Export Organic Materials Developing Fruits of Pea and Its ...HAMILTONANDDAVIES plants. Harvestofshoottipsformeasurementgenerallyconsisted of tissue from the apical bud down to the

Plant Physiol. 86, 0951-09550032-0889/88/86/0951/05/$01 .00/0

Export of Organic Materials from Developing Fruits of Pea andIts Possible Relation to Apical Senescence1

DOUGLAS A. HAMILTON2 AND PETER J. DAVIES*Section of Plant Biology, Cornell University, Ithaca, New York 14853

ABSTRACT

In the G2 line of peas (Pisum sativum L.) senescence and death of theapical bud occurs only in long days (LD) in the presence of fruits. Removalof the fruits prevents apical senescence. One possible reason for the se-nescence-inducing effect of fruit is that the fruits produce a senescence-inducing factor which moves to the apical bud and is responsible for theeffect. For this to be possible there must be a transport mechanism bywhich material may move from the pods to the apex. To examine theextent of fruit export, pods were labeled via photoassimilation of 14CO2beginning 12 days after anthesis. Under LD conditions, 1.14% of labelfixed was transported from the pods with only 10.5% of this found in theapical bud and youngest leaves after 48 hours, the remainder being foundprincipally in other developing fruits and mature leaves. During the onsetof apical senescence, less total label was actually exported to the apicalbud than at other times. In addition, more total export occurred frompods in short days than in LD, with the apical bud receiving a greaterpercentage than in LD. Thus the amount and distribution of export wouldnot seem to support the idea of specific export of targeted senescence-promoting compounds. Girdling of the fruit peduncle did not change thecharacteristics of export suggesting movement via an apoplastic xylempathway.

The reproductive structures of most legume crop species arethe ultimate sink for a large portion of the minerals and assim-ilates transported in the plant. The strength of this sink activityis the major factor determining the harvestable yield of the plant(7). As a result, virtually all of the literature tracing the move-ment of materials during fruit development has concentrated onflow into the fruit, with the developing reproductive structuresoften viewed as passive metabolic sinks. There is, however, alarge body of work detailing the ways in which the presence ofreproductive structures can influence many physiological proc-esses of the plant, including control of leaf photosynthesis (4,20, 29), development of axillary buds (26), development of otherfruits (19, 27), and leaf and whole plant senescence (16, 21, 25).While most of the effects of these reproductive sinks can be

attributed to the removal or alteration of translocated nutrientsand/or plant growth substances, it has been postulated that thesinks may themselves be sources of regulatory substances re-sponsible for these effects (6, 22). For this to be possible theremust be a mechanism by which fruit- or seed-produced com-pounds can move from their source to the target tissue. Thethree possible pathways for export out of the fruit and through

I Supported by Grant No. PCM821659 from the National ScienceFoundation.

2 Present address: Department of Biology, State University of NewYork, Albany, NY 12222.

the fruit stalk are via phloem, xylem, or cell-to-cell movement.Transport by any of these pathways would be expected to becounter to the predominant flow of material towards the devel-oping fruit. However, several workers have shown the existenceof substances translocated out of developing fruits, apparentlyagainst the flow of nutrients (1, 2, 9, 12, 18).

It has recently been shown that the developing fruits of theG2 genetic line of peas export several organic materials whichmove to other parts of the plant (6). The movement of thesecompounds was examined in relation to the photoperiodicallysensitive induction of apical senescence of the G2 line and thepossible production and export of a fruit produced 'senescencefactor.' Exported substances were detected by labeling the pho-tosynthetic pods with 14CO2 or '4C-labeled sucrose and moni-toring the movement of the resulting radioactive metabolites.After 2 to 3 d the bulk of the radioactivity was recovered fromplant metabolic sinks (other pods and the developing shoot tip).This pattern of recovery suggested that transport occurred viathe phloem.The present study was undertaken with the purpose of quan-

tifying the export of organic material from the developing G2pea pods, in relation to the known onset of irreversible fruit-induced apical senescence, in order to ascertain whether the datasupport or oppose the concept that senescence of the apex couldbe caused by fruit-exported substances. Knowledge of the pat-terns of pod export should also aid the goal of maximizing therecoverable quantities to use for identification of possible se-nescence-inducing compounds. In addition, it was hoped that thedata might elucidate the mechanism of observed export from thedeveloping G2 pea pods.

