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dissertation entitled

THE USE OF TERBACIL AS A TOOL TO
ESTABLISH A PHOTOSYNTHETIC THRESHOLD
IN APLLES

presented by

EDGARDO J. DISEGNA

has been accepted towards fulfillment
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MASTER HORTICULTU-RE

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THE USE OF TERBACIL AS A TOOL TO ESTABLISH
A PHOTOSYNTHETIC THRESHOLD IN APPLES

BY
Edgardo J. Disegna

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE

Department of Horticulture

1994

ABSTRACT

THE USE OF TERBACIL AS A TOOL TO ESTABLISH
A PHOTOSYNTHETIC THRESHOLD IN APPLES

BY
Edgardo J. Disegna

Ten-year—old apple trees (nalug domestic; Borkh.) cv.
Redchief 'Delicious' carrying either heavy or light fruit
loads were sprayed with terbacil, [5-chloro-3-(1,1-
dimethylethyl)-6-methy1-2,4(1H,3H)-pyrimidinedione)], a
photosynthetic inhibitor at 63 ppm + surfactant X-77 (1.25 ml.
1*) at: 15, 30, 60, 80, 100, and 145 days after full bloom
(DAFB) and compared with a control.

Inhibition of photosynthesis (Pn) at 15 and 30 DAFB
induced fruit abscission, which was markedly higher for trees
having a high crop load. Both treatments significantly reduced
yield by reducing fruit number. Pn inhibition at 30, 60, 80,
and 100 DAFB reduced return bloom. Terbacil at 63 ppm plus
surfactant caused a 50-60% reduction in Pn, but Pn recovered
13 days after application. Pn and the ratio variable
fluorescence to maximal fluorescence (FV/Fm) were
significantly correlated (r = 0.7, Y = 3.21 x (10.24)‘). No
differences were found in total terminal shoot growth, cold
hardiness, soluble solid concentration (SSC), fruit firmness,

density of the fruit or fruit color.

DEDICATION

To my parents. To Maryflor and Coqui for all their
support while I was studying at MSU. To Ing. Agr. Alberto C.
Ferreri (1919 - 1987) who introduced me to the world of the

viticulture.

ACKNOWLEDGMENTS

I would like to express my sincere thanks to my major
professor, Dr. James A. Flore, for his advise, support and
friendship throughout my Master's program.

I am also grateful to Dr. Frank G. Dennis Jr. for all his
suggestions and assistance.

My thanks to the members of my committee: Dr. James
Johnson, Dr. Ronald Perry.

I am grateful for the help, friendship and comradery of
Mark Hubbard, Lynne Sage, Sarah Breitkreutz, Tom Fernandez and
Rebecca Smith among others in the department.

Finally, my special thanks to my country, Uruguay, and

the authorities of I.N.I.A. Uruguay for the economic support.

ii

TABLE OF CONTENTS

Page
LISTOFTABLESOOOOOOOOO. OOOOOOOOOOOOOOOOO O ...... 00.00.00.000v
LISTOFFIGURES..... ................................. .....vii

LISTOFSYMBOBANDABBREVIATIONS00000000000000000000.000000x
LITEMTUREREVIEW ....... 0000000000 0000000000000000000000 0001

Factorsaffectinanpotential.........................3
Light levels to net photosynthesis (Pn) ................3
Lightthresholds formaximumPn........................5
Effectofcropload....................................6
SeasonalchangesinPn.................................9
Effectoanonproductivity..........................11
Relationship between Pn and yield . ..... ...............11
Effects of light on fruit production and quality . . .. . .16
Light levels and flower bud formation .................16
Lightlevelsandfruitset............................17
Lightlevelsandfruitsize...........................19
Lightlevelsandfruitguality........................20
LightlevelsandSLw..................................22
Effects of defoliation by diseases-insects . . . . . . . . . . . . 22
Damage thresholds .....................................22
Effectoanoncoldhardiness 27
Effectsoftimeof leafremoval 28
Removal of spur leaves vs. shoot leaves ...............28
Photosynthetic inhibition .............................29
Selective inhibitors of photosynthesis ................29
Mechanism of action of photosynthetic inhibitors . . . . . . 30
Mechanismofactionofuracils........................31
Uracils metabolism ....................................33
Determination of herbicide inhibition by fluorescence .34
The use of Terbacil as thinning agent 36
Literature cited ......................................39

INTRODUCTION ............... ....... ... ......... .............50
HATERIALSANDMETHODS...... ..... ...........................51

iii

RESULTS 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 061
DlstSION 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 130
SUMMARYANDCONCLUSIONSHHHH ..... . ........... ..........149

LITEMTURECITED0000000000 00000 00000000000 00000 0000000000152

iv

Table

LIST OF TABLES

Page
Effect of terbacil (63 ppm) treatment on Fv/Fm
values and percentage of photosynthetic efficency
reduction with respect to the controls 1 and 7
days after each terbacil treatment, Redchief
'Delicious' atCHES 69

The effect of Terbacil treatment (63 ppm) on
Redchief 'Delicious' leaf chl a, b, P chl, and
total chl content over time at HTRC ..................70

Fruit growth rate (mm/day) of king fruit for the
period 7-10 days after treatment with terbacil
RedChief 'DeliCious. ' CHES' 1993 0 0 0 0 0 0 O 0 O 0 0 0 0 0 0 O O O O O .99

The effect of terbacil (63 ppm) applied to

to Redchief 'Delicious' at different times during

the growing season on percentage of fruit by size

on trees with a high initial crop load at CHES ......100

The effect of Terbacil (63 ppm) applied to

Redchief 'Delicious' at different times during

the growing season on percentage of fruit by

size on trees with a low initial crop load
atCHES.............................................101

The effect of terbacil (63 ppm) on fruit weight
on percentage of large fruit (> 8.3 cm) at harvest
on Redchief 'Delicious' at CHES .....................102

The effect of terbacil (63 ppm) on total number

of fruits, total production per tree, fruit number

and production per cm2 trunk cross section area

(TCSA) at harvest (10/07/93) for trees with heavy

crop load, Redchief 'Delicious', CHES ...............107

The effect of terbacil (63 ppm) on the total

number of fruits, total production2 per tree,

fruit number and production per cm2 trunk section

area (TCSA) at harvest (10/07/93) for trees with

low crop load, Redchief 'Delicious', CHES ...........108

10

Shoot growth (mm/day) for the period 7-10 days
after treatment with terbacil (63 ppm), Redchief
'DeliCiouS" CHES' 1993 0.0...0.0.0000000000000000000109

The effect of crop load and terbacil (63 ppm)
application at different times during the season

on cold hardiness (T5) of new shoots during

the dormant period of’Redchief 'Delicious'
atCHES.............................................129

vi

LIST OF FIGURES

Figure Page

1.

10.

