abiscisao e raleio de frutos jovens bangerth

8/12/2019 Abiscisao e Raleio de Frutos Jovens Bangerth

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Plant Growth Regulation 31: 4359, 2000. 2000Kluwer Academic Publishers. Printed in the Netherlands.

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Abscission and thinning of young fruit and their regulation by planthormones and bioregulators

F. BangerthInstitut fr Obst-, Gemse- und Weinbau, Universitt Hohenheim, 70593 Stuttgart, Germany

Key words:auxin transport, correlative abscission, mode of action of bioregulators, thinning of fruit

Abstract

Natural abscission of young fruit and its regulation by plant hormones is considered and compared to the generallyaccepted model of senescence triggered abscission of, for example, leaves or mature fruit. It is concluded thatabscission of young fruit cannot be explained by this model. Alternatively, it is suggested that the senescence

triggered initial step in the classical abscission model should be replaced by a correlatively triggered step. Polarbasipetal IAA transport with its autostimulation and autoinhibition components is the main regulating signal in thiscorrelative acting system and replaces ethylene as the initial driving force from the senescence triggered model.Results supporting this model are presented and tested against existing results from the literature. Finally, thishypothesis is tested as a possible explanation of the mode of action of some thinning chemicals or bioregulators.It is speculated how a thinning chemical should be designed to function in a more reliable way, at least as far as itsinterference with the endogenous hormone system is concerned.

Abbreviations: ACC = 1-aminocyclopropane-1-carboxylic acid; AVG = aminoethoxyvinylglycine; AZ = abscissionzone; IAA = Indolylacetic acid; KF = king fruit; LF = lateral fruit

1. Introduction

Many fruit tree species bear an abundance of flowerswhich, even after poor pollination conditions, producea surplus of fruit that the tree is unable to support.Possibly in anticipation of this, many fruit trees havedeveloped a self regulatory-mechanism whereby theyshed part of their fruit load at a certain early period(e.g. during June drop in the Northern hemisphere).This ensures that more fruit are not retained by thetree than can be supported under prevailing environ-mental conditions. From a horticultural point of view,

this self-regulatory mechanism may be too strong forfruit species, such as mango, avocado etc., leadingto low fruit load and yield. With some other fruitcrops set is more or less sufficient, as for examplesome Citrus spec. (Monselise et al., 1981), whilst withmost of the temperature fruit group, as e.g. apple,pear, peach, plums, the self-regulatory mechanism isentirely insufficient to guarantee the required quality

standards. This unsatisfactory degree of self regula-tion in the latter group of fruit trees has a number ofdisadvantages, of which two are most serious:

low and often unacceptable market quality (seeLink, 1986 and this Vol.)

inhibition of flower bud induction, causing severealternate bearing (see Tromp, this Vol.)

To overcome these shortcomings, flower- or fruit-thinning is an efficient method and has become neces-sary in modern fruit production. However, in mostdeveloped countries, manual thinning is becomingmore and more uneconomical, leaving thinning with

bioregulators (PGR as well as endogenous plant hor-mones) as the only presently available alternative.Thinning with bioregulators is considered as

an amplification of the natural self-regulatory fruitabscission process. Knowing more precisely aboutthe mechanisms underlying this process of naturalfruit abscission would help to improve current thin-ning practice. Most bioregulators presently in use as


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chemical thinners are either unsatisfactory or unreli-able or both with regard to their thinning efficiency(see Williams, 1979 and Wertheim, this Vol., forliterature). It is, therefore, even more necessary tohave a better understanding of the processes leadingto abscission of young fruit in order to design better

thinning strategies.

2. Current ideas about the abscission of young

fruit

Presently there are two main hypotheses to explain theabscission of young fruit:

insufficient supply of assimilate to fruitlets asa result of limited assimilate production and/orallocation to the fruit

a regulatory hormonal mechanism by which the

plant safeguards selected fruit from assimilate lim-ited growth later in the season

There is support for the involvement of assimilateshortage in the process of abscission of young fruitfor a number of species. Even for some evergreen cit-rus species, it is claimed that assimilate shortage orlimitation in carbohydrate allocation may occur dur-ing certain periods of fruit development (Bustan et al.,1995, Goldschmidt and Koch, 1996). On the otherhand, Guardiola et al. (1984), and Ruiz and Guar-diola (1994), report higher carbohydrate reserves inabscising as compared to non-abscising citrus fruit,

casting doubt on the assimilate hypothesis. Theseauthors favour instead, a lack of sink demand asthe explanation. For apple and peach fruit, the evid-ence for assimilate limitation as one of the reasonsfor fruit abscission is stronger (Lakso 1994, Ber-ter 1985, Berter and Droz 1991, Stopar 1998).Again, however, carbohydrate analyses of abscisingversus non-abscising apple fruit revealed no evidencethat carbohydrate limitation or starvation could be acausal factor in abscission (Abruzzese et al. 1995).A brief summary of this unresolved issue would bethat there is no clear evidence that assimilate short-age is a direct cause of fruitlet abscission. The secondhypothesis mentioned above may thus be more relev-ant and will be treated preferentially thereafter. Twophysiological processes are critical in understandinghormonally-regulated abscission of young fruit:

the activation of an abscission zone (AZ) of a par-ticular fruit, which is the decisive event in thinningas well as in abscission (see Bonghiet al., this Vol.)

hormonally controlled dominance phenomenaamong fruit and between fruit and shoot(Bangerth, 1989)

3. The presently accepted model of abscission

zone activation

The activation of the AZ by endogenous planthormones has been intensively investigated in thepast. The model describing this process was mainlydeveloped on explants by Addicott (1982), Morgan(1984), Osborne and McManus (1984) and Osborne(1989) and has only been modified subsequently (Sex-ton 1994). It implies that auxin, specifically IAA,produced by the subtending leaf blade, is translocateddown the petiole where it retards AZ activation. Thephysiological effect of IAA in this process is to reducethe sensitivity of the AZ to ethylene (van Doorn andStead 1997). At low IAA concentration, ethylene thenactivates this usually preformed tissue, resulting inabscission. In this model, ethylene is, therefore, theprimary signal driving the abscission process.

