Plant Growth Regulation 31: 4359, 2000.

2000 Kluwer Academic Publishers. Printed in the Netherlands.

43
Abscission and thinning of young fruit and their regulation by plant
hormones and bioregulators
F. Bangerth
Institut 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 generally
accepted model of senescence triggered abscission of, for example, leaves or mature fruit. It is concluded that
abscission 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. Polar
basipetal IAA transport with its autostimulation and autoinhibition components is the main regulating signal in this
correlative 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, this
hypothesis 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 its
interference with the endogenous hormone system is concerned.
Abbreviations: ACC= 1-aminocyclopropane-1-carboxylic acid; AVG= aminoethoxyvinylglycine; AZ = abscission
zone; IAA = Indolylacetic acid; KF = king fruit; LF = lateral fruit
1. Introduction
Many fruit tree species bear an abundance of owers
which, even after poor pollination conditions, produce
a surplus of fruit that the tree is unable to support.
Possibly in anticipation of this, many fruit trees have
developed a self regulatory-mechanism whereby they
shed 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 the
tree than can be supported under prevailing environ-
mental conditions. From a horticultural point of view,
this self-regulatory mechanism may be too strong for
fruit species, such as mango, avocado etc., leading
to low fruit load and yield. With some other fruit
crops set is more or less sufcient, as for example
some Citrus spec. (Monselise et al., 1981), whilst with
most of the temperature fruit group, as e.g. apple,
pear, peach, plums, the self-regulatory mechanism is
entirely insufcient to guarantee the required quality
standards. This unsatisfactory degree of self regula-
tion in the latter group of fruit trees has a number of
disadvantages, of which two are most serious:
low and often unacceptable market quality (see
Link, 1986 and this Vol.)
inhibition of ower bud induction, causing severe
alternate bearing (see Tromp, this Vol.)
To overcome these shortcomings, ower- or fruit-
thinning is an efcient method and has become neces-
sary in modern fruit production. However, in most
developed countries, manual thinning is becoming
more 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 amplication of the natural self-regulatory fruit
abscission process. Knowing more precisely about
the mechanisms underlying this process of natural
fruit abscission would help to improve current thin-
ning practice. Most bioregulators presently in use as
44
chemical thinners are either unsatisfactory or unreli-
able or both with regard to their thinning efciency
(see Williams, 1979 and Wertheim, this Vol., for
literature). It is, therefore, even more necessary to
have a better understanding of the processes leading
to 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 the
abscission of young fruit:
insufcient supply of assimilate to fruitlets as
a result of limited assimilate production and/or
allocation 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 assimilate
shortage in the process of abscission of young fruit
for a number of species. Even for some evergreen cit-
rus species, it is claimed that assimilate shortage or
limitation in carbohydrate allocation may occur dur-
ing certain periods of fruit development (Bustan et al.,
1995, Goldschmidt and Koch, 1996). On the other
hand, Guardiola et al. (1984), and Ruiz and Guar-
diola (1994), report higher carbohydrate reserves in
abscising as compared to non-abscising citrus fruit,
casting doubt on the assimilate hypothesis. These
authors favour instead, a lack of sink demand as
the explanation. For apple and peach fruit, the evid-
ence for assimilate limitation as one of the reasons
for fruit abscission is stronger (Lakso 1994, Ber-
ter 1985, Berter and Droz 1991, Stopar 1998).
Again, however, carbohydrate analyses of abscising
versus non-abscising apple fruit revealed no evidence
that carbohydrate limitation or starvation could be a
causal factor in abscission (Abruzzese et al. 1995).
A brief summary of this unresolved issue would be
that there is no clear evidence that assimilate short-
age is a direct cause of fruitlet abscission. The second
hypothesis mentioned above may thus be more relev-
ant and will be treated preferentially thereafter. Two
physiological processes are critical in understanding
hormonally-regulated abscission of young fruit:
the activation of an abscission zone (AZ) of a par-
ticular fruit, which is the decisive event in thinning
as well as in abscission (see Bonghi et al., this Vol.)
hormonally controlled dominance phenomena
among fruit and between fruit and shoot
(Bangerth, 1989)
3. The presently accepted model of abscission
zone activation
The activation of the AZ by endogenous plant
hormones has been intensively investigated in the
past. The model describing this process was mainly
developed on explants by Addicott (1982), Morgan
(1984), Osborne and McManus (1984) and Osborne
(1989) and has only been modied subsequently (Sex-
ton 1994). It implies that auxin, specically IAA,
produced by the subtending leaf blade, is translocated
down the petiole where it retards AZ activation. The
physiological effect of IAA in this process is to reduce
the sensitivity of the AZ to ethylene (van Doorn and
Stead 1997). At low IAA concentration, ethylene then
activates this usually preformed tissue, resulting in
abscission. In this model, ethylene is, therefore, the
primary signal driving the abscission process.