Effect of terbacil concentration on Fv/Fm
(% of control) 1 to 22 days after treatment,
Red 'Delic1ou8" HTRCO 0000000.00000000000000000000063

Effect of terbacil (63 ppm) on Fv/Fm and A
of Redchief 'Delicious' at HTRC ....................65

Relationship between Pn (Y) and Fv/Fm (X)

during the following 12 days after application of
terbacil at concentrations of 50 and 100 ppm

to 'Golden Delicious'at P86 ........................68

Effects of timing of terbacil application and
cropload on fruit drop of Redchief 'Delicious'
at CHES, as of 28 July, 1993 (72 DAFB) .............73

Total fruit dropped as percentage of total
fruit produced (dropped + harvested),
Redchief 'Delicious', CHES ............... ..... .....75

Effect of terbacil (63 ppm) treatment and
timing on fruit set (number of fruit/cm2 BCSA)
RedChj-ef 'DeliCiouS" CHES 0.000.000.0000000000.00.077

Effect of terbacil on fruit retained. Number
of fruit/cm2 BCSA through the season (1993)
for high crop load Redchief 'Delicious' at CHES ....79

Effect of terbacil on fruit retained. Number
of fruit/cmz BCSA through the season (1993)
for low crop load Redchief 'Delicious' at CHES .....81

Effect of crop load and terbacil (63 ppm)

applied 15 to 100 days after full bloom (DAFB)

on fruit retention on September 23, 1993,

Redchief 'Delcious' at CHES ........................83

Cumulative fruit diameter (mm) for Redchief
'Delicious' king fruit in low crop trees
treated with terbacil 63 (ppm) at different

vii

11.

12.

13.

14.

15.

16.

17.

18.

19.

times during the season ............................88

Cumulative fruit diameter (mm) for

Redchief 'Delicious' king fruit on high

crop trees treated with terbacil at 63 ppm

at different times during the season ...............90

Absolute fruit growth (percentage of fruit

diameter increment between dates) on Redchief
'Delicious' king fruit on low crop trees

treated with terbacil (63 ppm) at different

times during the season ............................92

Absolute fruit growth (percentage of fruit

diameter increment between dates) of Redchief
'Delicious' king fruit on high crop trees

treated with terbacil (63 ppm) at different

times during the season ............................94

The effect of terbacil (63 ppm) applied

to Redchief 'Delicious' at different times

during the growing season on percentage of

fruit in six size categories on trees with a

high initial crop load .............................96

The effect of terbacil (63 ppm) applied

to Redchief 'Delicious' at different times

during the growing season on percentage of

fruit in six categories on trees with a

low initial crop load ..............................98

The effect of Pn inhibition (63 ppm) application

at different times of the season on the

number of fruit (fruit/cm2 TCSA) at harvest

for Redchief 'Delicious' at CHES ...................104

The effect of terbacil (63 ppm) application

at different times during the season on

final yield (Kg/cm2 TCSA) of Redchief

'Delicious' at CHES ................................106

The effect of crop load and terbacil (63 ppm)
application at different times during the

season on fruit soluble solid content at

harvest of Redchief 'Delicious' at CHES ............111

The effect of terbacil (63 ppm) application

at different times during the season on

fruit firmness at harvest for high and low

loaded trees of Redchief 'Delicious' at CHES .......113

viii

20.

21.

22.

23.

24.

25.

26.

The effect of terbacil (63 ppm) application

at different times during the season on

fruit density at harvest for high and low

loaded trees of Redchief 'Delicious' at CHES .......115

The effect of terbacil (63 ppm) application

at different times during the season on

final shoot lenght on high and low crop

loaded trees of Redchief 'Delicious' at CHES .......117

The effect of terbacil (63 ppm) application

at different times of the season on shoot

growth of Redchief 'Delicious', CHES, on

trees with a low crop load .........................119
The effect of terbacil (63 ppm) application

at different times of the season on shoot

growth of Redchief 'Delicious', CHES, on

trees with a high crop load ........................121

The effect of terbacil (63 ppm) application

at different times during the season on

water sprout production of Redchief 'Delicious'

at CHES ............................................124

The effect of terbacil (63 ppm) application

at different times during the season on

return to bloom (cluster flowers/cmz BCSA)

the following year (1994) on low and heavy

crop load trees of Redchief 'Delicious' at CHES ....126

The effect of terbacil (63 ppm) application

at different times during the season on

final fruit set (number of fruit/cm2 BCSA)

on low and high crop load trees of Redchief

'Delicious' at CHES ................................128

Appendix

1.

Temperature (°C) and precipitation (mm)
at CHES during the growing season 1993 .............162

ix

BCSA
CHES
Chl
Chl a
Chl b
DAFB
FS
Fv/Fm
HTRC
PAR
PSII
PSG
Pmax

PPFD
PPm

SSC
SLW
TCSA

LIST OF ABBREVIATIONS

Net carbon dioxide assimilation (molar units)
Branch cross-sectional area

Clarksville Horticultural Experiment Station
Chlorophyll

Chlorophyll a

Chlorophyll b

Days after full bloom

Full sunlight

Variable fluorescence/maximum fluorescence
Horticultural Teaching and Research Center
Photosynthetically active radiation
Photosystem II

Plant and Soil Greenhouses

Maximum leaf photosynthesis

Net photosynthesis (mass units)
Photosynthetic photon flux density

Parts per million

Correlation coefficient

Soluble solids concentration

Specific leaf weight

Trunk cross-sectional area

Temperature required to kill 50% of samples

LITERATURE RBVI EU

LITERATURE REVIEW

The importance of photosynthesis to plant productivity is
evident, for 90-95% of the dry weight of plants is derived
from photosynthetically fixed carbon (Flore and Lakso, 1989).
As much as 70% of a fruit tree's annual assimilation of
carbohydrate is often partitioned into fruit. Yet the tree
must have sufficient carbohydrate for maintenance respiration,
to form shoots and roots, to initiate and develop flower buds
for the next season, and to provide energy to survive the cold
stress of winter. Additional physiological activities such as
transpiration and respiration must also be considered as
carbohydrate demanding processes (Faust, 1989).

Fruit tree productivity is dependent on the efficiency of
photosynthesis and the allocation of photosynthates to
economic end products (DeJong, 1986).

The flow of carbon during early growth of apple trees is
dependent on both stored reserves and currently produced
photosynthates (Johnson and Lakso, 1986). The relative
importance of these two components on the early growth of
different organs is still not well understood. The leaf area
of trees develops rapidly during the spring (greater than 50%
within 30 DAFB) up to a maximum value, then becomes stable
during midseason and finally decreases when leaves start to
fall during autumn (Faust, 1989). Leaf area development is

dependent upon degree day accumulation, and begins before

1

2
flower buds open. Spur leaves are the first to develop after
bud break and comprise the majority of the tree canopy until
a few weeks after bloom. A high degree of spur formation is
desirable in apple to increase productivity. The leaf area is
relatively high in this species as compared with others that
develop leaves only on shoots (Faust, 1989).

Johnson and Lakso (1986) developed a computer model
simulating the carbon balance of a growing 'Jonamac' apple
shoot in order to estimate the time of first net carbohydrate
export from the shoot. That model was based on measurements of
net photosynthesis, dark respiration, and dry weight of the
different components of the shoot. The model showed that a
shoot growing to a final length of 50 cm became a net exporter
of carbohydrates 19 days after budbreak, when the shoot was 4
cm long with 10 unfolded leaves. A shoot with a final length
of 2 cm starts exporting at 15 days after budbreak. According
to this model, short shoots export more carbohydrates than do
long shoots until 36 days after budbreak, indicating that
short shoots supply greater amounts of carbohydrates to the
rest of the plant. during this early' period. The ‘model
estimated a total import of carbohydrates from reserves of
about 165 mg for the long shoot and 80 mg for the short shoot.
In each instance, these reserves only accounted for about 20%
of the total carbohydrates used by the shoot up to that point.

