditions. For the January plant-

ing, regression of ln (dry weight) versus time, separately for eachgrowth regimen, gave an R2 of about 0.95 (Fig. 1). The corre-sponding R2 for the March planting was 0.98. Second orderregression did not increase the R2, indicating that the RGR wasconstant within experimental error. Only in the January plantingdid RGR differ significantly for plants grown with and without

0

45r

4.0

2.0

1.0

0.4

02

0.1

0.063Jan II Jan 19Jan 27 Jan

FIG. 1. Total dry matter accumulation of tomato plants grown indifferent growth regimens in winter. The growth regimens are defined bythe symbols: (0, 0), ambient C02; (H,O), CO2 enrichment to 10001Ol1-'; (0, 0), control temperatures; (0, H), fluctuating temperatures. Barsindicate the SE of the estimate.

I

0t

695

www.plantphysiol.orgon October 22, 2020 - Published by Downloaded from Copyright © 1984 American Society of Plant Biologists. All rights reserved.


GENT Plant Physiol. Vol. 76, 1984

Table I. Average Growth Conditions and Relative Growth Ratesfor Tomato Plants under Different GrowthRegimens in Winter and Spring

Average ConditionsGrowth Regimen ReaieSE OfPeriod of Growth C02 Temperature Daily Portion of Temperature Growth Estimate

integrated photoperiod Rateirradiance CO2 enriched Day NightMJ.m2.d' % °C g-g-'-d'

January 3-31 Ambient Control 0 18.7 14.9 0.123Fluctuate 2.29 21.2 11.8 0.133 0.004

Enriched Control 83 18.7 14.9 0.148Fluctuate 21.2 11.8 0.150

March 18-April 13 Ambient Control 0 19.6 16.0 0.170Fluctuate 4.28 22.9 14.3 0.169 0.003

Enriched Control 46 19.6 16.0 0.175Fluctuate 22.9 14.3 0.170

250

IE04..

0co0

-i7d4.

04-co

04-0

200

150 [

100[

501200 1600 2000 2400 0400 0800

Hour of day ESTFIG. 2. TNC during one diurnal cycle on January 31 for tomato

plants grown in different CO2 and temperature regimens in winter.Symbols are the same as in Figure 1.

CO2 enrichment (Table I). In January, fluctuating temperaturesincreased growth under both CO2 regimens but this effect wasonly statistically significant (p < 0.05) in two-way analysis ofvariance of the dry weight of plants harvested on January 19versus the CO2 and temperature regimens. Tomato plants trans-planted in March grew significantly faster under all growthregimens than in January, probably because daily integratedirradiance was almost double in the spring. Mean daily temper-atures increased by only 1°C for the fluctuating temperatureregimen and 1.6°C for the control regimen in the spring com-pared to the winter. The difference in mean day and nighttemperatures remained about 4C for the control regimen andabout 9C for the fluctuating regimen in both plantings. Thedaily duration of CO2 enrichment was greatly reduced in thespring compared to the winter. Often ventilation from 1000 to1500 h EST in the spring, the period of greatest irradiance andmaximal photosynthesis, eliminated the difference in CO2 levelsbetween growth regimens. Consequently, little difference was

250

0,T

coE0-W

co-

ID.00

U

co

4..U

0c0c

4..0

200 F

150

100I

501200 1600 2000 2400 0400 0800

Hour of day ESTFIG. 3. TNC during one diurnal cycle on April 4 for tomato plants

grown in different CO2 and temperature regimens in spring. Symbols arethe same as in Figure 1.

expected in daily integrated photosynthesis.Total Nonstuctural Carbohydrate Level. The tomato plants

showed a large variation in TNC over one diurnal cycle. TNCreached a maximum of 170 to 220 mg.g-' and a minimum of80 to 120 mg-g-' for plants harvested on January 31, 1983 (Fig.2). A maximum of 210 to 230 mgg7' and a minimum of 105to 135 mg.g7' TNC were found in plants harvested on April 4,1983 (Fig. 3). The daily maximum TNC was always found inplants harvested at 1600 h EST and the minimum values at 0800h EST. Between these two harvests, TNC declined approximatelylinearly through the hours of darkness. Most of the increase in

TNC in the daylight hours occurred between 0800 and 1200 hwith only a small increase between 1200 and 1600 h EST. Neitherseason nor growth regimen changed this diurnal pattern. Ingeneral, TNC was lower in plants grown in winter than in spring.The growth regimens had a sigificant effect on the TNC of

tomato plants grown in January. On January 31, TNC wasgreater at all hours of the day under CO2 enrichment (Fig. 2)

696

0o

°-

o i

4

0

II I I~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~




Table II. Average Total Nonstructural Carbohydrate and Soluble Carbohydrate Levels in Tomato Plantsgrown in Different Growth Regimens in Winter and Spring

TNC and soluble sugars were assayed as described in "Materials and Methods". Results were averaged overthe six harvest times in one diurnal cycle.