Signicant progress has been made recently in
understanding the process of AZ activation and the
signal transduction pathway following the recognition
of ethylene by a receptor in the AZ (see Bonghi et
al., this Vol.). This aspect of AZ activation by ethyl-
ene will, therefore, not be discussed further here.
In contrast to this nal ethylene regulated part of
the abscission process, the desensitising of the AZ
caused by IAA is little understood. IAA is considered
the main factor in controlling the sensitivity of the AZ
to ethylene, but it may not be the only one. There
are periods during fruit development when the AZ is
insensitive to ethylene even though IAA transport to
these AZ during that period may be low. If more than
one AZ is present at a pedicel, e.g. in citrus or peach,
usually only one of them is sensitive at a time (Goren
1993). The fact that the AZ can become sensitive to
ethylene again, as e.g. during the pre-harvest period
(pre-harvest drop), suggests developmental control
apart from auxin regulation of this process.
In the above-mentioned model, it is the beginning
of the senescence process in the leaf blade or ripening
fruit which initiates the production of elevated levels
of ethylene. This then reduces production or stimu-
lates metabolism of auxin (Riov et al. 1982), but more
importantly, diminishes basipolar transport of IAA to
the AZ (Beyer and Morgan 1971), possibly by redu-
cing IAA export carriers (Suttle 1988). As a result,
45
the sensitivity of that tissue to ethylene increases (see
above) and the process of abscission by an increase
in hydrolytic enzymes and nally cell separation is
initiated (Osborne 1989, Sexton 1994). The question
arises as to whether the leaf explant model is valid for
the abscission of intact reproductive organs as well. In
this respect, the few documented examples are restric-
ted to owers (Wien et al. 1989, del Campillo and
Bennett 1996, van Doorn and Stead 1997) and mature
fruit during pre-harvest drop (Kasha 1989, Brady and
Spiers 1991, Goren 1993). The abscission of young
vigorously-growing fruit, however, certainly cannot
be compared with senescing leaves or ripening fruit
and the regulation of their abscission at particular peri-
ods may be signicantly different. A hypothesis will
be developed below which may better describe the
abscission of young fruit than the leaf explant model.
The intention is to evaluate this hypothesis by results
presented 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 following
hypothesis have been published previously (Bangerth
1989), correlative dominance rather than CDA was
the main subject considered. Here, CDA will be the
exclusive topic although these two hypotheses are
closely 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 starts
to senesce and produces higher amounts of ethyl-
ene. However, young fruit start to senescence only
after they are already determined to drop by a pre-
ceding correlative event (see below). Similarly, an
increase in ethylene evolution is not observed for
the very early stages of abscission. Also, a decrease
in auxin transport to the abscission zone, character-
istic of senescent leaves (see above), is not observed
with young fruit. To the contrary, auxin export from
young apple fruit and transport to the AZ generally
increases shortly after fruit set considerably (Gruber
and Bangerth 1990), whereas ethylene production
drops 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 fruit
should not abscise. Nonetheless, some of them do
and this can be explained by a hypothesis developed
earlier (Bangerth 1989, 1997). This hypothesis substi-
tutes senescence-controlled by correlatively-regulated
abscission of young fruit. Since the high IAA export
of young fruit would not allow sensitisation and activ-
ation of the AZ by ethylene, a mechanism has to
be found which explains the down-regulation of
the auxin export of those fruit which are eventually
destined to abscise. This is primarily achieved by
a correlative dominance effect of adjacent fruit or
nearby shoot tips. In a spur cluster of apple fruit, for
example, it is the fruit that is set and develops rst
(usually the terminal king fruit, KF) that dominates
over later developing lateral fruit (LF) and causes most
of them to abscise (Figure 1). Even among the lateral
fruit a ranking of dominance exists, although not as
great as between KF and LF. In other fruit species,
the spatial arrangement of the dominating fruit may be
different. In citrus, for example, it is again the terminal
ower which opens rst, but the ranking of the lateral
owers follows a more complex pattern (Spiegel-Roy
and Goldschmidt 1996) and in peach it is the distal
fruit on a shoot as compared to the proximal one which
dominates (Spencer and Couvillon 1975). Almost
always, however, it is the fruit that sets rst which
dominates later developing fruit and for this reason the
termprimigenic dominance was used to characterise
this phenomenon (Bangerth 1989). Dominated fruit
initially show a reduced growth rate and, decisively, a
lower auxin export (Figure 1). Both characteristics dis-
appear as soon as the dominant fruit(s)/shoot tips are
removed (Gruber and Bangerth 1990 and Figure 2), at
least as long as not a point of no return has been
reached. The measured difference in auxin export of
dominating versus dominated fruit can be explained
as follows:
IAA is able to stimulate its own basipolar transport
(autostimulation hypothesis; see Goldsmith 1977, and
Warren Wilson et al. 1988 for literature). At the junc-
tion where the strong polar IAA transport pathway
of a dominant fruit meets the weaker IAA pathway of
a dominated fruit the latter is inhibited by the former
(Bangerth 1989, Li and Bangerth 1999). This autoin-
hibition of auxin transport at junctions is illustrated
in Figure 1 and can be experimentally veried by
replacing the dominant king fruit by the application
of an auxin such as NAA or 2, 4-D (Bangerth 1997).
