CARBOHYDRATE METABOLISM IN THE TOMATO FRUITAS AFFECTED BY POLLINATION, FERTILIZATION
AND APPLICATION OF GROWTHREGULATORS'
E. MARRE AND A. E. MURNEEK
DEPART-MENT OF HORTICIULTURE, UNIVERSITY OF MISSOURI, COLUMBIA, MISSOURI
Received May 7, 1952
Introduction
Wl'hile there is considerable information on the morphological effectsfrom pollination and fertilization and application of growth-regulating sub-stances on fruit development, our knowledge of the physiological aspectsrelated thereto is still very meager. In a general way, it has been observedthat, as a result of sexual reproduction (syngamy), the over-all metabolismof ovaries and associated tissues is greatly stimulated resulting in diversionof food to these organs (25). This stimulus from reproduction can be initi-ated and maintained in many plants by the timely application of an appro-priate synthetic plant growth-regulator (8). The present paper deals withone physiological aspect, carbohydrate metabolism, as affected in fruitshortly after pollination, fertilization, or application of growth regulator.
Marked changes in carbohydrate content in ovaries after pollinationwere observed in orclhids by HSIANG (12), and SESHAGIRAH (32) noted anincreased starchl synthesis in the ovaries, receptacles, and pedicels immedi-ately after fertilization which also has been pointed out as a common occur-rence by IMARRE (16, 19). The excision of young seeds usually leads to areduction in starch and sugar content in associated tissues (17, 19) with acorresponding increase in amylase activity. These facts indicate quite defi-nitely that the seeds have a controlling influence on carbohydrate metabo-lism of the fruit and adjoining parts of the plant. An effect on carbohy-drate content is usually obtained by the application of a growth regulatoras is evidenced by the results secured with roots (4), leaves (22, 23), stems(2, 3, 5, 6, 35), young floral organs (16), and stomata (20). MARRE (16)was able to substitute the application of indoleacetic acid for pollinationand fertilization as regards an effect on amylase activity and synthesis ofstarch reserves in the fruit of Erodium and Pelargonium. That auxins areproduced in fruits has been shown by GUSTAFSON (8), WITTWER (37),HAAGEN-SMIT et al. (9), NITSCH (30) and othiers.
In the light of this evidence, the following inferences appear probable:(a) The fertilized ovules are powerful centers for the production of nativeauxins, wlhich regulate the carbohydrate metabolism in the fruit. (b) Growthregulators effect changes in carbohydrate metabolism similar to those
1 Journal series paper no. 1305, Missouri Agricultural Experiment Station.
brought about by pollination and fertilization. It was thought desirable tostudy further the analogy between pollination-fertilization and treatmentwith growth regulator in their bearing on change in carbohydrate content,with special reference to the crucial early stages of fruit development.
Experimental procedureThe experiments were conducted with the tomato (Lycopersicumn escu-
lenturn var. Marglobe) grown in soil in large containers and kept in a well-lighted, thermostatically controlled greenhouse. The plants were allowed togrow to a large size and were vigorous. Fruit setting was prevented bydefloration, excepting where specified otherwise. The experimental treat-ments were as follows: (a) Flowers pollinated, at noon on the first day ofanthesis. (b) Flowers einasculated the day before anthesis. Two thirds ofeach style was removed and pure lanolin applied at noon of the followingday. (c) Treatment as in (b) but a growth regulator was incorporated intothe lanolin.
The regulators used were p-chlorophenoxyacetic acid (CPA) and theethyl ester of indoleacetic acid (EtIA). The first compound has been shown
TABLE IEFFECTS OF POLLINATION AND GROWTH REGULATORS (p.CHLOROPHE-
NOXYACETIC ACID, CPA; ETHYL ESTER OF INDOLEACETIC ACID,EtIA) ON GROWTH AND CARBOHYDRATE CONTENT
OF YOUNG TOMATO FRUITS.