Carbohydrate LevelsHarvest Date Growth RegimenCO2 Temperature Total Total

nonstrtal Totalub Sucrose Glucose Fructosenonstructural soluble

mg-g9'

January 12 Ambient Control 139.0 24.5 7.1 4.4 13.0Fluctuate 138.0 30.2 7.6 6.7 15.9

Enriched Control 147.0 30.4 8.1 6.1 16.2Fluctuate 165.0 36.1 9.4 8.6 18.2

January 31 Ambient Control 127.0 28.0 6.8 6.2 15.0Fluctuate 132.0 31.0 6.8 7.4 16.7


April 4 Ambient Control 162.0 35.3 9.4 8.7 17.3Fluctuate 171.0 33.7 9.7 7.8 16.2


SE 3.3 2.4 0.4 0.7 1.3

Table III. Total Nonstructural Carbohydrate Levels at Noon in Various Tomato Hybrids and onVarious Dates

TNC was assayed as described in "Materials and Methods".Total Nonstructural Carbohydrate with

Daily following Growth RegimenHarvest Date Hybrid Integrated Ambient C02 C02enriched

IrradianceControl Fluctuate Control Fluctuate

Mj M-2 d-s mg-g9'

January 12 1.42Combined 148 150 151 163

January 19 3.51Sonato 196 216 253 303Virosa 197 203 229 284Michigan-Ohio 181 190 206 292Early Cascade 178 168 196 265

January 31 2.20Combined 139 146 166 191

April 4 3.29Combined 202 200 208 209SE 3.3

and to a lesser extent under fluctuating temperatures. Averagedover one diurnal cycle, the CO2 enrichment regimen increasedTNC over the ambient CO2 regimen by 24 to 31 mg.g' forplants under control and fluctuating temperature regimens, re-spectively (Table II). The fluctuating temperature regimen in-creased TNC by 5 to 12 mg-g-' with respect to control temper-ature regimen for plants grown under ambient and enrichedC02, respecfively (Table II). Effects of CO2 enrichment (p <0.01) and fluctuating temperatures (p < 0.05) were statisticallysignificant by the analysis of variance used. No significant inter-action was found between the effects of CO2 and temperature.Despite the 10-fold increase in plant size from January 12 toJanuary 31 (Fig. 1), there was little difference in TNC of plantsharvested on these two dates. In addition, the growth regimes

had similar effects on TNC of plants harvested on January 12and on January 31 (Table II), with the exception of plants grownunder the ambient CO2 and control temperature regimen.Of the plants grown in the spring and harvested on April 4,

only those grown under the CO2 enrichment and control tem-perature regimen had consistently greater TNC throughout thediurnal cycle (Fig. 3). There were no differences in TNC ofplantsgrown with and without CO2 enrichment under the fluctuatingtemperature regimen. Analysis of variance indicated that CO2enrichment increasedTNC significantly (p< 0.01), by an averageof 11 mg-g-', but this was canceled under fluctuating tempera-tures by a negative interaction (p < 0.01) between the effects ofCO2 enrichment and fluctuating temperature. The temperatureregimen alone had no statistically significant effect on TNC of

697



Plant Physiol. Vol. 76, 1984

25.

20

o g5LI S

10

CP)

C*0

C.)

CD

I0 [

51

0

I0,

5

0

1200 1600 2000 2400 0400 0800Hour of day EST

FIG. 4. Soluble carbohydrate levels during one diurnal cycle on Jan-

uary 31 for tomato plants grown in different CO2 and temperature

regimens in winter. Symbols are the same as Figure 1.