The degree of dominance of one fruit over another as
compared to a dominated fruit largely depends on:
the different (in hours or days) in fruit set between
dominant and dominated fruit (Stephenson 1981,
Stephenson et al. 1988, Gruber and Bangerth
1990).
46
the number of seeds/fruit (Stephenson 1981,
Bangerth et al. 1989). Seed number is an import-
ant determinant of auxin export of a particular fruit
(Callejas and Bangerth 1997)
the proximity and vigour of nearby vegetative
shoot 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 which
started their development earlier than other lateral
fruit (see Figure 1)
All these dominance effects are cumulatively
reected in the IAA export rates of a particular fruit.
Thus, IAA export out of a young fruit and transport
through the AZ is regulated by a number of correl-
atively acting factors from nearby organs which dif-
ferentially affect autostimulation and autoinhibition of
that transport system according to their ranking in the
dominance hierarchy. The nal effect of the resultant
correlative dominance on auxin transport autoinhib-
ition of dominated fruit leads to a situation where
the auxin transport of the most dominated fruit falls
below a certain threshold value at which stage it no
longer inhibits sensitisation and activation of the AZ
by ethylene, which then results in the shedding of that
fruit.
A further interesting aspect that follows from this
correlative process is that the more fruit that are
present in a cluster, the stronger is the autoinhibition
of auxin transport on the most dominated fruit in that
cluster and the higher the probability that this fruit
will be shed. On the other hand, when very few fruit
are 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 heavy
fruit load (high initial fruit set) before such a shortage
even exists and shed fruit heavily during the specic
fruit-fall periods. The self-regulatory process men-
tioned above could, therefore, also be explained by
the hypothesis of correlative abscission. Also, the
common observation that chemical thinning is easier
on trees bearing a heavy fruit load can be correlated
to this mechanism. With a larger number of fruit, the
dominance effect is greater and the thinning biore-
gulator only needs to reduce IAA transport of the
most dominated fruit (e.g. the most basal fruit in Fig-
ure 1) only by a small amount to reach the threshold
value mentioned above. Selective thinning, mean-
ing that most thinning-bioregulators remove the most
dominated fruit rst (Link 1968), would be a logical
consequence of that hypothesis. It should be men-
tioned, however, that some potent thinning chemicals
are non-selective thinners (see Green et al., 1992 for
literature)
Summarising the above hypothesis, it is the
correlatively-driven abscission which replaces
senescence-driven abscission of the classical
abscission model by an interorgan correlative
signalling. The latter results in a down regulation of
IAA transport by autoinhibition at junctions. From
there on, the process of abscission most certainly
proceeds in a fashion similar to that described above
for 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 specic IAA export carriers of
specialised cells near to the sieve tubes (Goldsmith
1977, Lomax et al. 1995). Thus, IAA is exported
from these cells at their basal sites, taken up again
by the next cell, exported at their basal end and so
on (Figure 3). These export carriers are highly reg-
ulated, e.g. by a number of so-called synthetic IAA
transport inhibitors such as TIBA, NPA and related
substances, morphactins etc. These substances can
reduce or even block the function of IAA export
carriers and thus polar auxin transport. Theoretical
considerations led Hertel (1983) to speculate that the
presence and function of these synthetic IAA trans-
port inhibitors can logically be explained only by the
assumption that naturally occurring endogenous auxin
transport inhibitors use the same receptor sites as the
synthetic 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 to
be fairly rapid and affected by other plant hormones.
Suttle (1988, 1991) and Yoon and Kang (1992) were
able to demonstrate that the well known IAA-transport
inhibition 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 their
degradation. It must be admitted, however, that a con-
siderable number of other possibilities are available
to explain IAA-autoinhibition beside the already
mentioned hypothetical endogenous transport inhibit-
ors and the turn-over rate of export carriers. Among
them are alterations in the concentration/afnity of
auxin-import carriers (Hertel 1983). These carriers are
47
Figure 1. Scheme of an apple fruit cluster. Numbers outside the fruit represent the ranking in PD hierarchy. Numbers inside the fruit give ng
IAA export per 20h standard error and, as an example, the number of seeds. Note the inuence of PD and the number of seeds on IAA export.