Significant progress has been made recently inunderstanding the process of AZ activation and thesignal transduction pathway following the recognitionof ethylene by a receptor in the AZ (see Bonghi etal., this Vol.). This aspect of AZ activation by ethyl-ene will, therefore, not be discussed further here.In contrast to this final ethylene regulated part ofthe abscission process, the desensitising of the AZ

caused by IAA is little understood. IAA is consideredthe main factor in controlling the sensitivity of the AZto ethylene, but it may not be the only one. Thereare periods during fruit development when the AZ isinsensitive to ethylene even though IAA transport tothese AZ during that period may be low. If more thanone AZ is present at a pedicel, e.g. in citrus or peach,usually only one of them is sensitive at a time (Goren1993). The fact that the AZ can become sensitive toethylene again, as e.g. during the pre-harvest period(pre-harvest drop), suggests developmental controlapart from auxin regulation of this process.

In the above-mentioned model, it is the beginningof the senescence process in the leaf blade or ripeningfruit which initiates the production of elevated levelsof ethylene. This then reduces production or stimu-lates metabolism of auxin (Riov et al. 1982), but moreimportantly, diminishes basipolar transport of IAA tothe AZ (Beyer and Morgan 1971), possibly by redu-cing IAA export carriers (Suttle 1988). As a result,


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the sensitivity of that tissue to ethylene increases (seeabove) and the process of abscission by an increasein hydrolytic enzymes and finally cell separation isinitiated (Osborne 1989, Sexton 1994). The questionarises as to whether the leaf explant model is valid forthe abscission of intact reproductive organs as well. In

this respect, the few documented examples are restric-ted to flowers (Wien et al. 1989, del Campillo andBennett 1996, van Doorn and Stead 1997) and maturefruit during pre-harvest drop (Kasha 1989, Brady andSpiers 1991, Goren 1993). The abscission of youngvigorously-growing fruit, however, certainly cannotbe compared with senescing leaves or ripening fruitand the regulation of their abscission at particular peri-ods may be significantly different. A hypothesis willbe developed below which may better describe theabscission of young fruit than the leaf explant model.The intention is to evaluate this hypothesis by resultspresented here and by reference to published literature.

4. A new hypothesis describing the loss of young

fruit by correlatively driven abscission (CDA)

Although some fundamental ideas of the followinghypothesis have been published previously (Bangerth1989), correlative dominance rather than CDA wasthe main subject considered. Here, CDA will be theexclusive topic although these two hypotheses areclosely related.

In the leaf explant model, polar auxin transport,

the system preventing activation of the AZ by ethyl-ene, is reduced as soon as the distal organ startsto senesce and produces higher amounts of ethyl-ene. However, young fruit start to senescence onlyafter they are already determined to drop by a pre-ceding correlative event (see below). Similarly, anincrease in ethylene evolution is not observed forthe very early stages of abscission. Also, a decreasein auxin transport to the abscission zone, character-istic of senescent leaves (see above), is not observedwith young fruit. To the contrary, auxin export fromyoung apple fruit and transport to the AZ generally

increases shortly after fruit set considerably (Gruberand Bangerth 1990), whereas ethylene productiondrops at the same time to a low level (Blanpied 1972,Ebert and Bangerth 1985, Miller et al. 1988). There-fore, according to the leaf explant model, these fruitshould not abscise. Nonetheless, some of them doand this can be explained by a hypothesis developedearlier (Bangerth 1989, 1997). This hypothesis substi-

tutes senescence-controlled by correlatively-regulatedabscission of young fruit. Since the high IAA exportof young fruit would not allow sensitisation and activ-ation of the AZ by ethylene, a mechanism has tobe found which explains the down-regulation ofthe auxin export of those fruit which are eventually

destined to abscise. This is primarily achieved bya correlative dominance effect of adjacent fruit ornearby shoot tips. In a spur cluster of apple fruit, forexample, it is the fruit that is set and develops first(usually the terminal king fruit, KF) that dominatesover later developing lateral fruit (LF) and causes mostof them to abscise (Figure 1). Even among the lateralfruit a ranking of dominance exists, although not asgreat as between KF and LF. In other fruit species,the spatial arrangement of the dominating fruit may bedifferent. In citrus, for example, it is again the terminalflower which opens first, but the ranking of the lateralflowers follows a more complex pattern (Spiegel-Roy

and Goldschmidt 1996) and in peach it is the distalfruit on a shootas compared to the proximal one whichdominates (Spencer and Couvillon 1975). Almostalways, however, it is the fruit that sets first whichdominates later developing fruit and for this reason theterm primigenic dominance was used to characterisethis phenomenon (Bangerth 1989). Dominated fruitinitially show a reduced growth rate and, decisively, alower auxin export (Figure 1). Both characteristics dis-appear as soon as the dominant fruit(s)/shoot tips areremoved (Gruber and Bangerth 1990 and Figure 2), atleast as long as not a point of no return has been

reached. The measured difference in auxin export ofdominating versus dominated fruit can be explainedas follows:

IAA is able to stimulate its own basipolar transport(autostimulation hypothesis; see Goldsmith 1977, andWarren Wilson et al. 1988 for literature). At the junc-tion where the strong polar IAA transport pathwayof a dominant fruit meets the weaker IAA pathway ofa dominated fruit the latter is inhibited by the former(Bangerth 1989, Li and Bangerth 1999). This autoin-hibition of auxin transport at junctions is illustratedin Figure 1 and can be experimentally verified byreplacing the dominant king fruit by the applicationof an auxin such as NAA or 2, 4-D (Bangerth 1997).The degree of dominance of one fruit over another ascompared to a dominated fruit largely depends on:

the different (in hours or days) in fruit set betweendominant and dominated fruit (Stephenson 1981,Stephenson et al. 1988, Gruber and Bangerth1990).