MATERIALS AND METHODS

Plant Material. Pea plants (Pisum sativum L. line G2) weregrown singly in 4.0 L clay or plastic pots filled with peat andvermiculite (1:1 v/v) in a greenhouse at about 20°C. Nodulesformed under these growth conditions. Plants were watered dailyafter germination and were supplied weekly with a completenutrient solution (20:20:20) until transfer to growth chambers 2weeks after germination. Growth chambers were maintained ateither 18 h light/6 h dark (LD)3 or 9 h light/15 h dark (SD)photoperiod. Temperatures were 19°C during the light periodand 17°C during the dark. Lighting was provided by a mixtureof F72T12 cool-white fluorescent (Sylvania, Danvers, MA) andincandescent lamps giving an average intensity of 250 ,uE m-2s- 1 at pot level. Plants were watered daily with a dilute completenutrient solution. Lateral branches and second fruits at a nodewere routinely removed unless noted. The lowest pod on theplant was treated at 12 d after anthesis (fully elongated, one-third full) unless otherwise specified. At this time the pod waslocated at the seventh node from the apical bud in LD-grown

3Abbreviations: LD, long day; SD, short day.

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HAMILTON AND DAVIES

plants. Harvest of shoot tips for measurement generally consistedof tissue from the apical bud down to the most recently fullyexpanded leaf.

"4CO2 Labeling. Labeling was routinely performed 3 to 4 hafter the start of the light period. Fruits to be treated wereenclosed in clear polyethylene bags (80-100 ml) and sealed aroundthe peduncle with tape, and the seal coated with petroleum jelly.This was shown to provide an air-tight seal. To produce the14CO2, 0.5 ml df 0.3 N HCI or 10% perchloric acid was firstinjected into the lowest corner of the bag, then 185 or 370 kBqof NaH14CO3 (specific radioactivity 1.9 GBq mmol- ') in aqueoussolution was injected into the acid through the initial puncturehole. This hole was then quickly sealed with Vaseline and tape.When treatment was stopped the bags were-opened in a strongfume hood to remove any residual 14CO2.

Radioactivity Measurements. Portions of the plants to be countedfor radioactivity were removed and rapidly frozen at - 80°C.These were then either freeze-dried or dried in an oven at 80°C.Samples were combusted in a Packard (Downers Grove, IL) Tri-Carb B306 sample oxidizer without grinding or subsampling. Ifthe sample was too large for a single combustion it was dividedinto two or more samples which were combusted separately andthe recorded radioactivity summed. The radioactivity from thereleased 14CO2 was trapped in Carbsorb II (Packard), correctedfor recovery, and then determined by counting in a Packard Tri-Carb 3255 liquid scintillation spectrometer with quench correc-tion. In other experiments fresh or frozen samples were extractedin 80% (v/v) aqueous methanol and aliquots counted by liquidscintillation spectrometry.

Extraction. Fresh or frozen samples were homogenized in aSorvall Omni-Mixer (Newtown, CT) in 80% (v/v) aqueous meth-anol and extracted overnight while stirring at 4°C. The extractswere filtered and the methanol was removed in vacuo at 35°C.The aqueous fraction was acidified to pH 3 with acetic acid andpartitioned three times against ethyl acetate.

Girdling Experiments. Heat girdling of the peduncle and stemwas accomplished by heating a pair of beaker tongs in a flameuntil red-hot. These were then placed around, but not touching,the plant part to be treated. Girdling was performed about 2 hbefore treatment of the pod.

RESULTSDetermination of Optimum Labeling Time. In earlier experi-

ments looking at export from pods in G2 peas, radioactivity wasrecovered only in the apical bud and other pods on the plant.As a result, in this and several other of these experiments onlythe apical bud and the untreated pods were combusted. Theobject of this particular experiment was to determine the bestradioactivity labeling procedures by finding the optimum lengthof time to supply 14CO2 for maximum fixation and export. Thelowest pod on each plant was treated for various durations todetermine the rate and qiantity of export of material out of thelabeled pod. Pods w'ere labeled by adding 185 kBq of NaH'4CO3to acid and leaving the labeling bag on the pod for periods rangingfrom 30 min to 48 h. The plants were then harvested after a totalof 48 h. The amount of radioactivity recovered from the treatedpod increased for up to 6 h of continuous exposure to the fixedamount of '4CO2, but longer exposure times did not result inrecovery of additional label from the pod (Fig. 1). Recovery ofradioactivity in the apical bud did not increase significantly abovethe level found at 0.5 h of treatment.Time Course of Label Transport within the Plant. To look at