All gures 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 occurs
AZ : abscission zone
partly responsible for the differential uptake of vari-
ous auxins (Delbarre et al. 1996) and, therefore, their
varying polar transport rates. Further experimentation
is urgently needed to sort out the more important steps
involved 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-transport
autoinhibition (see Li and Bangerth 1999).
Besides these uncertainties about the physiolo-
gical mechanisms responsible for polar auxin transport
there are other unresolved questions which need to be
investigated in order to gain a better understanding
of correlative abscission. It has long been known that
the application of IAA to the basal end of an explant
does not decrease but, to the contrary, considerably
increases 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 the
junction with the strong IAA export of a dominant
fruit. Higher concentrations of IAA in AZ of abscising
versus non-abscising cotton-and citrus fruitlets (Guinn
and Brummett 1987, Okuda and Hirabayashi 1998), in
spite of the reduced IAA transport out of these fruit,
48
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 yellow
colour of their pedicells).
B: A fruit cluster where the KF had been removed a few days after full bloom. Four of the original ve LF are still present shortly after June
drop and grow vigorously.
may also be the result of such a stagnation in IAA
transport. Results such as these raises the question
as to whether it is the concentration of IAA in the
AZ or the auxin ow through it which determines its
activation.
6. Does the hypothesis of correlative abscission
t experimentally obtained results?
If the above hypothesis for correlative abscission
describes abscission of young fruit better than the
existing leaf explant model, one should be able to test
its validity by comparing it with results already avail-
able in the literature or design experiments to evaluate
it.
Initial work to investigate the endogenous regu-
lation of fruit set or abscission mainly considered
changes in the concentration of endogenous extract-
able hormones in seeds/fruits to be one of the trigger-
ing events which then initiates senescence, increased
ethylene production, and fruit drop (Luckwill 1953 a
& b pioneered this area of research). Even though a
number of results could be obtained which seemed to
be closely related to fruit abscission, none could be
closely associated to the abscission process of young
fruit (see Dennis this Volume, for literature). From all
the determinations of hormone concentrations, only
ABA in a few instances could possibly be considered
as an abscission accelerating constituent. At present, it
is not clear whether ABA is able to directly stimulate
fruit drop, as Cooper and Horanic (1973) and Bangerth
(1975) demonstrated for fruit explants and which Juan
and Huang (1988) suggest for intact litchi fruit abscis-
sion and ABA accumulation. Alternatively, a higher
ABA concentration may stimulate ethylene production
as shown by Jackson and Osborne (1970) for explants.
Guinn and Brummet (1987), and more recently Talon
et al. (1997), found a close relationship between ABA
concentration and abscission of cotton and citrus fruit.
The later authors suggest a stimulating effect of ABA
on ACC- and ethylene biosynthesis, with the latter one
being responsible for the increased fruit drop. Whether
the effect of ABA is direct (Juan and Huang 1988)
49
Table 1. Concentration of ABA in seed and peri-
carp tissue of Elstar apple fruit after treatment with
the 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 be
assumed to be a trigger for fruit abscission. As with
most experimental results based only on correlations,
the assumption of a causal effect should be considered
with caution. In one recent experiment (Httche and
Bangerth, in prep.), a sharp and rapid drop in ABA
concentration in apple fruit after their release from
dominance by removal of the KF was found. This
was probably related to the interruption of the IAA-
transport autoinhibition by this manipulation. This
conclusion is based on the observation that a strong
IAA transport inhibition produced by spraying NPA
with or without Ethrel, strongly increased ABA in
treated fruit (Table 1). These two experiments suggest
that the observed increase in ABA may be more the
result of a disturbed auxin transport than the cause of
abscission.
Other endogenous plant hormones, beside ABA,
have been related to fruit abscission but with similar
problems to those discussed above for ABA (Den-
nis 1986 and this Vol.). An experimental method
described by Kondo and Takahashi (1987) and Kondo
(1989) might help to better discriminate between
cause and effect with endogenous hormones. Placing
apple trees into high (15

) or low (10

) night
temperatures caused considerable differences in fruit
abscission in their experiments, with the high tem-
perature fruit being considerably more susceptible
to abscission. Conducting similar experiments, Tukey
(1956, 1960) observed that high night temperatures
(e.g. 22.2

C) stimulated fruit growth more than low

night temperatures (e.g. 8.8

C). These results were

conrmed by us in four-year experiments with the cv.