The remainder was supplied by current photosynthesis.

3

Watson and landsberg (1979) have concluded that apple
spur leaves become net exporters of carbohydrates when they
reach 5% of their final size. In other species, such as tomato
and cucurbits, export begins at about 35% of final size.
Watson and landsberg (cited by lakso, 1984) estimated that
under English growing conditions spur leaves began to export
carbohydrates within 10 days of beginning growth. In contrast,
extension shoots do not exhibit net carbohydrate export to the
tree until they reach 12-15 unfolded leaves about; 3-4 weeks

after full bloom (Lakso, 1984).

Factors affecting Pn potential

Variables under field condition which affect maximum Pn
potential of apple are: leaf age and position, leaf exposure
to light, temperature, and environmental or biological stress.

Genetic variation in carbon assimilation (A) due to
scion, cultivar, or rootstock does not seem to be great in
apple, although it is difficult to compare rates between
studies (Flore (and. Lakso, 1989). Flore (and. Lakso (1989)
reported a maximum photosynthetic rate for apple in the order
of 15.7 i 5.6 umol C0211!"2 s”. This value is influenced by the
environment, stage of development, fruit load, and time of
determination and equipment used.

- Light levels to net photosynthesis (Pn).

Palmer (1986) found a linear relationship between light

4
interception and both total dry matter production and fruit
weight in apple. This observation agree with those of Monteith
(1977) and.Gallagher and Biscoe (1978; cited by 0rt and Baker,
1988), who reported a strong correlation between total dry
matter production and the total amount of light interception
in barley, potato, sugar beet and wheat.

Both by experimentation and definition light is obviously
the most important environmental factor in photosynthesis of
fruit trees (Lakso, 1986; Flore, 1994). The response of Pn to
increasing irradiance is a hyperbolic response characteristic
of C3 plants. In general, photosynthesis saturates between 400
and 600 uE m'2 s'1 for individual apple leaves (Faust, 1989).
In peach, cherry and other fruit trees this value is slightly
higher and may range between 400 and 700 uE‘m'2 s”.

Single-leaf photosynthesis is saturated approximately at
20-40% of full sunlight, but the saturation of a full tree
canopy is considerably higher due to the variety of leaf
exposures and inherent differences between sun and shade
leaves (Lakso, 1986; Lakso and Seeley, 1978).

Marini and Marini (1983) reported that apple leaves
developing 0.5 m from ‘the tree periphery' had lower Pn
potential, dark respiration and SLW than peripheral leaves.
Kappel and Flore (1983) reported that.peach leaves under’shade
became light-saturated between 400 and 600 uE m'2 s", while

full-sun leaves became light-saturated at 700-900 uE m'2 s”.

5

However, Lakso and Barnes (1978) demonstrated that
interior leaves could be relatively efficient, or at least
instantaneously respond to incoming light when a sunfleck
strikes them. They found that apple leaf photosynthesis was
more efficient under short term fluctuating light than under
continuous light. The authors reported an 85% higher
photosynthetic rate in apple leaves exposed to alternating
light than in those exposed to continuous high light.

0rt and Baker (1988) mentioned that the majority of the
photosynthesis occurring under field conditions occurs at non-
saturating light levels. In their opinion, plants have evolved
numerous photosynthetic mechanisms and chloroplast features to

ensure efficient photosynthesis at low light levels.

- Light thresholds for maximum Pn

According to Heinicke and Childers (1937) and confirmed
by others (Flore and Lakso, 1989), 25 to 30% of full sun
intensity is considered to be the minimum for the maximum
photosynthetic rate in apple. These authors in also noted that
areas that received less than 30% of full sunlight were
unproductive. Therefore, this level of light is considered as
a minimum threshold for light.

According to Rom (1990), approximately 30-50% of full
sunlight (600 - 1000 umoles photon flux, 400-700 nm) is

required for maximum Pn rates. Shading apple shoots to levels

between 50 to 100% ambient sunlight caused only a 10-50%
reduction in Pn. However, shoots grown in 25% sunlight had Pn
rates of 30-40% of full sunlight. Thus, 30% full sunlight is
a critical threshold value for maximum photosynthetic activity
and carbohydrate production.

Ninety percent shading reduced dry matter production of
potted apple rootstocks to 6 to 12% of that of controls
(Priestley, 1969). Similar results were reported by Barden
(1977) where reducing the irradiance by 80% caused a 50%

reduction in dry matter in apple trees.

- Effect of crop load (sink strength)

Carbohydrate sinks are either reproductive or vegetative
(Flore and Lakso, 1989). Sink strength is defined as sink
activity times sink size, and'varieS‘with.season, depending on
the stage of fruit and vegetative development, and with the
life cycle of the tree.

Carbohydrates are preferentially partitioned to the
fruit. Therefore, heavy fruit loads in apple trees result in
reduced leaf area as compared with trees having light loads.
Total dry matter is generally the same or higher in fruiting
trees (Faust, 1989). For example, Maggs (1960) found that

cropping apple trees produced more total dry matter per unit

7
area than did non-cropping trees. The presence of fruits leads
to higher rates of Pn (Hansen, 1967: DeJong, 1986: Flore and
Lakso, 1989; Sams and Flore, 1983).

Fruits also affect translocation and distribution of
photosynthates. The growth in diameter of branches and of the
trunk is depressed when a large amount of fruit is produced
(Hansen, 1967) . Maggs (1963) reported that increased fruit
production occurred at the expense of root growth. The author
hypothesized that the assimilates produced in the leaves were
diverted to the fruit rather than moving down the stem to the
roots. Translocation studies conducted with 1"C022 by Hansen
(1967) to shoots with and without fruits, have demonstrated
that nearly 90% of the 1"'C assimilated by the leaves can be
transferred to the fruits close by. The majority of the 1"C-
label was transferred during the first 4 to 5 days. Leaf “C
was reduced more rapidly in shoots with fruits than in those

2 of leaf area was 1.5

without. The uptake of 1"C02 per cm
greater in fruit-bearing shoots than in those not containing
fruits. These data imply that fruit removal should reduce Pn
in adjacent leaves.

Avery (1969) reported that in the apple cv. 'Worcester
Pearmain' fruiting suppressed the total dry weight increment
produced, but that the leaf efficiency (calculated as g dry
matter produced per dm2 of leaf surface) was greater on

fruiting trees. The same author concluded that "trees of high

fruitfulness produced as much, or even more, than deblossomed

8
trees because of increased photosynthetic efficiency”. He
reported values of 0.81 and 0.60 Kg m'2 for bearing versus non-
bearing apple trees for the growing season up to harvest.
These results are close to those of Proctor et al. (1976) who
found values of 1.07 and 0.62 Kg m'2 for fruiting and de-
fruited trees, respectively.

Proctor et a1. (1976) reported that fruit removal had no
effect on the Pn of the adjacent leaves during intervals of up
to 0.5 hr. The discrepancy in the results obtained may be due
to the different time periods involved. For example, Hansen's
data were obtained after several days of the application of
labelled carbon; whereas in the.experiments of Proctor et al.,
0.5 hr may be insufficient to reflect the adjustment in
"source-sink" balance to cause reduced Pn. These results agree
with that found by Rom and Ferree (1986), who observed that
the Pn of intact spur leaves of 'Golden Delicious' apple trees
were similar, regardless of the fruiting condition of the
spur.