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the number of seeds/fruit (Stephenson 1981,Bangerth et al. 1989). Seed number is an import-ant determinantof auxin export of a particular fruit(Callejas and Bangerth 1997)

the proximity and vigour of nearby vegetativeshoot tips (e.g. the bourse shoot, see Gruber and

Bangerth 1990) the number of fruits in a cluster, because there are

also dominance effects of those lateral fruit whichstarted their development earlier than other lateralfruit (see Figure 1)All these dominance effects are cumulatively

reflected in the IAA export rates of a particular fruit.Thus, IAA export out of a young fruit and transportthrough the AZ is regulated by a number of correl-atively acting factors from nearby organs which dif-ferentially affect autostimulation and autoinhibition ofthat transport system according to their ranking in thedominance hierarchy. The final effect of the resultantcorrelative dominance on auxin transport autoinhib-ition of dominated fruit leads to a situation wherethe auxin transport of the most dominated fruit fallsbelow a certain threshold value at which stage it nolonger inhibits sensitisation and activation of the AZby ethylene, which then results in the shedding of thatfruit.

A further interesting aspect that follows from thiscorrelative process is that the more fruit that arepresent in a cluster, the stronger is the autoinhibitionof auxin transport on the most dominated fruit in thatcluster and the higher the probability that this fruit

will be shed. On the other hand, when very few fruitare present in the cluster there will be little correlat-ive inhibition, resulting in a low rate of abscission.In this way the plant/fruit may anticipate the pos-sibility of assimilate limitation where there is a heavyfruit load (high initial fruit set) before such a shortageeven exists and shed fruit heavily during the specificfruit-fall periods. The self-regulatory process men-tioned above could, therefore, also be explained bythe hypothesis of correlative abscission. Also, thecommon observation that chemical thinning is easieron trees bearing a heavy fruit load can be correlated

to this mechanism. With a larger number of fruit, thedominance effect is greater and the thinning biore-gulator only needs to reduce IAA transport of themost dominated fruit (e.g. the most basal fruit in Fig-ure 1) only by a small amount to reach the thresholdvalue mentioned above. Selective thinning, mean-ing that most thinning-bioregulators remove the mostdominated fruit first (Link 1968), would be a logical

consequence of that hypothesis. It should be men-tioned, however, that some potent thinning chemicalsare non-selective thinners (see Green et al., 1992 forliterature)

Summarising the above hypothesis, it is thecorrelatively-driven abscission which replaces

senescence-driven abscission of the classicalabscission model by an interorgan correlativesignalling. The latter results in a down regulation ofIAA transport by autoinhibition at junctions. Fromthere on, the process of abscission most certainlyproceeds in a fashion similar to that described abovefor the classical leaf explant model.

5. Possible physiological mechanisms involved in

auxin transport autoinhibition at junctions

Polar basipetal transport of IAA is claimed to res-ult from localised specific IAA export carriers ofspecialised cells near to the sieve tubes (Goldsmith1977, Lomax et al. 1995). Thus, IAA is exportedfrom these cells at their basal sites, taken up againby the next cell, exported at their basal end and soon (Figure 3). These export carriers are highly reg-ulated, e.g. by a number of so-called synthetic IAAtransport inhibitors such as TIBA, NPA and relatedsubstances, morphactins etc. These substances canreduce or even block the function of IAA exportcarriers and thus polar auxin transport. Theoreticalconsiderations led Hertel (1983) to speculate that the

presence and function of these synthetic IAA trans-port inhibitors can logically be explained only by theassumption that naturally occurring endogenous auxintransport inhibitors use the same receptor sites as thesynthetic inhibitors (see e.g. Jacobs and Rubery 1988).Besides being regulated by these transport inhibit-ors the turn-over rate of the export carriers seems tobe fairly rapid and affected by other plant hormones.Suttle (1988, 1991) and Yoon and Kang (1992) wereable to demonstrate that the well known IAA-transportinhibition caused by ethylene is a result of a reduc-tion of these IAA export carriers, possibly caused by a

decrease in their synthesis and/or stimulation of theirdegradation. It must be admitted, however, that a con-siderable number of other possibilities are availableto explain IAA-autoinhibition beside the alreadymentioned hypothetical endogenous transport inhibit-ors and the turn-over rate of export carriers. Amongthem are alterations in the concentration/affinity ofauxin-import carriers (Hertel 1983). These carriers are


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Figure 1. Scheme of an apple fruit cluster. Numbers outside the fruit represent the ranking in PD hierarchy. Numbers inside the fruit give ngIAA export per 20h standard error and, as an example, the number of seeds. Note the influence of PD and the number of seeds on IAA export.All figures of IAA export, including the one of the bourse shoot tip, are from cv. Jonagold and were taken 25 days after full bloom.- - : polar IAA transport channels