Golden Delicious but results were less clear for Elstar
apple trees (Table 2). This experimental set up allows
the 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 observed
in almost all other experiments so far. The advantage
of this kind of experiment is that it helps to eliminate
the generally recognised crucial negative correlation
between growth rate and abscission rate of fruit (Zuc-
coni et al. 1978) and the argument that the hormonal
changes usually associated with the abscission process
(e.g. reduced IAA transport) are mainly the result of
this diminished growth rate.
Kondo and Takahashi (1987) presented evidence
for the involvement of an increased ethylene produc-
tion at high night temperature, which then affects seed
development and nally abscission. They based their
conclusion on the fact that application of AVG, a non-
specic inhibitor of ethylene biosynthesis, prevented
the negative effect of high night temperature on seed
development and abscission. Reduced abscission of
mature and young fruit after the application of AVG
was reported earlier (Bangerth 1978 and Rahemi et
al. 1997 for literature) and explained by its inhibition
on ethylene biosynthesis. However, Southwick and
Davis (1982), Fukui et al. (1984), Ebert and Bangerth
(1985) and more recently Rahemi et al. (1997), after
detailed studies, dismissed the idea that ethylene pro-
duction, particularly by young fruit, is related to fruit
set/drop, and the later authors suggest that AVG must
have a different as yet unknown mode of action on
fruit set. In the light of these results, it must be
questioned as to whether high night temperatures stim-
ulate abscission via an increased ethylene production.
Beside the higher ethylene production observed by
Kondo and Takahashi (1987), a rapid and considerable
decrease in IAA export was observed from fruit kept
at a high night temperature, with Golden Delicious
again reacting stronger than Elstar (Bangerth 1997,
and Table 2). This was in spite of the higher growth
rate of these fruit and opposite to the IAA export
from shoot tips on these trees which was increased
(Bangerth 1990). Whether this reduced IAA export
from the fruit is the result of a correlative inhibition
by the increased IAA export from the shoot tips (see
Gruber and Bangerth 1990) needs additional proof. If
so, localised applications of growth retardants to shoot
tips, or bending of shoots, which both strongly reduce
50
IAA export (Sanyal and Bangerth 1998, Bangerth,
unpubl.) should eliminate the negative effect of high
night temperatures on fruit abscission. Not only tree
fruit but also young legume pods and pepper fruit-
lets show an increase in abscission rate as a result of
a decrease in IAA export at high night temperatures
(Or et al. 1993, Huberman et al. 1997).
Additional support for a role of IAA transport
in the abscission process of young fruit comes from
experiments 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 active
ingredient in the commercial product Peach Thin in
the past. Together with other auxin transport inhibit-
ors it can considerably reduce IAA export from, for
example, apple fruit (Table 3). There is a thinning
effect of these chemicals at non-herbicidal concentra-
tions which is, however, not signicant and reliable
enough to justify their practical use. However, when
applied in combination with Ethrel (an auxin transport
inhibitor via ethylene) IAA transport inhibition is even
stronger and the thinning effect of these combinations
can be considerable. Further experiments are needed
to explore the thinning potential of such combinations
in the orchard, keeping in mind that some, but not all
of these auxin transport inhibitors severely reduce Ca
transport into the fruit and nal fruit size (Bangerth
1979, Banuelos et al. 1987).
7. Mode of action of thinning chemicals and
relationship to correlative abscission
Only those thinning chemicals will be considered
whose mode of action is not phytotoxic or herbicidal
(e.g. urea, Endothal, DNOC, ATS, Terbacil etc.). It
can be assumed that most of the remaining thinning
chemicals act by interfering with the endogenous hor-
mone system of the plant/fruit, although some authors
consider assimilate allocation as an alternative mode
of 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 for
decades, it is surprising that their mode of action is,
nonetheless, largely unknown. Most of the suggestions
raised to explain their action have not been supported
by later critical examinations. It has been proposed
that the interference mentioned above may lead to
the disturbance of the homoeostatic endogenous hor-
mone system, which nally may cause the initiation
of abscission of the weaker fruit (Luckwill 1953a).
Many experiments have been conducted to attempt
to prove this assumption (Dennis, 1986). Even the
most extensive studies, however, could not unequi-
vocally demonstrate a causal relationship between the
thinning effect of a chemical and changes observed
in the extractable hormonal make up of the treated
fruit. Ebert and Bangerth (1985) and Retamales (1988)
investigated the effect of various thinning chemicals
on ethylene production, IAA, ABA and cytokinin con-
centration of treated apple and peach fruit, but were
unable to make reliable conclusions from these invest-
igations as far as extractable IAA, ethylene, ABA,
Z/ZR and iAde/iAdo were concerned (Figure 4). The
only exception was a short transient increase in ABA
shortly after application of the thinning agent, which
probably would support the view of Talons group
about the causal involvement of this hormone in the
abscission 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 relationship
between the increase of ABA and stimulated abscis-
sion of satsuma mandarin fruitless. A similar relation-
ship for apples sprayed with carbaryl was found earlier
by Treharne et al. (1985). A more careful examina-
tion is needed to test whether the observed increases
in ABA is part of the initiation process of abscission
or is the result of the decreased growth rate and nal
abscission of the treated fruit (see above).