Roper et al. (1988) reported no difference in Pn in
fruiting vs. non-fruiting cherry plants on either a seasonal
or a diurnal basis. They suggested that Pn rates in sweet
cherry in the fields were primarily affected by ontogeny and
environment and not by sink strength.

Gucci and Flore (1990) observed different responses on Pn
of plum trees depending on the time of the season that fruits

were removed. Defruiting at pit-hardening stage decreased C02

9
assimilation by 25% within 24 hours, whereas removing mature
fruits did.not affect it. There is evidence from other studies
with apple that the fruit is dominant over other sinks in the
plant and may exert significant control over leaf activity. In
various experiments to manipulate the balance between fruit
and leaf area, reducing the fruit load resulted in
accumulation of leaf sugar and starch and, conversely,
reducing leaf area with constant fruit load resulted in
smaller concentrations of leaf sugar (Treharne, 1986).
Priestley (unpublished, cited by Treharne, 1986) has
demonstrated that the leaf responds to change in sink demand
by a rapid change in rate of assimilate export; in apple this

is mainly reflected in the sorbitol component.

Seasonal changes in photosynthesis

Heinicke and. Childers (1935, cited. by Faust, 1989)
determined the total photosynthesis of a young bearing apple
tree through the year. Their investigation showed that early
in the season as the leaf area expands, the net photosynthesis
increases, reaches a maximum and then declines as the leaves
senesce. Throughout the season the most important factor
governing this process was light level (irradiance) and the
total amount of light intercepted by the tree canopy.

Light interception and distribution are not only

dependent on the tree size, spacing, row orientation, canopy

10

shape, and training system, but in the seasonal development of
the foliage. Several studies have concluded that apple leaf
photosynthesis reaches a maximum just before or at the time of
full expansion. A different response was observed for fruiting
and non-fruiting shoots (Palmer, 1986b). According to Ghosh
(1973) the maximum.assimilation.rates in apple occurred in his
studies, at the end of June and the minimum rates at the end
of July for leaves of fruiting shoots. Toward the end of the
‘vegetativejperiod.Ghosh (1973) found that the leaves of fruit-
bearing shoots showed a slightly higher rate of
photosynthesis, whereas leaves of shoots without fruits showed
the opposite trend. Kennedy and Fuji (1986) found that as
apple leaves enlarged, the rate of photosynthesis increased
rapidly to a maximum of 40 to 43 mg COde"2 hr”. Thereafter,
photosynthetic rates remained constant (30 mg C02dm"2 hr”)
for several weeks before declining toward the beginning of
senescence.

In orchard studies, Kennedy and Fuji (1986) observed two
periods during the growing season when the rate of
photosynthesis in leaves of flowering or fruiting spurs was
10-20% higher than the leaves on non-flowering or non-fruiting
spurs. The first period was during flowering, and the second
during fruit maturation. Palmer (1986b) observed a different
pattern of Pn according to the type of leaf (spur vs shoot
leaves). In his study spur leaf Pn declined from early'June to

late October. During August, Pn rate varied considerably

11

between spurs of different ages. Pn in extension shoot leaves
showed a later maximum, and during August and September Pn
rate‘was three times greater than for spur leaves. The rate of
decline in photosynthesis after a maximum in both types of
leaves was associated with a decline in stomatal and mesophyll
conductances.

Rom (1990) studied the seasonal variation.of carbon balance in
spur leaves in apple. When "supply" (Pn on a daily per spur
basis) and "demand" (fruit relative growth rate) curves were
plotted against time, demand equalled supply at bloom, after
which supply exceeded demand for approximately a 40 day

period.

Effect of Pn on productivity

- Relationship between photosynthesis and yield

Evidence for a direct relationship between improved
photosynthesis and productivity has been elusive. In most
cases, there appears to be no direct association between
maximum leaf photosynthetic rates (Pmax) and yield in
perennial tree crops (Charles-Edwards, 1978; Ozbun, 1978;
Nelson, 1988: cited by DeJong, 1990). DeJong (1990) pointed
out that the lack of correlation between Pmax and productivity
reflects the fact that leaf Pmax is not an appropriate

indicator of total carbon assimilation by plant canopies.

12

According to Lakso (1980) four factors determine the
production of apple fruits: 1) light interception by the
canopy leaves, 2) potential photosynthetic capability of the
leaves, 3) internal and external factors that determine actual
photosynthesis and 4) distribution of the photosynthetically
fixed carbon to the developing organs of the tree.
Nevertheless, a canopy of high light interception, high
photosynthetic potential and high actual photosynthesis does
not guarantee a high yield of quality fruit. Therefore, the
distribution of the photosynthetic products to the various
organs in the tree is critical.

Flore and Sams (1989) , suggested that the carbon must not
only be produced, but be partitioned efficiently to fruit for
the current year's crop and to flowers for the next year's
crop. The lack of a relationship between Pmax and yield
emphasizes the importance of sink strength in determining
yield. This, coupled with evidence for feedback effects on
Pmax suggest, that sink strength rather than Pn is the primary
factor limiting yield in many crops (Chalmers, 1975).

Circumstantial evidence exists to support the hypothesis
that there is a direct relationship between yield and Pn
(Seely, 1978). Some of this has been reviewed by Moss (1976)
and Zelich (1971). This evidence includes decreased crop
yields in shaded conditions, the yield reduction resulting
from defoliation, enhancement of growth and productivity by

atmospheric C02 enrichment, and faster crop growth rates in

l3
photosynthetically efficient species.

Flore and Sams (1986) have demonstrated, based on sour
cherry studies, that photosynthesis may limit cropping in this
species. They proposed that, when considering whether
photosynthesis is limiting yield, a distinction should be made
between photosynthetic rate (C02 fixed per unit area) and
total carbon fixed, which also takes into account the leaf
area and leaf area duration. .According to the authors,
photosynthesis could limit growth of the crop during stage
three of fruit growth in sour cherry, if severe defoliation
occurs due to insect attack or disease, if environmental
conditions are not conducive for optimum photosynthesis, or if
the leaf to fruit ratio is less than 2. They also pointed out
that in most cases photosynthetic capacity is large enough in
cherries to provide carbohydrates even for relatively large
crops, but photosynthesis could limit yield when fruit crop
loads are high and/or when stresses occur during stage three
of fruit development. In some cases overcropping can limit
carbohydrate storage and vegetative growth to the extent that
cropping or plant health might be adversely affected (Flore
and Lakso, 1989: Flore and Howell, 1987).

Chang et al. (1987) pointed out the importance of the
effects of Pn on components of tree yield. Two major
components are important. in. «determining fruit tree

productivity: fruit number and fruit weight. Both components

are obviously influenced by Pn. Fruit weight is dependent on

14
the leaf area and leaf number/fruit, whereas fruit number is
usually determined not only by current photosynthesis that
ensures a high degree of fruit set but also by the previous
year's photosynthesis.

Hansen (1977) found a positive curvilinear relationship
between fruit growth/m3 of leaf area and crop load. The same
relationship was reported by Beers et al. (1987) who found a
curvilinear relationship between mean fruit weight and leaf
fruit ratio (LFR) in apples.

Carbohydrate levels must be high enough that, in addition to
supporting fruit and tree growth, the tree can develop
sufficient flower buds and reserves in the wood. During the
spring reserves are needed for a high fruit set, and therefore
high yield. In sour cherry Pn is limited when the leaf-fruit
ratio is less than 2.0 (Flore and Sam, 1986). Carbohydrate
shortage in apple has been reported for leaf-fruit ratios less
than 15 leaves per fruit (Faust, 1989).