Age and Average Reducing Sucrose Starch Soluble solubletreatment weight sugars sugars sugars
by MURNEEK (24) to be potent in the stimulation of tomato fruit setting,and the second has been found to be an unusually active naturally occurringderivative of indoleacetic acid (31). In either case the substance was firstdissolved in ethanol and then incorporated into lanolin in concentrationsgiven in the tables (tables I and II). The alcohol was removed at 400 C.The lanolin paste was applied to the cut surface of the style by means of amicrometer controlled syringe fitted to a medium-sized needle which madeit possible to control the quantity of paste used at 0.01 ± 0.001 ml.
Treatments were performed at noon to minimize as much as possible thefluctuations in carbohydrate content due to variations in light and tempera-ture. The plant material for analyses was collected on the same day, or two,three, or eight days after treatment. Each sample consisted of 8 to 14 aver-age fruits. The material was fixed and preserved in alcohol, extracted andcleared by the usual procedures, and the carbohydrates were determined bythe NELSON colorimetric technique (28).
Results
The results of carbohydrate analyses are presented for unpollinatedovaries treated with lanolin, ovaries stimulated by pollination and fertiliza-tion, ovaries treated with growth regulators, and ovaries treated with growthregulator in the presence of other developing fruits. Growth of the ovarieswas measured by average changes in fresh weight. The data presented in
tables I and II and figures 1 and 2 show that, if pollination is prevented, nosignificant change in starch and reducing sugar content occurs during aperiod of two to three days after anthesis. The small decrease in sucroseconcentration probably indicates a loss due to respiration. Considering therelative stability in carbohydrate metabolism of unpollinated ovaries, it ispossible to make a comparative study of the effects of pollination and fertili-zation and chemical treatment.
a! ' L O 0 3 'DAYS FROM ANTHESIS DAYS FROM ANTHESIS
(C) STARCH ()TOTAL SUGARS&STARCH...1500 CI 3000 TOTAL SUGARS---- EIA103FIGTONTcLPOLL.NTg POLL.
3250CPA; or ethylestrofindolecticacidEtIA)ocarbohyrateconentofyLPA ung
1000 I2
someextentp.aswhtplto POLL.
ioo~8-~..-a.
C01 3I~CMRN9T POLL.0 3 ~~~~*0 3 0
DAYS FROM ANTHESIS DAYS FROM ANTHESIS
FIG. 1. Effects of pollination and growth regulators (p-chlorophenoxyacetic acid,CPA; or ethyl ester of indoleacetic acid, EtIA) on carbohydrate content of youngtomato fruits. A, reducing sugars. B, sucrose. C, starch. D, total sugars and starch.
As early as 48 hours after pollination, there was a marked increase instarch content of the ovaries, a slight increase in reducing sugars and anoticeable decrease in sucrose, which, as was noted before, had occurred tosome extent also without pollination. From the third to eighth day afterpollination there was a further striking increase (500 to 11000%) in reducingsugars and starch. A further decrease of sucrose, not as marked as on the
MARRE AND MURNEEK: CARBOHYDRATE METABOLISM IN TOMATO 259
first days but still noticeable, was also observed. As a consequence of thisalteration in sucrose content in comnparison to reducing sugars, the concen-tration of the total sugars decreased after pollination until the third day andthen increased rapidly. Total carbohydrate (starch plus sugars) contentincreased immediately after pollination or treatment.
Both p-chlorophenoxyacetic acid (CPA) and the ethyl ester of indole-acetic acid (EtIA) induced carbohydrate changes in young tomato fruits
(A) INCREASE IN FRESH WT-NO FRUIT
26t--.RUMEENT ElA 4XI10
24
22 // ^EIA I
20./E A4Cf
lpz// ,/EIA 104
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is. "~/~~~~ COFdTR. POLL.
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A2.-CNR O PIOLL.
10
0 1 2
DAYS FROM ANTHESIS OR POLLINATION
(C) SUCROSE
- NO FRUITF_fRUITS PRESENT
---CONTROLS
~CNR. POLL.