the accumulation of label within the plant, radiolabeling wasattempted in two ways. Pods were either supplied with 370 kBqof '4CO2 for 0.5 h only (at which time the treatment bags wereremoved), or for the entire time before harvest. Plants were thenharvested at various times from 0.5 to 48 h after the start of

oD I In

0~~~~~ ~ ~ ~~~

x~~~~~~~~~~~~~~~0 4-°x

"EXPORTED TO APICAL BUD

0 a

1 3 6 12 24 48TIME (hrs)

FIG. 1. Time course of fLxation and export to the apical bud of radiol-abeled metabolites from "4CO2 supplied to 12 d old pods on pea plantsgrown in LD. Pods were treated for the indicated time periods and thentreated pods and apical buds were harvested after a total of 48 h.

50s

Anfl

0

30.x

0L 20-0

10 -

0O

12T I ME (hrs)

FIG. 2. Time course of appearance of label in the apical bud andnontreated pods of pea plants grown in LD, following labeling of thelowest pod (12 d postanthesis at the seventh node from the apical bud)with "'CO2. Pods were either labeled for 0.5 h only (O, O) or untilharvest at the time indicated (U, *). Time indicates time of harvest.

labeling and the radioactivity exported to nontreated pods andthe apical bud was determined (Fig. 2). As expected, the totalamount fixed by all treated pods stayed constant. The amountexported to the apical bud reached a pleateau very quickly anddid not increase significantly over time, in a pattern similar tothe previous experiment. The amount exported to the nonlabeledpods continued to increase over time, even though no additionallabel was added to the plant. The rapidity with which the labelappeared in other parts of the plant suggested that we try evenshorter labeling times. It was found that even a 10 min labelingperiod before harvest allowed recovery of 14C-compounds trans-ported to other parts of the plant (Fig. 3).The increase with time of recoverable radioactivity from the

untreated pods could arise either by preferential export from thelabeled pod (the amount in the apical bud did not significantlyincrease), or by remobilization of label from some other initialsink, possibly the leaves. To examine the possibility of export toparts of the plant other than sinks, all parts were harvested 42h after a 6 h labeling period and distribution of 14C in the plantwas determined (Table 1). Pods on individual plants were foundto export an average of 1.14% of all the "4C fixed by the pod inLD, and an average of 3.72% in SD. On plants grown in LDthe pattern of distribution was found to be Other Pods> Leaves- Apical bud > Stems = Roots. In SD this distribution was

* Pods. bog onO Pods. bog off at 1/2 hr.* Apicol bud. bag onO Ap1col bud. bog off ot 1/2 hr.

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FRUIT EXPORT AND SENESCENCE

(T)~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~1

x2

L A UNTREATED PODS

0

0 1 0 20 30 40 c 60

TIME (min)

FIG. 3. Recovery of label in the apical bud and untreated pods duringthe first hour after treatment as in Figure 2. Treatment bag was left onuntil harvest.

altered such that Leaves Other Pods > Apical buds > Stems

= Roots. Of the label remaining in the treated fruit after 48 happroximately 82% remained in the carpel, and 5 and 13% wererecovered from the seed coat and embryo, respectively. In thenontreated pods an average of 20% of the recovered label wasfound in the carpel, while 51 and 29% were found in the seedcoat and embryo.Export versus Pod Age. To determine if there is a correlation

between the amount of pod export and the onset of senesence,the lowest pods of plants grown under LD were treated with'4C02 for 6 h at ages from 6 to 30 d after anthesis. After a totalof 48 h, apical buds and other pods were harvested, combusted,and counted. The amount of fixation in the treated pod variedwidely among individual plants. The average amount of fixationof 14C by the treated pod changed little with age except for a

period of increased fixation between d 16 and 22 after anthesis(Fig. 4A). Total export to other pods and the apical bud was

initially low (d 6-14) but increased to a maximum around d 20-22 (Fig. 4B). The percent of the exported label which wentspecifically to the apical bud declined steadily throughout thetreatment period (Fig. 4C).