In contrast to the almost absent relationship
between extractable hormone and fruit abscission after
chemical thinning treatments, IAA export from those
fruit was considerably reduced after the application
of a number of thinning chemicals, such as NAA,
Ethrel, Carbaryl, 3-CPA, CGA, (Crowe 1965, Ebert
and Bangerth 1982, Retamales 1988). Here again,
more rigorous examination is needed to test whether
IAA 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 to
discriminate between such cause or effect altern-
atives seems to be the parallel measurement of the
growth rate of individual fruits, as an indicator of their
abscission potential (Zucconi et al. 1978, Ruiz and
Guardiola 1994), which later serve as a source for
hormone and carbohydrate analyses. Although time-
consuming, this experimental procedure will give a
better insight into the hormonal and physiological
regulation of the abscission of young fruit. A pos-
sible alternative could be the more extensive use of
51
Figure 3. Scheme of basipolar IAA- and acropetal Ca-transport. Uptake of IAA into the cell from the cell wall apoblast occurs, because of the
low 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 the
CPL 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 auxin
transport inhibitors, such as NPA, and if this occurs IAA-export will be blocked. In weak transpiring organs, like fruit or shoot tips, Ca ions
are obviously moving in an opposite direction to IAA. A relationship seems to exist between the two polar transport pathways, since some of
the 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 two
different 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 fruit
1
20h
1
) at Fruit weight 9d after Total abscission of fruit
temperature (

C) 6 and 9d after treatment treatment (g fruit

1
) (% 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
52
Figure 4. Concentrations of IAA, ABA and Z/ZR of Early le Grand peach fruit (A: pericarp; B: seed). Treatments are control (Co.) and after
thinning by hand, 3-CPA or CGA. No remarkable differences are seen between control (unthinned) or thinned fruit. The only exception is a
transient increase of ABA in both tissues after chemical but not after hand thinned or control fruit (data are from Retamales, 1988). Thinning
treatments were applied 50 days after full bloom (DAFB).
53
Table 3. Effect of the IAA-transport inhibitors TIBA and NPA, with or without in combination with
Ethrel, on the number of remaining fruit after June drop and on IAA export of Coxs and Elstar apple
fruit (1987). Samples were taken 6, 9, and 16 days after treatment.
Treatment Fruit/100 ower clusters IAA export (ng/fruit) at 6, 9 and 19
days after treatment
Coxs Elstar Cox Elstar
6 9 16 6 9 16
Control 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 night
temperatures.
Of particular interest in this respect is the frequent
observation that some of the thinning chemicals are
only effective when applied to the leaves, whereas
application to the fruit itself is ineffective. BA and
particularly NAA belong to this group (Green et al.
1992, Dennis this Vol.) whereas Carbaryl and Ethrel
are only effective when directly sprayed to the fruit
(Knight 1983, Bangerth, unpubl.). This again raises
the important question as to whether these thinning
chemicals exert their effect on IAA transport directly
or indirectly.
8. Interactions between environmental variables,
orchard practices, and correlative abscission of
young fruit
Both environmental factors and horticultural practices
are obviously responsible for a signicant part of the
variability encountered during thinning with bioreg-
ulators. Beside affecting uptake and metabolism of
thinning chemicals (see Schnherr et al., this Vol.),
the environment as well as orchard practices have a
strong inuence on the correlative behaviour of the
tree which in turn has an effect on fruit set and fruit
drop. Only some of the most inuential factors will be
considered below:
8.1 Light intensity and light quality
Shading of trees is a most efcient method to reduce
the intensity of light intercepted by the tree can-
opy. Beyond that, shading has a considerable thinning
effect on a number of different fruit species (Byers and
Wolf 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 average
daily sunlight is necessary. It has been frequently sug-
gested that the decreased photosynthetic activity and
the resulting limited carbohydrate availability to the
fruit might be the main or the only reason for the
observed thinning effect. The main rationale behind
this 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 articial shad-
ing also changes light quality giving a higher far red
proportion. Because far red increases abscission and
reduces 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 IAA
transport rates. In fact, Green et al. (1986) were able
to reduce drop of young apple fruit by a short pulse
of red light which increases IAA transport (Mao et
al. 1989) during the night. Further, Kondo (1989)
was able to show that three applications of GA
4
(100
ppm) during the shading period diminished drop of
shaded fruit up to 95%. Since it is unlikely that GA
4
affected carbohydrate availability under the low light
conditions, this effect of GA
4
may be explained by the
greatly stimulated IAA export from young fruit after
such a treatment (Callejas and Bangerth 1997). The
often accepted mono-causal hypothesis on the action
of shading, therefore, needs a more thorough exam-
54
ination considering red: far red light affected auxin
transport possibly mediated by a red-light effect
on gibberellins rather than on auxins as an addi-
tional possibility for the stimulation of the fruit drop
observed.