: Indicates junctions where IAA-transport autoinhibition occursAZ : abscission zone

partly responsible for the differential uptake of vari-ous auxins (Delbarre et al. 1996) and, therefore, theirvarying polar transport rates. Further experimentationis urgently needed to sort out the more important stepsinvolved in this complex transport system. In the con-text of correlatively driven abscission it will be essen-tial to elucidate particularly those steps in this complex

transport system which are sensitive to IAA-transportautoinhibition (see Li and Bangerth 1999).Besides these uncertainties about the physiolo-

gical mechanisms responsible for polar auxin transportthere are other unresolved questions which need to beinvestigated in order to gain a better understandingof correlative abscission. It has long been known that

the application of IAA to the basal end of an explantdoes not decrease but, to the contrary, considerablyincreases AZ activation and may even induce sec-ondary AZ (Pierik 1980, Warren Wilson et al. 1986,1988). Autoinhibition at junctions could be an explan-ation for this surprising result, because, in analogy,the concentration of IAA at the basal side of a dom-

inated fruit should be increased, at least transiently,because of the stagnation in auxin transport at thejunction with the strong IAA export of a dominantfruit. Higher concentrations of IAA in AZ of abscisingversus non-abscising cotton-and citrus fruitlets (Guinnand Brummett 1987, Okuda and Hirabayashi 1998), inspite of the reduced IAA transport out of these fruit,


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Figure 2. Photographs of two apple fruit clusters.A: before June drop. The dominance of the KF (king fruit) is clearly visible. Two of the LF (lateral fruit) will eventually drop (note yellowcolour of their pedicells).B: A fruit cluster where the KF had been removed a few days after full bloom. Four of the original five LF are still present shortly after Junedrop and grow vigorously.

may also be the result of such a stagnation in IAAtransport. Results such as these raises the question

as to whether it is the concentration of IAA in theAZ or the auxin flow through it which determines itsactivation.

6. Does the hypothesis of correlative abscission

fit experimentally obtained results?

If the above hypothesis for correlative abscissiondescribes abscission of young fruit better than theexisting leaf explant model, one should be able to testits validity by comparing it with results already avail-able in the literature or design experiments to evaluateit.

Initial work to investigate the endogenous regu-lation of fruit set or abscission mainly consideredchanges in the concentration of endogenous extract-able hormones in seeds/fruits to be one of the trigger-ing events which then initiates senescence, increasedethylene production, and fruit drop (Luckwill 1953 a

& b pioneered this area of research). Even though anumber of results could be obtained which seemed to

be closely related to fruit abscission, none could beclosely associated to the abscission process of youngfruit (see Dennis this Volume, for literature). From allthe determinations of hormone concentrations, onlyABA in a few instances could possibly be consideredas an abscission accelerating constituent. At present, itis not clear whether ABA is able to directly stimulatefruit drop, as Cooper and Horanic (1973) and Bangerth(1975) demonstrated for fruit explants and which Juanand Huang (1988) suggest for intact litchi fruit abscis-sion and ABA accumulation. Alternatively, a higherABA concentration may stimulate ethylene productionas shown by Jackson and Osborne (1970) for explants.Guinn and Brummet (1987), and more recently Talonet al. (1997), found a close relationship between ABAconcentration and abscission of cotton and citrus fruit.The later authors suggest a stimulating effect of ABAon ACC- and ethylene biosynthesis, with the latter onebeing responsible for the increased fruit drop. Whetherthe effect of ABA is direct (Juan and Huang 1988)


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Table 1. Concentration of ABA in seed and peri-carp tissue of Elstar apple fruit after treatment withthe IAA-transport inhibitors NPA and NPA+Ethephon.Samples were taken 15 and 22 days after treatment(DAT).

Treatment Tissue ABA (ng/g dry wt.)

15 DAT 22 DAT

Control Seeds 492 1068

NPA (100 mg/l) 982 1079

NPA + Ethephon 1812 986

(100 + 300 mg/l)

Control Pericarp 240 250

NPA 407 192

NPA + Ethephon 579 406

or indirect (Talon 1997), in both cases ABA must beassumed to be a trigger for fruit abscission. As withmost experimental results based only on correlations,the assumption of a causal effect should be consideredwith caution. In one recent experiment (Httche andBangerth, in prep.), a sharp and rapid drop in ABAconcentration in apple fruit after their release fromdominance by removal of the KF was found. Thiswas probably related to the interruption of the IAA-transport autoinhibition by this manipulation. This

conclusion is based on the observation that a strongIAA transport inhibition produced by spraying NPAwith or without Ethrel, strongly increased ABA intreated fruit (Table 1). These two experiments suggestthat the observed increase in ABA may be more theresult of a disturbed auxin transport than the cause ofabscission.

Other endogenous plant hormones, beside ABA,have been related to fruit abscission but with similarproblems to those discussed above for ABA (Den-nis 1986 and this Vol.). An experimental methoddescribed by Kondo and Takahashi (1987) and Kondo

(1989) might help to better discriminate betweencause and effect with endogenous hormones. Placingapple trees into high ( 15 ) or low ( 10 ) nighttemperatures caused considerable differences in fruitabscission in their experiments, with the high tem-perature fruit being considerably more susceptibleto abscission. Conducting similar experiments, Tukey(1956, 1960) observed that high night temperatures

(e.g. 22.2 C) stimulated fruit growth more than lownight temperatures (e.g. 8.8 C). These results wereconfirmed by us in four-year experiments with the cv.Golden Delicious but results were less clear for Elstarapple trees (Table 2). This experimental set up allowsthe study of increased abscission rates at high temper-

atures in spite of the higher growth rate of these fruit.This is entirely opposite to what has been observedin almost all other experiments so far. The advantageof this kind of experiment is that it helps to eliminatethe generally recognised crucial negative correlationbetween growth rate and abscission rate of fruit (Zuc-coni et al. 1978) and the argument that the hormonalchanges usually associated with the abscission process(e.g. reduced IAA transport) are mainly the result ofthis diminished growth rate.