KS4
200
P0
ISOIInE 140
j 1200B 100
a0so2 so
(B) REDUCING SUGARS
-NO FRUITF__.-jqrWENT A£ 6
A4eCIA 4X 104
/ CIA W4//, A 104
-=-= = =...=.c-ONTR.POLL.CONTR.NOT POLL
DAYS FROM ANTHESIS OR POLLINATION
r 1200
X 1000U.
a goo
k!400
i202
DAYS FROM ANTHESIS OR POLLINATION
(D) STARCH
EIA 115- NO FRUIT C.-FRINIS PESENT-.-O TROS N
IA 4XI14
/sI10%/
IA 163/// EIA 4X F
,- ,.EIA S4, .-CONTI1POLL.
CONTFR NOT PO-
DAYS FROM ANTHESIS OR POLLINATION
FiG. 2. Effects on growth and carbohydrate content of young tomato fruits, duringa two-day interval, when treated with different concentrations of the ethyl ester ofindoleacetic acid (EtIA). A, increase in fresh weight. B, reducing sugars. C, sucrose.
D, starch.
that were very similar to those brought about as a result of pollination andsubsequent fertilization. Reducing sugars and starch increased and sucrose
decreased. The chief difference between the effects of pollination and fertili-zation and of an external supply of a growth regulator was a more rapidresponse to the latter, which however showed a tendency to disappear withtime. CPA was possibly more active than EtIA in increasing the reducing
sugar content but was less active in stimulating starch synthesis. WhenEtIA was applied in concentrations greater than 10-4 1YJI, the effect on carbo-hydrate metabolism appeared to be proportional to the concentration, buta concentration of 3 x 10-5 W was practically inactive. This observationsuggests the probable existence of a threshold concentration as regards theeffects of EtIA on carbohydrate metabolism, at least in this instance.
The fruit set and development of the tomato is affected by the presenceof older fruits on the plant, whether the growing fruits are in the immediatevicinity of the young ones (fig. 3) or at some distance (26). In this test,older fruits were absent or five to seven fruits approximately three weeksold were present. These fruits were borne at other positions on the plantthan the experimental ovaries. It is evident from table II and figure 2 thatin the presence of fruits the increase in reducing sugars and starch and the_..similar reduction in increase in fresh weight of the fruit.
During the first 48 hours the growth of the fruit, as indicated by changein fresh weight, was increased as a result of pollination but much more fromapplication of EtIA. It was also significantly greater in the absence thanin the presence of other large fruits on the plant (table II). After fertiliza-tion (from the third day on) which usually has a more marked stimulationon growth than pollination alone, there was still a noticeable difference insize between the fruits induced naturally and those induced by the hormonein favor of the latter. By the eighth day this difference had decreased con-
siderably. It would seem that stimulation from an external supply of ahormone was initially greater than from pollination and fertilization butthat it decreased more with time. The native auxin produced as a result offertilization seems to hav,;e a continuous and probably increasing effect onmetabolism and growth (23).
NIARRE AND M'-URNEEK: CARBOHYDRATE METABOLISNI IN TOMATO 261
Discussion
It is a well established fact that indigenous auxins are of importance forfruit setting and development (8, 25). In the present investigation it hasbeen shown that a close similarity exists in general carbohydrate metabolismbetween pollinated and fertilized ovaries and ovaries treated with a hor-mone. The fact that the carbohydrate changes are less marked after polli-nation than with auxin treatment but that after fertilization they soon reachthe same level both in the fertilized and in the treated ovaries seems to indi-cate that during pollen germination and pollen tube growtth, auxin is re-leased in smaller amounts than after fertilization, which in the tomato occursabout two days after pollination (13). It has been demonstrated that incorn, following fertilization, a peak in native auxin concentration is reachedin about 10 to 15 days (37). No such maximumlhas been established in thetomato.
The main features of carbohydrate metabolism as a result of pollinationand fertilization or treatment of tomato ovaries, were the over-all increaseof the total carbohydrate concentration and the passage to a different equi-librium between the different carbohydrates through the initiation of starchsynthesis, the decrease of sucrose, and the striking increase of reducingsugars. These results are in good agreement with the analytical records forflowers, the naturally set young fruit of Pyrus malus (27), and the observa-tions of carbohydrate changes after pollination or chemical treatment oforchids (12). Following pollination a rapid starch synthesis has been ob-served in ovaries of orchids (32) and ovaries of Aralia, Erodium and Pelar-gonium (14, 16).