Percentage of Export Partitioning into Ethyl Acetate. Earlierwork had suggested that the fraction of labeled material re-

covered from apical buds which partitioned into ethyl acetatewas higher when exported from younger labeled pods (TJ Gian-fagna, personal communication). To examine this, pods of ages6 to 16 d after anthesis were labeled and the other pods andapical bud were extracted as described. It was found that thepercentage of label moving into the acidic ethyl acetate fraction

peaked at around 37% on d 8 to 10 in the extracted apical buds(Fig. 5). Label recovered from the pods mostly remained in theaqueous fraction with less than 6% partitioning into the ethylacetate fraction.

Girdling Experinents. Peduncles of pods to be treated were-heat-girdled as described and then the pods treated with '4CO0as usual. It was found that heat-girdling had little effect on theamount or distribution of label throughout the plant (Table I).To determine if the bag we used for labeling produced an artificialatmosphere which resulted in artifactual export of material inthe xylem, '4C-sucrose was applied to the surface of the podwithout a surrounding bag. Export of the '4C-sucrose occurredthrough a heat-girdled peduncle (data not shown). Heat-girdlingof the main stem above and below the treated pod also resultedin little change in the export of label, similar to results publishedby Bennett et al. (2).

DISCUSSION

During their early growth, the photosynthetic carpels of peasact as sinks for metabolites, but are known to decrease in dryweight during the latter part of development (5). Studies of car-pel-seed interactions have shown that the material lost by thecarpel at maturity is largely exported to the enclosed ovules,indicating that carpels are able to mobilize and export compoundsin response to developmental cues. Carbon fixed by the carpelderives primarily from CO. respired by the ovules, but some newcarbon is assimilated from the atmosphere. We have utilizedthese phenomena to radiolabel the-pod and the enclosed seedswith '4C, and then have monitored the subsequent flow of ra-dioactive metabolites around the plant.

14CO2 fixation varied with age of the pods peaking from 14 to24 d after anthesis. While the net total fixation by pea pods isnever positive during the life of the fruit (diurnal assimilation ofcarbon never outweighs respiratory losses at night [5]), net fix-ation during the light is positive for the middle part of pod de-velopment, and net CO, uptake in P. sativum has been reportedto occur between d 15 and d 22 (4). This was attributed todecreased CO2 loss during that period, rather than increasedphotosynthesis. The early phase of CO2 loss coincides with therapid growth of the pod, and the later phase with seed growth.However, pod photosynthetic rates have been shown to changeduring the life of the pod reaching maximum rates soon afterfull elongation (8) so this might also contribute to the observedchange in fixation capacity.

In these experiments, as well as others involving pod fixationof 14CO2 from enclosed atmospheres, some of the provided la-beled carbon was not assimilated (cf. 6, 17, 18). Lovell and Lovell(17) reported only an average of 634 cpm detected in pods onthe plant treated with 5 ,uCi each for 4 h. While net daytimeCO2 assimilation is reported to be positive for much of the life

Table I. Distribution of Exported Label to Plant Parts Harvested 42 h after Allowing a 12-d-old Pod toPhotosynthesize for 6 h in '4CO2

The data are the average of 5 plants each treatment.

% of Total Fixed Label (% of Total Exported)Plant Part LD SD Peduncle

Girdled (LD)% ± SE

Apical bud 0.12 + 0.04 (10.5) 0.59 t 0.12 (15.8) 0.26 + 0.07 (20.5)Nonlabeled pods 0.73 ± 0.13 (64.0) 1.19 + 0.20 (32.0) 0.80 ± 0.11 (63.0)Leaves 0.20 ± 0.04 (17.5) 1.31 ± 0.22 (35.2) 0.16 ± 0.04 (12.6)

Proximal 0.13 t 0.03 (11.4) 0.97 ± 0.13 (26.1)Distal 0.07 ± 0.03 (6.1) 0.34 ± 0.07 (9.1)

Stems 0.06 ± 0.04 (5.3) 0.33 ± 0.12 (8.9) 0.03 ± 0.02 (2.4)Roots 0.03 ± 0.05 (2.6) 0.30 ± 0.23 (8.1) 0.02 ± 0.02 (1.6)Total 1.14 + 0.40 3.72 + 0.77 1.27 ± 0.18