Kondo and Takahashi (1987) presented evidencefor the involvement of an increased ethylene produc-tion at high night temperature, which then affects seed

development and finally abscission. They based theirconclusion on the fact that application of AVG, a non-specific inhibitor of ethylene biosynthesis, preventedthe negative effect of high night temperature on seeddevelopment and abscission. Reduced abscission ofmature and young fruit after the application of AVGwas reported earlier (Bangerth 1978 and Rahemi etal. 1997 for literature) and explained by its inhibitionon ethylene biosynthesis. However, Southwick andDavis (1982), Fukui et al. (1984), Ebert and Bangerth(1985) and more recently Rahemi et al. (1997), afterdetailed studies, dismissed the idea that ethylene pro-

duction, particularly by young fruit, is related to fruitset/drop, and the later authors suggest that AVG musthave a different as yet unknown mode of action onfruit set. In the light of these results, it must bequestioned as to whether high night temperatures stim-ulate abscission via an increased ethylene production.Beside the higher ethylene production observed byKondo and Takahashi (1987), a rapid and considerabledecrease in IAA export was observed from fruit keptat a high night temperature, with Golden Deliciousagain reacting stronger than Elstar (Bangerth 1997,and Table 2). This was in spite of the higher growthrate of these fruit and opposite to the IAA exportfrom shoot tips on these trees which was increased(Bangerth 1990). Whether this reduced IAA exportfrom the fruit is the result of a correlative inhibitionby the increased IAA export from the shoot tips (seeGruber and Bangerth 1990) needs additional proof. Ifso, localised applications of growth retardants to shoottips, or bending of shoots, which both strongly reduce


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IAA export (Sanyal and Bangerth 1998, Bangerth,unpubl.) should eliminate the negative effect of highnight temperatures on fruit abscission. Not only treefruit but also young legume pods and pepper fruit-lets show an increase in abscission rate as a result ofa decrease in IAA export at high night temperatures

(Ofir et al. 1993, Huberman et al. 1997).Additional support for a role of IAA transportin the abscission process of young fruit comes fromexperiments with synthetic auxin transport inhibitors.Naphthylphthalamic acid (NPA) is a potent inhib-itor of auxin transport in many biological systems(see Lomax et al. 1995) and was used as the activeingredient in the commercial product Peach Thin inthe past. Together with other auxin transport inhibit-ors it can considerably reduce IAA export from, forexample, apple fruit (Table 3). There is a thinningeffect of these chemicals at non-herbicidal concentra-tions which is, however, not significant and reliable

enough to justify their practical use. However, whenapplied in combination with Ethrel (an auxin transportinhibitor via ethylene) IAA transport inhibition is evenstronger and the thinning effect of these combinationscan be considerable. Further experiments are neededto explore the thinning potential of such combinationsin the orchard, keeping in mind that some, but not allof these auxin transport inhibitors severely reduce Catransport into the fruit and final fruit size (Bangerth1979, Banuelos et al. 1987).

7. Mode of action of thinning chemicals andrelationship to correlative abscission

Only those thinning chemicals will be consideredwhose mode of action is not phytotoxic or herbicidal(e.g. urea, Endothal, DNOC, ATS, Terbacil etc.). Itcan be assumed that most of the remaining thinningchemicals act by interfering with the endogenous hor-mone system of the plant/fruit, although some authorsconsider assimilate allocation as an alternative modeof action (e.g. Schneider 1978, McArtney et al. 1995,Stopar 1998). Even though most of these chemic-als and their thinning potential have been known fordecades, it is surprising that their mode of action is,nonetheless, largely unknown. Most of the suggestionsraised to explain their action have not been supportedby later critical examinations. It has been proposedthat the interference mentioned above may lead tothe disturbance of the homoeostatic endogenous hor-mone system, which finally may cause the initiation

of abscission of the weaker fruit (Luckwill 1953a).Many experiments have been conducted to attemptto prove this assumption (Dennis, 1986). Even themost extensive studies, however, could not unequi-vocally demonstrate a causal relationship between thethinning effect of a chemical and changes observed

in the extractable hormonal make up of the treatedfruit. Ebert and Bangerth (1985) and Retamales (1988)investigated the effect of various thinning chemicalson ethylene production, IAA, ABA and cytokinin con-centration of treated apple and peach fruit, but wereunable to make reliable conclusions from these invest-igations as far as extractable IAA, ethylene, ABA,Z/ZR and iAde/iAdo were concerned (Figure 4). Theonly exception was a short transient increase in ABAshortly after application of the thinning agent, whichprobably would support the view of Talons groupabout the causal involvement of this hormone in theabscission process of young fruit (Zacarias et al. 1995,

Talon et al. 1997). Similarly, Kojima et al. (1996)found, after the application of uniconazol, an inhib-itor of gibberellin biosynthesis, a close relationshipbetween the increase of ABA and stimulated abscis-sion of satsuma mandarin fruitless. A similar relation-ship for apples sprayed with carbaryl was found earlierby Treharne et al. (1985). A more careful examina-tion is needed to test whether the observed increasesin ABA is part of the initiation process of abscissionor is the result of the decreased growth rate and finalabscission of the treated fruit (see above).