Flore (1986) stated that the Pn potential in fruit crops is
under'two forms of control: 1) the environment, which directly
influences the immediate physical and biochemical reactions
and indirectly, through light exposure, affects the
morphological development of the leaf, and 2) through sink
demand and some type of feedback signal from the sink itself.
He emphasized that the anpotential is seldom reached in fruit
trees. Thus, when improvement of crop is considered,

photosynthesis may be only one of the many important factors.

15

Studies of the effect of photon flux density (PFD) on
yield show a direct relationship between light intensity, over
a certain threshold, and yield affected through its different
components. Experiments with spinach (Jackson et al., 1991)
and lettuce (Sanchez et al., 1989) showed that a decrease in
PFD substantially reduced crop yield in these species. In
lettuce, shading, regardless of the degree, reduced growth and
yield during the heading stage of development. Similar results
were found in tomato grown under different light conditions.
McAvoy et a1. (1989) observed a strong correlation (r=0.947)
between the total yield of tomato plants and total
photosynthetic photon flux (PPF) received in the period from
anthesis to harvest.

Bravdo (1986) reported that a 25% reduction in PFD in

apple trees, cv. 'Granny Smith', by the use of net covering,
increased leaf photosynthesis and fruit yield.
In the experiments conducted the number and size of fruits
were significantly higher in the shaded trees. The author
attributed this increase to an increase in water potential
observed in the shaded trees. Reduced atmospheric stress and
increased water potential during bloom and various stages of
fruit growth can reduce fruit drop and also increase fruit
size (Assaf et al., 1982).

Any factor'that affects Pn, such as altered light levels,
injury to the leaf, defoliation of trees, markedly affects

fruit set, flower bud formation, fruit size, fruit color and

16
quality, carbohydrate distribution, specific leaf weight

(SLW), and wood hardiness.

Effects of light on fruit production and quality

- Light levels and flower bud formation

The contribution of leaves to flower bud initiation has

been established in most plants, including mangos, apple,
olives and oranges (Monselise and Goldschmidt, 1982).
The strongly negative effect of shade on flower bud initiation
has been known for a long time (Auchter et al., 1926: Paddock
and Charles, 1928). In apple trees several years of shading
have a cumulative negative effect on the initiation of flower
buds (Jackson and Palmer, 1977).

Recently investigators have attempted to evaluate the
light effect on flower bud initiation quantitatively. An
increase in radiation from 32.3% to only 37.5% of full
sunlight increased the percentage of flowering spurs in the
center of the apple tree from 13.6 to 43.8%. 30% of full
sunlight or 27% of photosynthetically active radiation (PAR)
are regarded as threshold values for flower bud formation
(Gur, 1985). A hyperbolic regression of the number of
flowering apple spurs on the "fisheye perc, sky value" in late
May, in the year preceding the counting of the flowering

spurs, has also been established (Lakso, 1980).

17

The negative effect of shade on flower bud initiation
explains the (negative effects results. of‘ densely spaced
hedgerows on flowering (Jacyna and Soczek, 1980).

Finally, Jackson and Palmer (1977) pointed out that in
some experiments they found a marked interaction between
shading and crop load in their influence, not only on flower
bud formation, but also on fruit set and size. This suggests
that the effect of shading in one year may partially'pre-adapt

the tree for such conditions in the following year.
- Light levels and fruit set

The importance of photosynthesis as the major factor
governing yield can be established by analyzing the effects of
low light levels and leaf injury/defoliation on the different
components of crop yield.

Reducing light level within the canopy 20% at bloom and
10-20% the remainder of the season by over-tree shade, reduced
fruit set 62% in 'Delicious' apple trees (Doud and Ferree,
1980). These results agree with those found by Jackson and
Palmer (1977). 'Cox's Orange Pippin' apple trees were shaded
so as to receive 37, 25 or 11% of full sunlight during the
post-bloom growing season, and their flowering and fruit
development and yield was compared with those of non-shaded
control plants. Shading reduced fruitlet retention and fruit

size and percentage dry matter in the year of shading. The

18
number of fruit per 100 flower clusters was reduced 25% by
heavy and medium shading. Moreover, trees shaded heavily
during two consecutive years produced only one-third as many
fruits per 100 flower clusters in the second year as did the
controls. Similar effects of shading on apple fruit set were
reported by Auchter et a1. (1926) and Heinicke (1977).

Conclusive studies about the effect of shading apple
trees at different times on fruit set came from the studies of
Byers et al. (1990a). Shading (92%) of Redchief 'Delicious'
apple trees for 10 day periods at different times after full
bloom showed that 10 to 30 DAFB, when fruits were 8 to 33 mm
in diameter, was the most sensitive period for inducing fruit
abscission. Similar results were obtained by Byers et al.
(1990b) with spur 'Delicious' apples. Shading trees for’4‘days
at FB + 17 days with 92% shade reduced fruit set 50%.

Byers et al. (1984) reported that abscission can be
induced in nectarines when trees are shaded 45 to 58 DAFB.
Peaches most sensitive to shade at 31 to 41 DAFB.

Early removal of spur leaves similarly reduces fruit set.
Ferree and Palmer (1982) demonstrated the importance of spur
leaves on fruit set and development. Removal of 50% 'Golden
Delicious' spur leaves at full pink reduced final fruit set.
The combination of spur ringing and removal of all leaves
resulted in a complete loss of fruit. Comparable results were
reported by Arthey and Wilkinson (1964), Llewelyn (1966) and

Lakso (1984). Lakso (1984), reported that defoliation of spur

19
leaves prior to fruit set caused severe reductions in fruit
set while defoliation of shoot leaves had relatively little
effect. Neither removal of spur leaves later in the season
(after 30-50 DAFB) or shading spur leaves after'bloom‘affected
fruit size. 0n the other hand, Rom and Ferree, 1986 reported
that later in the season, shoot leaves contribute to<continued
fruit growth. All these results pointed out the importance of
photosynthesis in fruit set.

However, partial defoliation below a certain threshold
may be overcome photosynthetic compensation (Flore and Irwin,
(1983); Layne and Flore, (1992), see below).

On the other hand, Darnell and. Martin (1988) found no
correlation between 1"C accumulation in strawberry flower
receptacles and fruit set or initial fruit growth. 1"C-labeled
photosynthate was not the source for the observed dry weight
increases. From their study they concluded that fruit set and
initial fruit growth in strawberry is not limited by the
capacity of receptacles either to mobilize current sources of

assimilates or to accumulate carbohydrates.

- Light levels and fruit size

Light penetration into trees and the relationship of this
to fruit size and color was studied by Heinicke (1966) who
found that both size and color of 'McIntosh' and Red

'Delicious' apples were correlated with degree of exposure to

20
sunlight. A linear relationship was found between light
interception and fruit dry weight (Palmer, 1986); and between
yield and leaf area/light interception (Barritt et al. , 1991) .
Fourty-five percent shade of 'Cox's Orange Pippin' apple trees
resulted in the production of high numbers of small fruits
(Jackson, 1968). Shading reduced fruit size and especially
fruit weight. Sixty-two percent shade did not affect fruit
size, but fruit color. Jackson et al. (1977) reported that
shading to 34% or 13% of full sunlight caused a decrease in
fruit size by reducing both cell size and cell number. Fruits
grown under shade had less dry matter and starch per unit
fresh weight than those grown under full sunlight. In a study
of fruit characteristics at different positions within the
tree canopy, Barritt et a1. (1987) observed that apple fruit
weight and size were greater at the top than at the bottom.
Size was correlated with the percentage of full sunlight
received by each area of the tree. The top of the trees (3m)
received 48% of full sunlight, whereas at the bottom the

percentage was 9%.