It would seem to be desirable to emphasize some general aspects of theaction of hormones, native or externally supplied, on the carbohydrate con-tent of the ovaries. In consideration of the relationship between activationof carbohydrate metabolism and growth of the fruit, the following pointsmay be recognized: A significant increase in ovary growth occurred only inpresence of those concentrations of an applied hormone that gave a stimu-lation in starch and reducing sugar accumulation. Growth was closely pro-portional to changes in carbohydrate content. When carbohydrate responseto hormone treatment was reduced, because of the presence of other rapidlydeveloping fruits on the plant, the growth of the ovaries was also reduced.This parallelism suggests a probable interdependence between the growth ofthe fruit and its carbohydrate metabolism.
It would seem logical to assume that the observed carbohydrate changeswere not induced by stimulation of growth but that probably it was theother way around. When a hormone concentration too high to give increasedstimulation of growth was applied, it was still effective in bringing about thecharacteristic changes in carbohydrates. Growth of the ovaries, therefore,probably was affected by the changed carbohydrate metabolism in the tis-sues until the appearance of some limiting factor of a different nature. The
importance in metabolism of other substances such as various formis ofnitrogen compounds and the soil nutrients mnust not be denied however.
The over-all increase of carbohydrate concentration in the growing ovaryappears in complete agreement with the general occurrence of high sugarconcentrations in or near points of high metabolic activity. A similar be-lhavior was found by MARRE (15) to be common to floral buds, young fruits,immature seeds, and root apices, and it is interesting to observe that in allthese organs the removal of the probable centers of auxin production wasfollowed by a clear decrease in sugar concentration.
The mechanism of such an acculmulation of carbohydrates is still anopen problem. In the case of the rapidly growing ovary, one would expecta decrease of the initial concentration as a consequence of water uptakeduring growth and metabolic utilization of carbohydrates for respiration,whichi is noticeably increased after pollination or auxin treatmiient (12, 34,36, 39), and for synthetic purposes. The fact that the opposite condition isfound, i.e., carbohydrate concentration increases, slhows that in the develop-ing ovary a powerful mechlanism is working to accelerate the rate of sugarintake in the growing cells. This mechanism, as far as is known, could oper-ate in two different ways. One seems to consist of the action of the youngfruit in mobilizing reserves in other regions of the plant. The existence ofthis effect of mnobilization at a distance and its correlativ-e naturie waspointed out by MURNEEK (26) and in its enzymatic aspects, by MAIARRE andby MARRE and BARLASSINA (17, 19). But a siml)le mobilization effect, ifactive in increasing the availability of carbohydrates, does not explain theirpreferential accumulation in the growing ovary. In fact, in these tomllatoplants the following concentrations in soluble carbohydrates were found inthe following organs: leaves 0.71%o (fresh weight basis); young stems,0.78%; old stems, 0.92%; fruit pedicels, 0.56%; fruits seven days after polli-nation, 1.45%; fruits seven days after treatmient with p-chlorophenoxyaceticacid, 1.75%. This preferential accumulation in the ovary tissues suggeststhat in these tissues after pollination or auxin treatment the power to obtainsugars from the vascular system is increased. A similar conclusion wasreached by MASKELL and MASON (21) in order to explain the movement ofsugars and nitrogen to the young fruits of cotton. These authors speak ofan increase in permeability to these compounds in the growing cells. Itwould appear preferable to speak of an increase in absorption power ratherthan of an increase of permeability, as plant cells are, as a rule, only veryslightly permeable to sugars, so a rapid uptake of the latter is, withoutdoubt, to be considered an active physiological process.