In contrast to the almost absent relationship

between extractable hormone and fruit abscission afterchemical thinning treatments, IAA export from thosefruit was considerably reduced after the applicationof a number of thinning chemicals, such as NAA,Ethrel, Carbaryl, 3-CPA, CGA, (Crowe 1965, Ebertand Bangerth 1982, Retamales 1988). Here again,more rigorous examination is needed to test whetherIAA transport inhibition is in fact one of the decis-ive reasons for young fruit abscission or is a con-sequence of abscission. The only available method todiscriminate between such cause or effect altern-atives seems to be the parallel measurement of thegrowth rate of individual fruits, as an indicator of theirabscission potential (Zucconi et al. 1978, Ruiz andGuardiola 1994), which later serve as a source forhormone and carbohydrate analyses. Although time-consuming, this experimental procedure will give abetter insight into the hormonal and physiologicalregulation of the abscission of young fruit. A pos-sible alternative could be the more extensive use of


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Figure 3. Scheme of basipolar IAA- and acropetal Ca-transport. Uptake of IAA into the cell from the cell wall apoblast occurs, because of thelow pH, in the non-dissociated form or as H+ symport by diffusion through the PL or via an uptake carrier. Because of the higher pH in theCPL the now dissociated IAA will be exported at the basal end of the cell by an IAA export carrier. A component of this carrier can bind auxintransport inhibitors, such as NPA, and if this occurs IAA-export will be blocked. In weak transpiring organs, like fruit or shoot tips, Ca ionsare obviously moving in an opposite direction to IAA. A relationship seems to exist between the two polar transport pathways, since some ofthe auxin transport inhibitors not only reduce IAA but also Ca transport.(CW = cell wall; CPL = cytoplasm; PL = plasmalemma)

Table 2. IAA-export, fruit weight and total abscission of Golden Delicious and Elstar apple fruit after keeping the trees at twodifferent night temperatures. Note that the experiment for detecting abscission was conducted in a different year.

1997 Experiment 1998 Experiment

Cultivar Night (18.007.00) IAA-export (ng fruit1 20h1) at Fruit weight 9d after Total abscission of fruit

temperature (C) 6 and 9d after treatment treatment (g fruit1) (% of initial fruit set)

Golden Delicious 5 5.2 5.7 0.34 48

15 3.2 5.0 0.25 85

Elstar 5 4.7 5.4 0.31 4.5

15 4.3 5.0 0.54 14


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Figure 4. Concentrations of IAA, ABA and Z/ZR of Early le Grand peach fruit (A: pericarp; B: seed). Treatments are control (Co.) and afterthinning by hand, 3-CPA or CGA. No remarkable differences are seen between control (unthinned) or thinned fruit. The only exception is atransient increase of ABA in both tissues after chemical but not after hand thinned or control fruit (data are from Retamales, 1988). Thinningtreatments were applied 50 days after full bloom (DAFB).


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Table 3. Effect of the IAA-transport inhibitors TIBA and NPA, with or without in combination withEthrel, on the number of remaining fruit after June drop and on IAA export of Coxs and Elstar applefruit (1987). Samples were taken 6, 9, and 16 days after treatment.

Treatment Fruit/100 flower clusters IAA export (ng/fruit) at 6, 9 and 19

days after treatment

Coxs Elstar Cox Elstar

6 9 16 6 9 16Control 50 6 77 11 1.4 5.5 3.4 4.1 10.0 1.9

TIBA (100 mg/l) 55 5 62 8 0.8 0.9 1.6 1.9 1.2 1.1

NPA (100 mg/l) 43 9 66 12 0.8 1.9 1.2 2.1 2.7 1.3

Ethephon (300 mg/l) 45 7 54 15 1.0 3.9 1.4 3.7 5.2 1.7

TIBA+Ethephon (100 + 300) 34 9 13 15 0.4 n.a. 1.2 1.1 1.0 1.2

NPA + Ethephon (100 + 300) 40 6 35 13 0.4 n.a. 1.4 2.0 1.8 1.5

n.a. = not analysed.

the above discussed experiments with elevated nighttemperatures.

Of particular interest in this respect is the frequentobservation that some of the thinning chemicals areonly effective when applied to the leaves, whereasapplication to the fruit itself is ineffective. BA andparticularly NAA belong to this group (Green et al.1992, Dennis this Vol.) whereas Carbaryl and Ethrelare only effective when directly sprayed to the fruit(Knight 1983, Bangerth, unpubl.). This again raisesthe important question as to whether these thinningchemicals exert their effect on IAA transport directlyor indirectly.

8. Interactions between environmental variables,

orchard practices, and correlative abscission of

young fruit

Both environmental factors and horticultural practicesare obviously responsible for a significant part of thevariability encountered during thinning with bioreg-ulators. Beside affecting uptake and metabolism ofthinning chemicals (see Schnherr et al., this Vol.),the environment as well as orchard practices have astrong influence on the correlative behaviour of thetree which in turn has an effect on fruit set and fruit

drop. Only some of the most influential factors will beconsidered below:

8.1 Light intensity and light quality

Shading of trees is a most efficient method to reducethe intensity of light intercepted by the tree can-

opy. Beyond that, shading has a considerable thinningeffect on a number of different fruit species (Byers andWolf 1988, Yuan and Huang 1988, Byers et al. 1991,Guardiola this Vol.). To achieve this effect, reduc-tion of light intensity down to about 10% of averagedaily sunlight is necessary. It has been frequently sug-gested that the decreased photosynthetic activity andthe resulting limited carbohydrate availability to thefruit might be the main or the only reason for theobserved thinning effect. The main rationale behindthis hypothesis was the observation that the applica-tion of the photosynthesis-inhibiting herbicide, Terba-cil, stimulates fruit drop at a similar rate as shading(Stopar 1998). In addition to reducing light intensity,

natural (i.e.by another leaf) as well as artificial shad-ing also changes light quality giving a higher far redproportion. Because far red increases abscission andreduces basipolar IAA-transport (Mao et al. 1989),it is expected that shading, by changing red: far red,might affect fruitlet abscission also by changes in IAAtransport rates. In fact, Green et al. (1986) were ableto reduce drop of young apple fruit by a short pulseof red light which increases IAA transport (Mao etal. 1989) during the night. Further, Kondo (1989)was able to show that three applications of GA4(100ppm) during the shading period diminished drop of

shaded fruit up to 95%. Since it is unlikely that GA 4affected carbohydrate availability under the low lightconditions, this effect of GA4may be explained by thegreatly stimulated IAA export from young fruit aftersuch a treatment (Callejas and Bangerth 1997). Theoften accepted mono-causal hypothesis on the actionof shading, therefore, needs a more thorough exam-


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ination considering red: far red light affected auxintransport possibly mediated by a red-light effecton gibberellins rather than on auxins as an addi-tional possibility for the stimulation of the fruit dropobserved.

8.2 TemperatureTemperature, in particular night temperature, hasalready been discussed as a factor strongly affectingfruit abscission, IAA transport and ethylene produc-tion alike. Opposite to the effect of a reduction of lightintensity, high night temperature increases the growthrate of fruit and shoots while enhancing abscission. Atfirst glance this seems to exclude carbohydrate limita-tion as a mode of action for the observed temperatureeffect. However, this high temperature effect is mainlyrestricted to the dark period (Byers and Smith 1998)and, therefore, it is still possible that an accelerated

dark respiration due to the high night temperat-ure leads to an excessive carbohydrate utilisation andlimitation. Thus, here again, a more careful examin-ation of the two alternative explanations of the highnight temperature effect, and their interrelationship,is needed. Prevailing temperatures affect fruit reten-tion not only in the way discussed above but they alsohave a strong influence on the number of seeds perfruit through their effect on the activity of bees andthe longevity and viability of unfertilised ovules. Seednumber is one of the main factors determining whichfruit in a cluster will abscise (Wertheim 1971) and maybe as important as primigenic dominance. High seednumber of a lateral fruit, which otherwise has a lowprobability of survival because of its low ranking inthe dominance hierarchy, may prevent its abscission.Seed number also strongly determines IAA transportrate (Figure 1). Fruit with zero seeds and no tend-ency for parthenocarpic development, have a very lowIAA transport rate and usually abscise (Bangerth et al.1989). However, seeded fruit show a strong increasein IAA export as seed number increases up to about 8to 10 seeds (Callejas and Bangerth 1997, and unpubl.results). However, given the same number of seedsper fruit, KF and lateral fruit still differ in their IAA

export rate. This underlines the importance of primi-genic dominance of the earlier developing over thelater fruit.

8.3 Horticultural practices

A number of horticultural procedures, such as gird-ling and bending of shoots, application of growth

retardants, nitrogen fertilisation, use of different root-stocks etc. all affect fruit retention and the efficiencyof thinning. Their influence is usually explained bytheir effect on the vegetative growth of bourse shootsor shoots near fruit or fruit clusters, which then, bycompetition for carbohydrates, change fruit drop. In

fact, by removing the tips of growing shoots Quin-lan and Preston (1971) and Grauslund (1978) showedan increased fruit set, which demonstrates the neg-ative effect of vegetative growth on fruit retention.However, Gruber and Bangerth (1990), by findinga considerable increase in IAA export from applefruit after bourse shoot tip removal question at leasta mono-causal explanation via carbohydrate shortage.A correlative inhibition of IAA export of fruit bystrongly growing shoot tips seems, therefore, moreappropriate.

It seems conceivable that where shoots, adjacent tofruit, are growing vigorously their high level of IAA

export results in a correlative inhibition of IAA exportfrom young fruit. Corresponding with this assump-tion, IAA export from shoot tips is increased bythe application of gibberellins, which stimulate shootgrowth, while application of growth retardants suchas Alar or prohexadione-Ca, will have the oppos-ite effect (Callejas and Bangerth 1997). The latteraspect is particularly interesting since Browning et al.(1992) showed that paclobutrazol transiently increasedextractable IAA in shoot tips, demonstrating the inde-pendence of auxin transport from the extractable auxinconcentration in the shoot tips. Contrary to expecta-

tion, however, gibberellin as well as prohexadione-Catreatments have little influence on fruit drop. This maybe explained by our unpublished results, which showvery similar effects of these substances on IAA exportboth from fruit and shoot tips, leaving the resultantcorrelative interaction between fruit and shoot moreor less undisturbed.

Other horticultural procedures, such as bendingand girdling of shoots, are known to have signific-ant effects both on vegetative growth of treated shootsas well as on the retention of fruit growing on theseshoots. Horizontal bending of vertical growing appleshoots is well known to reduce shoot growth andincrease fruit retention (Robbie et al. 1993). Bendingor girdling of shoots or whole trees has similar effects.Sanyal and Bangerth (1998) and Bangerth (unpubl.)showed that bending has considerable effects on endo-genous ethylene, cytokinin, gibberellin, and auxinconcentration of the treated apple shoots. Beside theseeffects, bending causes a long-lasting reduction in


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IAA export from the shoot tips. Similarly, girdlingconsistently decreased shoot tip IAA export while con-siderably increasing export out of fruit (Figure 5),which corresponds with the reduced fruit drop aftersuch treatments.