- Light levels and fruit quality

In general the better colored apple fruits occur on the
more exposed portion of the trees. Fruits from the tops, where
photosynthetic photon flux density (PPFD) is greatest, are

redder and have higher soluble solid concentration (SSC) than

21
fruits harvested with similar ground color from the tree
interiors (Marini, 1985).

Several studies have shown the importance of light on
fruit color and content of soluble solids. All of them
revealed a positive correlation between high light levels and
fruit color and sugar content (Jackson et al., 1977; Barritt
et al. 1987). Heinicke (1966) reported that color development
of Red 'Delicious' and 'McIntosh' apple was directly related
to light exposure, with best color in fruit exposed to more
than 70% of full sunlight (FS). Fruits exposed to 40-70% of FS
were adequately color; those receiving less than 40% F8 were
very poorly color. Seeley et a1. (1980) showed that apple
fruit size, red color, and soluble solids concentration (SSC)
increased linearly with PPFD for on shaded 'Delicious' limbs.
Morgan et a1. (1984) found similar relationships for 'Gala'
fruit developing at various canopy positions.

Izso and Rom (1989) observed that fruit epidermal
chlorophyll content exhibited a quadratic response, with
maximumLapparent.greenness between 30% and 60% of full sun and
decreases at irradiances above 60% of full sun.

Campbell and Marini (1992) determined a PPFD threshold
for apple color intensity and SSC. The authors found a
threshold level of 250 pmol m'2 s'1 for all fruit quality
characteristics. 0n ‘the other' hand, Saks et al. (1990)
demonstrated that development of red pigmentation had a

threshold PPFD level of 150 umol m'2 s", whereas SSC should

22
presumably have a higher threshold due to its dependence on

photosynthesis.

- Light levels and specific leaf weight

The structure of the apple leaf varies with the light
conditions under which it develops and functions (Jackson,
1980). Specific leaf weight (SLW) is highly correlated with
net photosynthesis in apple (Barden, 1977; Marini and Marini,
1983). Barden suggested that SLW might be a useful index of
the light environment previously experienced by the leaf and
of its Pn potential. Palisade cell development is responsible
for the difference in SLW of apple leaves grown under
different PPFD (Warrington et al. 1990). Studies of peach and
apple canopies have indicated that leaves in areas of the tree
receiving less than 36-40% PAR have a lower SLW than
peripheral or non-shaded leaves (Kappel and Flore, 1983;

Marini and Marini, 1983).

Effects of defoliation by diseases and insects. Damage

thresholds.

Injury to the leaf caused by diseases or insects, as well
as defoliation, can decrease Pn rate and cause economic loss.
Ferree (1978) and Ferree et al. (1986) summarized the effects

of diseases on Pn. The authors reported that powdery mildew

23

(Egggsphaera leucotricha) caused a 75% decrease in Pn 35 days
after infection. Apple scab (Venturia inaegualis) reduced Pn
20%. However, the loss of foliage induced by apple scab may
cause much more severe damage, especially when defoliation
occurs at the time of flower initiation. Pn was not reduced
until visible lesions were present and leaves did not recover
photosynthetic capacity when the disease was inactivated by
fungicides.

Ferree et a1. (1986) observed that mite infestation
decreased Pn in apple trees. As the population of two-spotted
spider mites (Tetranychus urticae) increased, Pn decreased and
the reductions appeared. to jpermanently' destroy' the
photosynthetic capacity of the leaf. A population of 60 mites
per leaf caused a significant reduction in apple Pn'three‘days
after placement on the leaf. Nine days after infection, 15
mites per leaf reduced Pn by 26%, 30 mites per leaf by 30%,
and 60 mites per leaf by 43% below the value observed in
uninfested controls. Similar results were reported by Campbell
et al. (1990) using greenhouse trees. Working with two-spotted
spider mite (Tetranychus urticae Koch) on infested Imperial
'Delicious' apple, they found that accumulation of 1200 mite
days.per leaf (MD) reduced.Pn by 40%. Field experiments showed
that 3056 MD reduced Pn only 17%.

Mites can also reduce yield in citrus. Hare et al.
(1992), using"Navel' orange (Citrus ginensi L.) reported.that

when populations of Eanonichus citri (McGregor) reached

24
densities of 2.2, 7.1 and 9.7 adult females per leaf, yield
was reduced 6.6, 9.0, and 11.4%, respectively.

The simultaneous impact of European red mite and spotted
tentiform leafminer on 'McIntosh' apple yield and quality was
studied over a three year period by Nyrop et al. (1993).
Cumulative mite days up to 500 per leaf and leaf miner
densities of 2 per leaf independently or jointly did not
affect yield or quality. However, reductions in whole tree
photosynthesis were observed. These reductions were correlated
with cumulative mite days and fruit growth, indicating that
reduction in fruit size was a good integrator of foliar damage
by spider mite.

Nyrop et al. (1993) proposed the following empirical
damage threshold densities for different insects: European red
mite - 400 mite days; spotted tentiform leafminer - 2 mines
per leaf; white apple leafhopper - 50 hopper days.

Jones (1993) studied the effect of different population
densities of two spotted spider mites in order to establish
damage levels on tart cherry. The population densities were 0,
185, 470 and 750 mite-days per leaf. Levels of over 470 mite-
days reduced photosynthesis approximately 33%. The author
suggested that preliminary economic thresholds be set at 185
mite-days per leaf.

Reaction to mite infestation varies among cultivars.
Among eight cultivars tested , Pn reduction ranged from 0 to

20%. Mites caused greater decreases in Pn of 'Delicious',

25
'Gallia Beauty', 'Jonathan', and 'Melrose' than in the other
cultivars tested (Ferree et al., 1986)

Studies of simulated defoliation have shown that removal
of part of the leaf blade does not affect Pn until more than
7.5% of the leaf is removed (Ferree et al. 1986). More than
15% has to be removed before the photosynthetic capacity on
the remaining tissue is reduced. Greater reduction in Pn
occurs when main lateral veins are severed as part of leaf
removal compared to removal of only intervenal tissue.
Reduction in Pn due to leaf injury was closely related to the
amount of cut surface exposed. Similar results have been
observed in experiments with defoliating arthropods and
artificial defoliation on peanut canopies (Boote et el.,
1980). Removal of 25% of 'the total leaf area of peanuts re*AT
1"C02 uptake by 30% and canopy C exchange rate (CER) by 35%. In
a second experiment, severe leafspot damage reduced LAI by
80%, “co,_ uptake by 85%, and canopy CER by 93%.