I C0

101cn

0,C-)

C-

.0

0

0.20

0.18

0.16

0.14

0.12

0.100..10 0.14 0.18

Predicted rgr

FIG. 5. Observed relative growth rates versus the prediction of a

mathematical model using the average irradiance, CO2 level, and tem-

perature during the growth interval. Symbols are the same as in Fig-

ure 1.

plants grown in the spring.Daily integrated irradiance affected TNC of plants harvested

at noon more than the growth regimens. Plants harvested on

January 19 and April 4 had similar TNC and the irrdiance was

similar for the two days (Table Ill). The irradiance on January

31 was close to the average for the period over which RGR was

determined for the winter planting. Thus, TNC of plants har-

vested on this date should approximate the level over the entiregrowth interval. The irradiance on April 4 was less than the

average for the spring planting. TNC of plants harvested on this

date may have been less than the average for the growth periodof the spring planting.There was some variation in TNC between hybrids. With few

exceptions the TNC of the hybrids was in the order. Sonato >Virosa > Michigan-Ohio > Early Cascade, in each of the growth

regimens on January 19. However, the growth regimens generallyhad the same effect on the TNC of each hybrid. Also, the growthregimens had the same effect on TNC of the combined sampleof all hybrids, for the three separate harvest dates in January.

Soluble arbohydrate. The level of the soluble carbohydrates,sucrose, glucose, and fructose, varied 2-fold from day to night(Fig. 4). In contrast to the diurnal variation in TNC, whichdeclined in a linear fashion throughout the night, the level ofsoluble carbohydrates showed a rapid decline at the onset ofdarkness. This pattern was the same for both plantings and allgrowth regimens.The levels of sucrose, glucose and fructose in plants grown in

winter and harvested on January 31 were inced by the C02enrichment regimen at all times in a diurnal cycle (Fig. 4). Plantsgrown under CO2 enrichment and fluctuating temperatures hadthe highest level of solublecarbohydrates during the day. Analysisof variance indicated that CO2 enichment increased the level ofeach of the soluble sugars significantly (p < 0.01), by about 2mg-g-', but the fluctuating temperature regimen had no effect.Nearly identical trends were found for plants harvested on Jan-uary 12 (Table II).No consistent differences in soluble carbohydrate levels were

found for plants under the different growth regimens in thespring. The levels of all soluble carbohydrates in plants harvestedon April 4 were about the same as for plants grown under CO2enrichment and harvested on January 31. Total soluble carbo-

hydrates were significantly greater in spring than winter for plantsgrown under the ambient CO2 regimen.

Reltion between Carbohydrate and Growth. There was a goodcorrelation between TNC of plants harvested on January 31 andApril 4 and RGR for the respective 1-month period in winterand spring. Regression of TNC, averaged over one diurnal cycle,versus RGR for each of the four growth regimens in the twoplantings accounted for 90% of the variance in RGR, R2 = 0.90.Regression of sucrose levels versus RGRgave a similar R2, 0.89.However, other soluble carbohydrates showed less correlationwith RGR; R2 values for regression ofRGR versus levels of totalsoluble carbohydrate, glucose, and fructose were 0.48, 0.30, and0.18, respectively. TNC or sucrose were significantly better cor-related with RGR than any one of the environmental parametersthat varied between plantings or growth regimens within plant-ings. Regression of RGR versus daily integrated irradiance, per-cent of phQtoperiod with CO2 enrichment, or mean daily tem-perature resulted in an R2 of 0.81, 0.02, and 0.65, respectively.RGR was consistent with the environmental data when these

data were used in a whole plant model of photosynthesis, car-bohydrate metabolism, and growth. The model was based on thehypothesis that RGR, carbohydrate metabolism, andrespirationassociated with growth werelinearly related to TNC and expo-nentially related to temperature (5). Coefficients forrespirationassociated with growth and maintenance were 65 mg C02g-'TNCrh-' and 3.0 mg C02.g- lh-', respetvely, at 25C with atemperature dependence that doubled every 10C. The modelalso assumed photosynthesis had an asymptotic dependence onirradiance, C02, and temperature. Maximal photosynthesis wasassumed to be 12 g.CO2.m-2-hl' with ahalfmaximal rate atirradiance of 50w.m-2 PAR, CO2 level of 250,dul-', andtemperature of 12°C, respectively. Leaf area index was assumedto be one and leaf arearafio was 50 g.m-2.