A good, even if indirect, evidence that auxin increases the absorptionpower towards sugars in the ovary tissues may be found in the fact thatexcised tomato ovaries, cultured in a medium containing sucrose, thus pre-cluding a mobilization effect, react to auxin with an increase in growth (29)and with the initiation of starch synthesis (present evidence), since growthand synthesis of starch appear closely related to an efficient carbohydrate
'MARRE AND LMURNEEK: CARBOHYDRATE METABOI,ISMI IN TOMATO 263
uptake. Another interesting aspect of the changes in carbohydrate metabo-lism in the pollinated or auxin treated ovaries consists of the initial sharpdecrease in sucrose which could be due to a preferential utilization of thissugar to the hexoses for anabolic purposes as well as for respiration. A simi-lar interpretation was proposed by CHRISTIANSEN and THIMANN (5) for thedecrease in sucrose without a decrease in reducing sugars in sections of peastems cultured in a mediumii containing auxin. Though other interpretationssuch as the partial conversion of the disaccharide to reducing sugars arepossible, a preferential utilization of sucrose in the first stages of growthcould be explained by the possibility that it undergoes phosphorolysis, yield-ing highly active hexose phosphate, and by its higher energy content (7,11, 33).
As far as the two most iimaportant features of carbohydrate response,the increase in total carbohydrate concentration and the synthesis of starch,are concerned it is interesting to consider them in connection with the in-crease in respiration, whichl apparently is a normal consequence of pollina-tion and fertilization or auxin treatment. The accumulation of carbohy-drates, as pointed out before, probably involves an increase in the power ofabsorption of sugars in the tissues of the ovary. An increased power ofabsorption requires an increase in expenditure of energy, which must be sup-plied by respiratory metabolism. The rate of respiration appears to becorrelated also with the initiation of starch synthesis in the activatedovaries. As phosphorylase is present in tomato fruit (unpublished results)and seems to be most important for starch synthesis in higher plants (10, 18,38), it appears reasonable to assume its vital role in this case. But phos-phorolytic synthesis of starch implies, as the first step, the phosphorylationof hexoses through a reaction of the type:
Hexose + ATP > Hexose phosphate + ADP.
The production of adenosine triphosphate (ATP) is conditioned by the rateof respiration, and with this reasoning, the main responses of carbohydratemetabolism to pollination and fertilization or auxin treatment appear closelyrelated to the increase in respiration which probably is the basis for theinitiation of ovary activation and fruit development.
SummaryIn the pollinated and fertilized ovaries of the tomato the first stages of
development are accompanied by significant changes in carbohydrate me-tabolism. Two main aspects of these changes are recognizable: (a) Alterna-tions in the equilibrium between the different carbohydrates occur, indicatingmodifications in the enzymatic pattern. Conspicuous features of this aspectare a rapid increase in starch, a simultaneous decrease in sucrose and a pro-gressive rise in reducing sugar concentration. (b) A marked increase of thecapacity to absorb, retain, and concentrate carbohydrates occurs. The totalconcentration of carbohydrates (soluble and insoluble) rose steadily after
pollination but especially after fertilization. The concentration of solublesugars, after a slight initial decrease, soon reached an amount far above thatpresent at anthesis.
Application of the growth regulator, p-chlorophenoxyacetic acid or theethyl ester of indoleacetic acid, to the cut surface of the style of emascu-lated flowers produced effects strikingly similar to those induced by pollina-tion and fertilization including starch synthesis, a decrease of sucrose, andan increase of reducing sugars. Carbohydrate accumulation during the firsttwo days was noticeably higher in treated ovaries which may be related tothe comparatively slow release of auxin after pollination with a gradual andmore prolonged increase after fertilization.
The degree of modification in carbohydrate metabolism in the unpolli-nated ovaries was in proportion to the concentration of the growth regulatorapplied. At the lowest threshold concentration there was a minimal andparallel response for both induction of parthenocarpy and effect on carbo-hydrate metabolism. At the highest concentration used the growth regu-lators, while ineffective for further stimulation of growth of ovaries, stillstimulated accumulation of starch and reducing sugars.
In presence of older developing fruit on the tomato plant, a treatmentwith a growth regulator had a reduced effect on both the changes in carbo-hydrates and the rate of fruit development.
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