8.2 Temperature
Temperature, in particular night temperature, has
already been discussed as a factor strongly affecting
fruit abscission, IAA transport and ethylene produc-
tion alike. Opposite to the effect of a reduction of light
intensity, high night temperature increases the growth
rate of fruit and shoots while enhancing abscission. At
rst glance this seems to exclude carbohydrate limita-
tion as a mode of action for the observed temperature
effect. However, this high temperature effect is mainly
restricted 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 and
limitation. Thus, here again, a more careful examin-
ation of the two alternative explanations of the high
night temperature effect, and their interrelationship,
is needed. Prevailing temperatures affect fruit reten-
tion not only in the way discussed above but they also
have a strong inuence on the number of seeds per
fruit through their effect on the activity of bees and
the longevity and viability of unfertilised ovules. Seed
number is one of the main factors determining which
fruit in a cluster will abscise (Wertheim1971) and may
be as important as primigenic dominance. High seed
number of a lateral fruit, which otherwise has a low
probability of survival because of its low ranking in
the dominance hierarchy, may prevent its abscission.
Seed number also strongly determines IAA transport
rate (Figure 1). Fruit with zero seeds and no tend-
ency for parthenocarpic development, have a very low
IAA transport rate and usually abscise (Bangerth et al.
1989). However, seeded fruit show a strong increase
in IAA export as seed number increases up to about 8
to 10 seeds (Callejas and Bangerth 1997, and unpubl.
results). However, given the same number of seeds
per 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 the
later 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 efciency
of thinning. Their inuence is usually explained by
their effect on the vegetative growth of bourse shoots
or shoots near fruit or fruit clusters, which then, by
competition for carbohydrates, change fruit drop. In
fact, by removing the tips of growing shoots Quin-
lan and Preston (1971) and Grauslund (1978) showed
an increased fruit set, which demonstrates the neg-
ative effect of vegetative growth on fruit retention.
However, Gruber and Bangerth (1990), by nding
a considerable increase in IAA export from apple
fruit after bourse shoot tip removal question at least
a mono-causal explanation via carbohydrate shortage.
A correlative inhibition of IAA export of fruit by
strongly growing shoot tips seems, therefore, more
appropriate.
It seems conceivable that where shoots, adjacent to
fruit, are growing vigorously their high level of IAA
export results in a correlative inhibition of IAA export
from young fruit. Corresponding with this assump-
tion, IAA export from shoot tips is increased by
the application of gibberellins, which stimulate shoot
growth, while application of growth retardants such
as Alar or prohexadione-Ca, will have the oppos-
ite effect (Callejas and Bangerth 1997). The latter
aspect is particularly interesting since Browning et al.
(1992) showed that paclobutrazol transiently increased
extractable IAA in shoot tips, demonstrating the inde-
pendence of auxin transport fromthe extractable auxin
concentration in the shoot tips. Contrary to expecta-
tion, however, gibberellin as well as prohexadione-Ca
treatments have little inuence on fruit drop. This may
be explained by our unpublished results, which show
very similar effects of these substances on IAA export
both from fruit and shoot tips, leaving the resultant
correlative interaction between fruit and shoot more
or less undisturbed.
Other horticultural procedures, such as bending
and girdling of shoots, are known to have signic-
ant effects both on vegetative growth of treated shoots
as well as on the retention of fruit growing on these
shoots. Horizontal bending of vertical growing apple
shoots is well known to reduce shoot growth and
increase fruit retention (Robbie et al. 1993). Bending
or 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 auxin
concentration of the treated apple shoots. Beside these
effects, bending causes a long-lasting reduction in
55
IAA export from the shoot tips. Similarly, girdling
consistently decreased shoot tip IAAexport while con-
siderably increasing export out of fruit (Figure 5),
which corresponds with the reduced fruit drop after
such treatments.
The correlative nature of these shoot/fruit IAA
transport interactions can be demonstrated by, for
instance, removal of fruit which stimulates shoot IAA
export and vice versa as shown above for shoot tip-
ping. In addition, in some cases the function of the
removed organ could be replaced by applying auxin
to the cut surface, indicating the probability that com-
petition for carbohydrates may not be the main factor
involved.