These coefficients were used with the values for irradiance,CO2 enrichment, and day and nighttemperature averaged over1 month of growth (TableI) topredict RGR in each growthregimen of the two plantings (Fig. 5). The predicted RGR ac-counted for 85% of the variance observed so the prediction wasabout as reliable as one based on average TNC alone. The modelpredicted correctly the differences found in RGR between growthregimens in the winter planting. However, the model always

698 GENT

* d

*~~ *

9~~~(P 13 0 0 30

o 3o

0

0~~~~~~

* U

0

o 0

I i ~ ~~~~~~ido

4J *

-o0

* a,F107 ¶ 7

I

I




predicted higher growth rates and TNC under fluctuating com-pared to control temperature regimens while this difference wasnot observed in the spring planting.More important, the model predicted accurately the observed

variation in TNC throughout the diurnal cycle, and for the winterplanting, the variation in TNC due to growth regimens. Themodel accounted for 95% of the diurnal variation of TNC onJanuary 31 and 93% ofthe variation found on April 4, accordingto analysis of variance of observed minus predicted values ofTNC. The model also accounted for 95% of the variation ofTNC due to the effects of CO2 and temperature regimens in theJanuary planting. The negative interaction observed between theeffects ofCO2 enrichment and fluctuating temperature regimenson TNC of plants harvested on April 4 could not be predictedby the model, so it accounted for only 44% of this variation.

DISCUSSION

Thornley and Hurd (23) proposed that a linear relationshipbetween TNC and growth rate explained the combined effects ofirradiance, photoperiod, and CO2 concentration on the RGR ofyoung tomato plants. The measurements ofTNC presented hereprovide experimental evidence to support this concept and ex-tend it to include the effects of diurnal temperature fluctuations.A model incorporating a linear dependence of RGR on TNCand an exponential dependence on temperature not only pre-dicted RGR but also simulated accurately the average level ofTNC and its diurnal fluctuation. Challa (3) proposed that thebeneficial effect ofa cool night period on winter-grown cucumberwas to prevent complete exhaustion ofTNC. The present exper-iments showed no evidence of exhaustion of TNC at any timeduring the diurnal cycle for tomato plants grown under a meantemperature of 17°C.The relation observed between TNC and RGR on the whole

plant level may not necessarily hold for single leaves. In expand-ing leaves oftomato, the carbohydrate level decreased at the timeof fastest growth (9). Likewise, in various cereals there was apositive correlation between the elongation rate of individualleaves and the TNC of the whole plant (19), but there was anegative correlation between leaf elongation rate and TNC ofthe extension zone of the leaf in wheat (1 1). Thus, it is only thewhole plant TNC that should be considered in relation to RGRof the whole plant.The model used here (5) more successfully predicted RGR

and TNC of tomato plants grown in winter than in spring. Themodel predicted a benefit of diurnal temperature fluctuation onboth TNC and RGR from increased photosynthesis under thewarm day temperatures of the fluctuating temperature regimen.Otherwise the increased carbohydrate metabolism under fluc-tuating temperatures would be detrimental to growth (16). Forinstance, subterranean clover swards grew more slowly underhigh light and fluctuating temperatures than at a constant tem-perature with the same mean of20C over the diurnal cycle (16)and this was predicted by a whole plant model of growth andcarbohydrate metabolism that assumed daily integrated photo-synthesis was the same for both growth regimens, as was ob-served. Under the high light and warm temperatures of spring,photosynthesis ofthe tomato plants may not have been increasedsufficiently under fluctuating temperatures to offset the predictedincrease in carbohydrate metabolism.The biochemistry of growth metabolism suggests that RGR

should be more highly correlated to the level of soluble carbo-hydrates than to the level of starch or TNC. This was notobserved in practice. Tomato plants grown under high light andvarious CO2 levels had increased rates of growth (14) and in-

creased levels of starch up to 2200 jul .1-' CO2 while levels ofsucrose and glucose remained constant at CO2 levels above 1000;d-.L' (13). In my experiments there was a poorer correlationbetween total soluble carbohydrate and RGR than between TNCand RGR. Since soluble carbohydrates were an intermediary inthe transformation of starch to structurl material, and the starchwas never completely depleted under the growth conditions usedhere, there was no compelling reason for the level of solublecarbohydrate to vary with RGR. In fact, TNC was most highlycorrelated with RGR. Although TNC varied within a diurnalperiod, from day to day according to irradiance, and amonghybrids of tomato, it was a more reliable indicator of the RGRthan any other aspect of the plants or their environment.

Acknowledgments-I thank Roxanne Brown for assistance in growing the plantsand analyzing their carbohydrate levels.