953

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HAMILTON AND DAVIES

A

ID0

x

ax0

B TOTAL EXPORTED

6

x

>;4/0-

0

2-

z ~ ~~~~/L

C PERCENTAGE OF EX\RECOVERED IN API

30iZz

L 20 sL-

010

6 10 14 18 22DAYS AFTER ANTHESIS

FIG. 4. Time course of total fixation (A), total expoicent exported to the apical bud (C), in pea plants groifunction of the age of the treated pod. Pods were treatec6 h and the plants harvested after 48 h.

of the pod, this lack of complete fixation of all ththe treatment atmosphere suggests dilution of thepired CO2 especially during the early and late pdevelopment. Another possibility is ineffective parising from inadequate lighting of the pod duringperhaps from closure of carpel stomata by elevatlin the chambers; however, Harvey et al. (8) found nfby carpels increased at higher CO2 concentrations.have been shown to have net rates of atmospheric c;much less than those of leaves (8), especially duhigh reassimilation of respired CO2. Thus, decrealution might explain the increased fixation noted iments during the period 14 to 22 d after anthesis.When various treatment times with a single amoi

14CO2 were tested, the amount of '4C fixed increa6 h, at which time about 75% of the '4CO2 had bethe fixation and loss of 14CO2 must have come intoamount of radioactivity in the other pods to whicexported rose initially rapidly and then more slow

6 10 14 6 10 14DAYS AFTER ANTHESIS

FIG. 5. Percent of exported radiolabel partitioning into ethyl acetatefrom acidic extracts of the apical bud and untreated pods of pea plantsgrown in LD, as a function of the age of the 14CO2-treated pod. Podswere treated with '4CO2 for 6 h and the plants harvested after 48 h.

| However, the amount of 14C in the apical bud rose significantlyfor only about 30 min, and thereafter rose only slightly. It ispossible that the loss of 14CO2, resulting from rapid metabolismin the developing tissues of the apical bud, comes into equilib-rium with the small supply of '4C-labeled materials faster thanoccurs in the other pods, which have a more self-contained car-

bon economy.

PORT In the G2 genetic line of peas, senescence and death of theCAL BUD apex require both LD and the presence of seeds (25), and it has

been postulated that a senescence factor produced by the fruitsof these plants might be responsible for this phenomenon (6).Earlier studies of the onset of senescence in G2 pea have shownthat apical senescence symptoms appear about 11 d after anthesisof the first flower while apparent death of the apex occurs atabout 18 d (3). A senescence-inducing compound produced bydeveloping pods might therefore be expected to be exported priorto or during that time. The data showing quantitative exportoccurring from pods 6 to 30 d after anthesis indicate relativelylittle export from 6 to 14 d but increased levels thereafter, peak-ing around d 20 to 22 (Fig. 4B). The percentage of exported

_ _ label recovered from the apical bud is higher when the pods are

26 30 younger (and the plants are commensurately smaller), but thelarge increase in total export exhibited by older pods producesan actual net increase in amount of labeled products moving to

rt (B) and per- the apical bud in older plants even though the apices are becom-wn in LD, as a ing senescent. This finding does not rule out a compositionalwith 'C02 for change in the export between younger and older pods; indeed,

the label from apical bud extracts that partitions into ethyl acetatechanges quantitatively with the age of the pod (Fig. 5). However,

e '4CO2 from it does show that a simple increase in the bulk quantity of ex-label by res- ported material cannot be responsible for the observed senes-

eriods of pod cence effect.hotosynthesis Long days are also necessary to induce apical senescence.treatment, or However, in the present study the total amount of material ex-ed CO2 levels ported from developing pods and the amount going to the apicalet CO2 uptake bud was found to be less in LD than in SD. While the reasonLegume pods for this difference is not clear, it again indicates that the totalarbon fixation export pattern does not support the idea of fruit-derived senes-iring times of cence-promoting compounds. Again, however, this finding doessed CO2 evo- not rule out a compositional change in the exported materialin our experi- between LD and SD. The possibility that a promotive factor

could be produced and exported by pods in SD is not likely,unt of labeled given the fact that continued apical growth occurs in both LDised for up to and SD in the absence of pods.-en fixed, and The distribution of exported radioactivity determined in thisbalance. The study is in partial agreement with that previously observed (6).Theh the '4C was ability of the pods to export material produced from photoas-'ly up to 48 h. similated 14CO2 was clearly shown. However, in this study, export