9. Conclusions and possible prospects
An attempt has been made to demonstrate that abscis-
sion of young fruit at certain periods cannot be
explained by the model developed for leaf- or fruit-
explants. Young fruit abscise because of the correl-
ative inuences exerted on them by more dominant
fruit and/or shoots. The signal that transmits these
correlative events is the basipolar transport of IAA.
This uni-directional transport has a multidirectional
component at junctions where two or more auxin
streams from organs (fruit or shoot) with different
degrees of dominance meet (see Figure 1 and Bangerth
1989). At these junctions, the auxin stream of the
more 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 fruit
growth. More importantly, this autoinhibition mechan-
ism down regulates IAA transport through the AZ of
these fruit and nally triggers their abscission. Ethyl-
ene is necessary for the nal step(s) in this process,
but, contrary to abscission induced by senescence, is
not the initial driving signal.
Experimental results fromour own research as well
as from literature are presented to support the above
hypothesis on correlative abscission. Since most of
these experiments have been conducted on apple and
peach, their validity for other fruit species requires
further experimentation.
In spite of the evidence presented above, correl-
ative abscission, as distinguished from senescence
abscission, may not be the only triggering mechanism
in the abscission process of young fruit. In fact, there
still exists a considerable controversy as to whether
carbohydrate availability or limitations in allocation
(Bustan et al. 1995) contributes to natural or induced
fruit abscission. Most certainly, both alternatives,
assimilates as well as hormones, must be considered.
However, it is difcult to view carbohydrate limitation
as a direct trigger of the abscission process, because, in
this case, it would be complicated to explain why most
tree fruit show certain periods of increased fruit drop
and why only particular fruit are destined to abscise
rather than all being retained only to grow smal-
ler. It seems more reasonable that assimilate short-
age, like many environmental events, intervenes in an
unknown way in the described correlative IAA signal
process.
The ecological advantage for the correlative
abscission system is that it may, to some extent, anti-
cipate carbohydrate shortage and produce a reaction
accordingly (see above and Stephenson, 1981). This
could mean supporting a smaller number of fruit/seed
to maturity in contrast to lose most fruit prematurely
because of carbohydrate limitation. Where fruit set is
heavy, the slower-growing dominated fruit are more
likely to abscise rst, whereas the dominant, most
competitive and eventually larger fruit survive. In this
way, the ecological meaningful system turns out to be
also of horticultural advantage, since it is the larger
fruit that earns the better price.
Correlative abscission is a process affected by
numerous environmental and intrinsic variables, and
is one of the most difcult obstacles for a successful
thinning strategy employing bioregulators. As shown
above, IAA autoinhibition for a particular fruit is the
outcome of the IAA transport rates of all neighbouring
fruits and shoots, which by themselves are affected by
factors such as time of fertilisation, seed number, other
hormones, temperature, light, carbohydrate availabil-
ity etc. Interference with these processes by applying a
thinning chemical usually will affect not just the IAA
signal of the weaker fruit intended to be removed but
the IAA export of the other generative and vegetative
organs as well. A thinning treatment which selectively
affects IAA transport only of strongly dominated fruit
is, therefore, understandably difcult. As an example,
the application of an ethylene generating compound,
such as Ethrel, will reduce the IAA export out of fruit
and of shoots alike. In this way, the correlative inhib-
iting effect, for example, of the bourse shoot tip is
reduced but fruit drop may not change because of a
similar reduction in IAA export from the fruit as well.
Another example may be the application of BA. The
mode of action of BA as a thinning chemical is cer-
56
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. This
is presumably the time when fruit abscission is determined. Percent abscission (right hand side of the gure) was recorded after June drop, 32
days 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 tip
after girdling).
tainly different fromEthrel and may involve a transient
stimulation of the growth of lateral side shoots (Green
and Autio 1990, Elfving and Cline 1993). By virtue of
this, the IAA transport out of all these newly released
lateral buds may correlatively inhibit IAA transport
from fruit leading to the abscission of some of the
them. Recent results by Bianchi et al. (unpubl. res-
ults) support this assumption. If this over-simplied
assumption 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 acts
via leaves and Ethrel via fruit.
What presently can be achieved by the application
of thinning chemicals is always only a disturbance
of the balance between the correlatively acting IAA
transport streams. By gaining a better knowledge of
these complicated interactions one may nally be able
to design more reliable and more environmentally
friendly thinning compounds. An alternative to this
would be the construction and implementation of a
chimeric abscission gene coupled to an induceable
organ specic promotor. That goal, however, is for the
future.
Acknowledgements
The author is greatly indebted to Dr. J. D. Quinlan for
his critical reading of the manuscript. Financial sup-
port by the German Research Organisation (DFG) is
greatly acknowledged.
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