LITERATURE CITED1. CALVERT A 1972 Effects of day and night temperatures and carbon dioxide

enrichment on yield of glasshouse tomatoes. J Hortic Sci 47: 231-2472. CALVERT A, G SLACK 1975 Effects of carbon dioxide enrichment on growth,

development and yield of glasshouse tomatoes I. Responses to controlledconcentrations. J Hortic Sci 50: 61-71

3. CHALLA C 1976 Analysis of the diurnal course of growth, carbon dioxideexchange, and carbohydrate reserve content of cucumber. Agric Res RepWageningen 861

4. DOWNTON WJS, JSHAWKER 1975 Response ofstarch synthesis to temperaturein chilling-sensitive plants. In Marcelle R, ed, Environmental and BiologicalControl of Photosynthesis. Dr W Junk, The Hague, pp 81-88

5. GENT MPN, HZ ENOCH 1983 Temperature dependence of vegetative growthand dark respiration: A mathematical model. Plant Physiol 71: 562-567

6. HARSEMMA H 1977 Root temperature and growth of young tomato plants.Meded Landbouwhogesch Wageningen 77-19

7. Ho LC 1976 The relationship between the rates of carbon transport andphotosynthesis oftomato leaves. J Exp Bot 27: 87-97

8. Ho LC 1978 The regulation of carbon transport and the carbon balance ofmature tomato leaves. Ann Bot 42: 155-164

9. Ho LC, AF SHAW 1977 Carbon economy and translocation of'4C02 in leafletsof the seventh leaf oftomato during leaf expansion. Ann Bot 41: 833-848

10. HURD RG, JHM THORNLEY 1974 An analysis ofthe growth ofyoung tomatoplants in water culture at different light integrals and CO2 concentrations. I.Physiological aspects. Ann Bot 38: 375-388

11. KEMP DR, WM BLAcKLow 1980 Diurnal extension rate of wheat leaves inrelation to temperatures and carbohydrate concentrations of the extensionzone. J Exp Bot 31: 821-828

12. KLAPWUK D, PJAL DE LINT 1975 Growth rates of tomato seedlings andseasonal radiation. Neth J Agric Sci 23: 259-268

13. MADsEN E 1968 Effect of CO2 concentration on the accumulation of starchand sugar in tomato leaves. Physiol Plant 21: 168-175

14. MADsEN E 1973 The effect of CO2 concentration on development and drymatter production in young tomato plants. Acta Agric Scand 23: 235-239

15. MCCREE KJ 1974 Equations for the rate of dark respiration of white cloverand grain sorghum as functions of dry weight, photosynthetic rate andtemperature. Crop Sci 14: 509-514

16. MCCREE KJ, ME AmTHOR 1982 Effects ofdiurnal variation in temperature onthe carbon balances ofwhite clover plants. Crop Sci 22: 822-827

17. MOLDAU H, A KAROLIN 1977 Effect of the reserve pool on the relationshipbetween respiration and photosynthesis Photosynthetica 11: 38-47

18. NEWTON P 1966 The influence of increased Co2 concentration and supple-mental illumination on growth oftomato seedlings during the winter months.Ann Appl Biol 57: 345-353

19. PENNING DE ViuEs FWT, JM WVLAGE, D KREMER 1979 Rates of respirationand of increase in structural dry matter in young wheat, ryegrass and maizeplants in relation to temperature, water stress and to their sugar content.Ann Bot 44: 595-609

20. RAJAN AK, GE BLACKMAN 1975 Interacting effects of light and day and nighttemperatures on the growth of four species in the vegetative phase. Ann Bot39: 733-743

21. STREETER JG, DL JEFFERS 1979 Distribution of total non-structural carbohy-drates in soybean plants having increased reproductive load. Crop Sci 19:728-734

22. THORNLEY JHM 1982 Interpretation of respiration coefficients. Ann Bot 49:257-259

23. THORNLEY JHM, RG HURD 1974 An analysis of the growth of young tomatoplants in water culture at different light integrals and CO2 concentrations. II.A mathematical model. Ann Bot 38: 389-400

24. WITTWER SH, WM ROBB 1964 Carbon dioxide enrichment of greenhouseatmospheres for food crop production. Econ Bot 18: 34-56

699



Documents

Carbohydrate Level and Growth ofTomatoPlants · GENT PlantPhysiol. Vol. 76, 1984 Table I. AverageGrowthConditionsandRelativeGrowthRatesforTomatoPlantsunderDifferent Growth Regimensin