Proctor et al. (1982) found that at 20 mines per leaf,
spotted tentiform leafminer (Phyllonorycter’ blancardglla)
injured 33% of the apple leaf, but assimilation was decreased
by only 23%. In this study, at maximum irradiance, 10 mines
(17% leaf area loss) were needed before Pn fall below that of
the control plants. Flore and Irwin (1983) reported similar
response to mechanical injury and tentiform leafminer for
'Golden Delicious' apple. Photosynthesis was reduced when 20%

of the leaf area was removed. When one-year-old trees were

26
defoliated to 90, 80 and 70 % of the control at weekly
intervals, total tree growth was not affected at 10 or 20%
defoliation, which indicated a degree of compensation to the
leaf loss by the remaining tissue on the plant.

Sylvertsen et al. (1986) found that in citrus leaves
infested with six-spotted and spider mite Pn was depressed in
relation to the percentage of damage. However, citrus leaves
exhibited some recovery, and apparently they compensate for
mite damage, showing little loss of net gas exchange potential
at low damage levels. Similar results were reported by Layne
and Flore (1992) for sour cherry. They observed that when
defoliation does not exceed 20% the plant is capable of
compensating by increasing its photosynthetic rate. This
compensation was accounted for by a higher estimated
carboxylation efficiency and ribulose-1,5-bisphophate (RuBP)
regeneration capacity of the remaining leaves.

Studies on leaf photosynthetic responses to injury by
insects indicated that gross tissue removal did not alter
photosynthetic rates in remaining, uninjured tissue in
soybean, apple, or sunflower (Higley, 1992). In early
reproductive stages, soybean canopies with defoliation of over
70% exhibited no significant reduction in canopy
photosynthesis as compared to the non-defoliated control.
Delayed leaf senescence in defoliated plants was responsible
for this compensation.

Starck and Stahl (1986) found that partial defoliation

27

did not retard fruit growth in tomato. Partial defoliation did
not affect the final fruit dry matter, but reduced
accumulation of substances in the leaf blades. Measurements of
assimilation of “co,_ and partitioning of 1"C-substances in
tomato plants with modified source-sink relationships
(defruited and/or defoliated) showed that fruit growth was not
limited by photosynthetic production, but by the sink
capacity.

According to Flore and Lakso (1989), compensation may
occur because the remaining leaves are relieved from
constrains, i.e., carbohydrate accumulation, feedback
inhibition from sugar or starch buildup, the loss of some
inhibitory phytohormone, or increased allocation of resources

remaining leaf area.

Effect of Pn on cold hardiness

Any factor that affects photosynthesis and thus
carbohydrate accumulation, has an effect on cold hardiness.
Early leaf loss in tart cherry trees causes delayed
acclimation in the fall and more rapid deacclimation in the
spring (Howell and Stackhouse, 1973) resulting in reduced bud
survival and. decreased fruit set. The effects of’ early
defoliation carried over into the second season.

Two possible roles of carbohydrates in hardiness have
been suggested (Howell and Stackhouse, 1973). Some

investigators suggest that sugars prevent protein denaturation

28
(Faust, 1989). Some others take a more general view of the
role of carbohydrates and suggest that acclimation,
deacclimation, and reacclimation are all energy-requiring
phenomena and the role of carbohydrates is to provide that

energy.

The effects of time of leaf removal.

- Removal of spur leaves vs. shoot leaves.

Carbohydrate supply throughout the growing season is
important for fruit growth and production. Early in their
development apple fruits depend on the Pn provided by spur
leaves; the availability of carbohydrates during the first
stage of fruit growth is crucial for fruit retention.
Inhibiting photosynthesis at that time is an effective way of
thinning peaches and apples (see below) . Previous studies have
indicated that removal of spur leaves early in the season
reduces fruit set, fruit growth and fruit calcium content
(Rom, 1990). Removal of spur leaves 55-117 days after petal
fall has no effect on eventual fruit size (Faust, 1989). Rom
(1990) reported that removing spur leaves after 30-50 DAFB or
shading them after 60 DAFB did not affect fruit size. Ryugo
(1986) observed that when spur apple leaves were removed at
weekly intervals after full bloom, no flower buds formed on
spurs that were defoliated 6 to 10 weeks after full bloom.

Shoot leaves early in the season have no effect on fruit size.

29
However, shading or removing of shoot leaves later in the
season reduces the size of the fruit (Rom and Ferree, 1986).
The authors conducted an experiment on Starkrimson 'Delicious'
apple trees. Shading shoots from 60 DAFB until maturity,
reduced fruit growth and delayed maturity, but shading spurs
had no effect on either. This is further corroborated by
ringing experiments that prevented carbohydrate transport from
the shoot leaves, but not from the spur leaves, to the fruit
(Faust, 1989). Ringing bourse shoots decreased fruit size
(Ferree and Palmer, 1982) . The authors found that although
early in the season the presence of bourse shoot on 'Golden
Delicious' apple was detrimental for fruit set, later in the
season shoot leaves provide the carbohydrates needed for fruit

growth and thus, high yield.

Photosynthetic inhibition

- Selective inhibitors of photosynthesis

Several herbicides are photosynthetic inhibitors, such as
the ureas (1951), the triazines (1955) and the bipridiniums
(1960) (Van Rensen, 1989) . About 50% of all commercially
available herbicides are inhibitors of photosynthesis (Trebst,
1981) . Among this class of herbicides, terbacil (3-tert-butyl-
5-chloro-6-methyluracil) is classified as an organic herbicide

of the uracil group (Ashton and Crafts, 1977). It is used to

30
control many annual weeds, and some perennial weeds, in
deciduous tree fruit orchards, blueberries, citrus, alfalfa,
mint, and sugarcane. It is a soilborne toxicant absorbed by
the roots and translocated apoplastically to the leaves.
However, it may also be taken up by the leaves directly,
especially with the aid of surfactant materials (Izawa and
Good, 1965). Leaf chlorosis followed by necrosis is a common
response of plants following terbacil application.
Ultrastructural examination of these leaves usually reveals
abnormal and degenerating chloroplasts as well as

deteriorating membranes.

Mechanism of action of photosynthetic inhibitors

The studies of Cooke (1956) and Wessels and Van der Veen
(1956) demonstrated that photosynthetic inhibitors interfered
with the Hill reaction, which occurs in the chloroplasts. The
Hill reaction is defined as the evolution of oxygen by a
suspension of isolated chloroplasts when illuminated in the
presence of an artificial electron acceptor (Moreland, 1980).
The Hill reaction is associated with ATP formation. Therefore,
the mechanism of herbicide action involves an inhibition of
energy production. This concept was maintained as the primary
explanation of the herbicide action of herbicides for
convenience and because herbicide action was evaluated under

nonphosphorylating conditions.

31

In recent years, more sophisticated studies have been
conducted with herbicides and more is known about their
differential action. Moreland (1967, cited by Moreland, 1980)
separated herbicidal inhibitors of the photochemically induced
reactions into electron transport inhibitors and inhibitory
uncouplers. Electron transport is inhibited when one or more
of the intermediate electron transport carriers is removed or
inactivated. The site of action of most herbicidal electron
transport inhibitors studied is closely associated ‘with
photosystem II (PS II). Most of the herbicides are inhibitors
of electron flow at the functional site between the primary
and secondary electron acceptors of PS II (plastoquinone Q and
B). Inhibitory uncouplers are those electron flow inhibitors
that also have an uncoupling property on the

photophosphorylation system (Trebst, 1981).