T

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FRUIT EXPORT AND SENESCENCE

occurred not only to sink tissue but was recovered in matureexporting leaves as well. The previous work was based on ra-dioactive counting of punched leaf discs collected 2 to 3 d eitherafter 14C-labeled sucrose was injected into the pod cavity, orafter the pod was allowed to photosynthesize in the presence of14CO0. The apparent discrepancy between the data presented inthis paper and those from the earlier work is most likely due tothe shorter incubation period and more accurate oxidizing tech-niques employed here. Tissue punches would be likely to showradioactivity only in those tissues with the highest specific activ-ity, namely, young leaves and pods.

This recovery of radioactivity from mature exporting leavesimplies either bidirectional phloem transport in the pedunclesand petioles, or movement by some alternate pathway. Recoveryof radioactivity in the plant after girdling the peduncle of thetreated pod points to flow in the girdled area either being throughthe dead cell layer, through the nonliving xylem, or both. Theseobservations are consistent with the finding of Bennett et al. (2)who applied ['4C]sucrose to the surgically opened seed cups ofsoybean, and determined that 0.1 to 0.5% of the applied 14C wasexported to other parts of the plant after 4 h. Of the total amountexported in Bennett et al. 's experiments 80% was recovered fromleaves, 5% from petioles, 11% from internodes, and 4% fromother fruits. Roots were not sampled. The experiment was re-peated after steam girdling of the main stem just above and belowthe treated pod with little change in the amount or distributionof the recovered radioactivity. The lack of a change in the flowof exported material prompted them to conclude that normalexport must most likely be through the xylem. The authors sug-gested that the mechanism by which reverse xylem flow occursmight be a return of excess water delivered to the developingseeds by the phloem.

Several other studies calculating the transport of nutrients todeveloping reproductive structures have suggested that excessamounts of N (15, 24), minerals (19, 30), or water (11, 23, 28)delivered to the seeds might be returned to the parent plant viathe xylem. The most recent of these studies (23) has employedthe application of 3H2O to a developing legume (Vigna ungui-culata) fruit and noted the export of radioactivity back into thefruit peduncle. Similarly, feeding of the apoplast-mobile dye acidfuschin to the cut distal end of fruits showed movement out ofthe pod into the peduncle, and in some cases into the subtendingleaf.One possible mechanism suggested for reverse flow in the

legume fruit peduncles is that an excess of water delivered tothe fruit via the phloem presumably produces a small positivereverse pressure on the xylem (23). However, this would be incontradiction with the results of the girdling experiments pre-sented here and by Bennett et al. (2). Girdling of the peduncleshould terminate water delivery by the phloem and any positivepressure formed in the xylem should dissipate quickly. Thus, thismechanism cannot account for results indicating continued ex-port from 2 h (this report) to 16 h (2) after girdling.Another possible explanation might be found in the work of

Klepper (13). In this study of diurnal shrinkage in the pear fruitshe concluded that water loss (as measured by fruit shrinkage)correlated to the midday period when the water potential of thetranspiring leaves fell far below that of the fruit. Thus, the drivingforce for the movement of water out of fruits appeared to be thewater potential difference between the leaves and fruits duringperiods of heavy foliar transpiration. Diurnal shrinkage and waterloss have been shown for a variety of fruit (14) and could rep-resent a plausible mechanism bv which materials could leavefruits via the xylem. This type of mass flow in the xylem wouldbe nonselective, but would account for the results presented inthis paper, and could deliver metabolically significant amountsof materials to other parts of the plant. Research to determine

if this might be the mechanism accounting for the export ob-served from G2 pea pods is reported in the following paper.

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22. NOODEN LD, AC LEOPOLD 1978 Phytohormones and the endogenous regu-lation of senescence and abscission. In DS Letham. PB Goodwin. TJV Hlig-gins. eds, Phytohormones and Related Compounds-A ComprehensiveTreatise, Vol II. Elsevier/North Holland Biomedical Press. Amsterdam. pp329-369

23. PATE JS. MB PEOPLES, AJE VAN BEL. J Kuo, CA ATKINS 1985 Diut-nalwater balance of the cowpea fruit. Plant Physiol 77: 148- 156

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