The correlative nature of these shoot/fruit IAA

transport interactions can be demonstrated by, forinstance, removal of fruit which stimulates shoot IAAexport and vice versa as shown above for shoot tip-ping. In addition, in some cases the function of theremoved organ could be replaced by applying auxinto the cut surface, indicating the probability that com-petition for carbohydrates may not be the main factorinvolved.

9. Conclusions and possible prospects

An attempt has been made to demonstrate that abscis-

sion of young fruit at certain periods cannot beexplained by the model developed for leaf- or fruit-explants. Young fruit abscise because of the correl-ative influences exerted on them by more dominantfruit and/or shoots. The signal that transmits thesecorrelative events is the basipolar transport of IAA.This uni-directional transport has a multidirectionalcomponent at junctions where two or more auxinstreams from organs (fruit or shoot) with differentdegreesof dominance meet (see Figure 1 and Bangerth1989). At these junctions, the auxin stream of themore dominant organ exerts an autoinhibiting effect

on the auxin transport of the more dominated organ,which, by inhibiting IAA and possibly CK biosyn-thesis (Httche 1996), has negative effects on fruitgrowth. More importantly, this autoinhibition mechan-ism down regulates IAA transport through the AZ ofthese fruit and finally triggers their abscission. Ethyl-ene is necessary for the final step(s) in this process,but, contrary to abscission induced by senescence, isnot the initial driving signal.

Experimental results fromour own research as wellas from literature are presented to support the abovehypothesis on correlative abscission. Since most ofthese experiments have been conducted on apple andpeach, their validity for other fruit species requiresfurther experimentation.

In spite of the evidence presented above, correl-ative abscission, as distinguished from senescenceabscission, may not be the only triggeringmechanismin the abscission process of young fruit. In fact, therestill exists a considerable controversy as to whether

carbohydrate availability or limitations in allocation(Bustan et al. 1995) contributes to natural or inducedfruit abscission. Most certainly, both alternatives,assimilates as well as hormones, must be considered.However, it is difficult to view carbohydrate limitationas a direct trigger of the abscission process, because, in

this case, it would be complicated to explain why mosttree fruit show certain periods of increased fruit dropand why only particular fruit are destined to absciserather than all being retained only to grow smal-ler. It seems more reasonable that assimilate short-age, like many environmental events, intervenes in anunknown way in the described correlative IAA signalprocess.

The ecological advantage for the correlativeabscission system is that it may, to some extent, anti-cipate carbohydrate shortage and produce a reactionaccordingly (see above and Stephenson, 1981). Thiscould mean supporting a smaller number of fruit/seed

to maturity in contrast to lose most fruit prematurelybecause of carbohydrate limitation. Where fruit set isheavy, the slower-growing dominated fruit are morelikely to abscise first, whereas the dominant, mostcompetitive and eventually larger fruit survive. In thisway, the ecological meaningful system turns out to bealso of horticultural advantage, since it is the largerfruit that earns the better price.

Correlative abscission is a process affected bynumerous environmental and intrinsic variables, andis one of the most difficult obstacles for a successfulthinning strategy employing bioregulators. As shown

above, IAA autoinhibition for a particular fruit is theoutcome of the IAA transport rates of all neighbouringfruits and shoots, which by themselves are affected byfactors such as time of fertilisation, seed number, otherhormones, temperature, light, carbohydrate availabil-ity etc. Interference with these processes by applying athinning chemical usually will affect not just the IAAsignal of the weaker fruit intended to be removed butthe IAA export of the other generative and vegetativeorgans as well. A thinning treatment which selectivelyaffects IAA transport only of strongly dominated fruitis, therefore, understandably difficult. As an example,the application of an ethylene generating compound,such as Ethrel, will reduce the IAA export out of fruitand of shoots alike. In this way, the correlative inhib-iting effect, for example, of the bourse shoot tip isreduced but fruit drop may not change because of asimilar reduction in IAA export from the fruit as well.Another example may be the application of BA. Themode of action of BA as a thinning chemical is cer-


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Figure 5. Effect of girdling an apple fruit bearing shoot on IAA export from KF, LF and shoot tips 22 days after girdling at full bloom. Thisis presumably the time when fruit abscission is determined. Percent abscission (right hand side of the figure) was recorded after June drop, 32days after girdling, and was particularly reduced for KF.(K.F.C. = KF control; K.F.G. = KF after girdling; L.F.C. = L.F. control; L.F.G. = LF after girdling; S.C. = shoot tip control; S.G. = shoot tipafter girdling).

tainly different from Ethrel and may involve a transientstimulation of the growth of lateral side shoots (Green

and Autio 1990, Elfving and Cline 1993). By virtue ofthis, the IAA transport out of all these newly releasedlateral buds may correlatively inhibit IAA transportfrom fruit leading to the abscission of some of thethem. Recent results by Bianchi et al. (unpubl. res-ults) support this assumption. If this over-simplifiedassumption is correct, thinning with this endogenous(van Staden and Crouch 1996) plant hormone, BA,would be more selective than with Ethrel. This is sur-prising, since, as mentioned above, BA preferably actsvia leaves and Ethrel via fruit.

What presently can be achieved by the applicationof thinning chemicals is always only a disturbanceof the balance between the correlatively acting IAAtransport streams. By gaining a better knowledge ofthese complicated interactions one may finally be ableto design more reliable and more environmentallyfriendly thinning compounds. An alternative to thiswould be the construction and implementation of achimeric abscission gene coupled to an induceable

organ specific promotor. That goal, however, is for thefuture.

Acknowledgements

The author is greatly indebted to Dr. J. D. Quinlan forhis critical reading of the manuscript. Financial sup-port by the German Research Organisation (DFG) isgreatly acknowledged.

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