Mechanism of action of uracils

Uracils are herbicides that block both the Hill reaction
and photosystem II in the photosynthetic pathway (Ashton and
Crafts, 1973). D1 protein of the P811 reaction centre is the
”herbicide binding protein" (Dodge , 1991). Hoffmann (1971)
proposed that the mechanism of action of uracils is very
similar to, if not identical with, that of the urea-type
herbicides. They have no effect on bacteria, fungi and non-

photosynthetic organisms except at concentrations one or two

32

times greater than those that affect photosynthesis. Foliar
chlorosis is the first symptom following application of the
uracil herbicides; root and shoot growth are also inhibited.
Ashton et al. (1977) studied the effect of uracils on growth,
anatomy, morphology and cytology of oat plants. Bromacil at
10'3 M was marginally inhibitory of root growth, with effect
been restricted to 0.5 mm segment immediately behind the
meristem. Chloroplast grana development was inhibited: normal
growth in the number of loculi per granum and normal increase
in width of grana was prevented. However, the length of the
grana.was increased. The authors concluded that these effects
appear to be associated with loss of integrity of membranes.
Loss of membrane integrity has been reported to occur within
2 to 4 hr following treatment with herbicidal Hill inhibitors
(Moreland, 1980). In contrast Sieber et al. (1973) reported
that Lenacil (uracil herbicide) had no effect on
ultrastructure of chloroplasts of sugar beet or Capsella Bursa
Pastoris. In Ehaseolus vul aris, Citrus sinensis L. and m
M, Herhodt (1968) reported a similar degree of
inhibition of the Hill reaction in isolated chloroplasts of
both species. Beans were more susceptible to terbacil, so he
concluded that the difference in susceptibility between the
two species was due to differential accumulation and
transport.

Schiver and Bingham (1973) found that following foliar

absorption, Bromacil moved acropetally in Kentucky bluegrass

33
and orchardgrass, and these patterns are typical of apoplastic
translocation. They suggested that Bromacil diffused
predominantly along cell walls, entered the xylem, and did not
readily enter the phloem. The same patterns of translocation
of terbacil following root absorption has been found in
peppermint. Adjuvants increase herbicidal activity by
increasing cuticle retention, penetration, absorption, and
possible translocation (Kirkwood, 1991) . The importance of the
leaf cuticle as a barrier to penetration of herbicides is well
documented. Among a range of factors, the physicochemical
characteristics of the epicuticular waxes may be of particular
significance since they can affect the retention and
distribution of the active ingredient. The incorporation of
surfactants may be required to achieve spreading or

activation.

Metabolism of uracil herbicides

A characteristic of many uracil herbicides is the
reversibility of their effects (Van Rensen, 1989) . Van Rensen
and Van Steekelenburg (1965) found that the inhibition of
oxygen evolution in algae by some urea-type herbicides could
be removed easily by washing. Izawa and Good ( 1965) showed
that diuron was reversibly bound to chloroplasts. This implies
that only weak bonds were involved in the interaction of this

herbicide and the receptor molecule in the thylakoid membrane.

34

Cyclization reactions appear to be important in the metabolism
of terbacil in alfalfa tissues, which are capable of
metabolizing terbacil through a cyclization pathway yielding
a heterocyclic oxazolo ring formed from the cyclization of the
carbonyl group (C=0) at the 2-position and of the tert-butyl
group [-C(CH93] at the 3-position of the molecule (Rhodes,
1979).

Herholdt (1968) reported extensive degradation of terbacil in
citrus and beans following root uptake, but he did not
characterize its metabolites. Terbacil was degraded more in
susceptible species such as beans than in tolerant ones such
as citrus. 0n the other hand, Barrentine and Warren (1970)
found that terbacil was metabolized at a higher rate in
'tolerant species (e.g., peppermint) than. in. susceptibles

(e.g., ngmggg sp.) with both leaf and root treatments.

Determination of herbicide inhibition by fluorescence

In recent years, chlorophyll a fluorescence has been
increasingly applied to various fields of plant physiology.
The technique of measuring chlorophyll fluorescence has been
used to determine photosynthetic activity, and to provide
detailed information about the photosynthetic system (Krause
and Weis, 1984). Measurement of chlorophyll fluorescence at
685 nm indicates the energy state of the P 680 reaction

centres of photosystem II (P811) and its associated pigments.

35

Fluorescence reflects the rate of electron transport from PSII
to chemical acceptors, and the coupling between ATP and
electron transport (krause and Weis, 1984).

In the leaf, the yield of fluorescence is influenced in
a very complex manner to events that are directly or
indirectly related to photosynthesis. A part of the light
absorbed by green plants is reemitted in the form of
chlorophyll fluorescence. When photosynthetic electron
transport is blocked, an increased proportion of the absorbed
excitation energy is reemitted as fluorescence. Pannels et al.
(1987) reported an inverse relationship between assimilation
and photosynthesis after the application of electron transport
herbicides. Miles and Daniels (1973) detected changes in leaf
fluorescence resulting from the inhibition of photosynthetic
electron transport by several inhibitors, including the
herbicides simazine. and. diuron. Schreiber' et. al. (1977)
quantitatively demonstrated the effects on the fast phase of
chlorophyll fluorescence following vacuum infiltration of
spinach leaves with diuron and following exposure of been
leaves to ozone. In the latter study, ozone-induced injury was
detected by fluorescence assay 20 hr before any visible signs
of leaf injury. Richard et al. (1983) used the technique of
Chl fluorescence measurement for detecting herbicide
inhibition in studies ‘using intact soybean leaves. They
concluded that this kind of technique can be used

quantitatively measure the effects of photosynthetic electron

36
transport inhibiting herbicides in intact plants, prior to
visual symptoms. Increases in terminal levels of fluorescence
(Fr) were detected in plants 0.5 and 1 hr, following the
foliar application of atrazine or diuron, respectively.
Panneels et al. (1987) observed that in barley and weed
species treated with DCMU and S-triazine there was a linear
relationship between the increase of the variable
fluorescence/maximal fluorescence (Fv/Fm. or jphotochemical
efficiency of PSII) and the log of herbicide concentration
used. Similar results were reported by Voss et al. (1984).
When analyzing the Chl fluorescence from leaves of different
species treated with photosynthetic inhibitors, they found
that the decrease in the ratio Fv/Fm provided a good
estimative of the changes in the photosynthetic capacity of

the leaves after the herbicide treatment.

The use of terbacil as a fruit thinning agent on fruit trees.

It has been demonstrated in a series of experiments, that
terbacil can induce fruit abscission in peaches and apples
through its action as a photosynthetic inhibitor. Byers et al.
(1985) observed that terbacil at 400 ppm applied to
Starkrimson 'Delicious' apple limbs at 6 and 16 days after
full bloom (DAFB) significantly reduced fruit set, but
applications 26 and 36 days AFB were ineffective. Similar

results were found by the same authors with terbacil

37

application on peaches. Terbacil, applied to peach cv. Biscoe
limbs at 400 ppm thinned fruits 35 and 40 DAFB. Byers et al.
(1990) reported similar results of terbacil applied to
Redchief 'Delicious' . Application at 50 ppm plus surfactant at
5, 10 or 15 DAFB reduced fruit set and increased fruit size,
but did not affect shoot growth. All these findings suggest
that different species, as well as different cultivars within
a species, vary in their responses to terbacil. Inhibition of
Pn caused by natural conditions may affect the response of
plants differently depending on the time at which the
inhibition occurs, and also depending upon the period when the
plant.or'parts of the plants, e.g., fruit, are more sensitive.
Responses to chemical inhibitors can be expected to rang in a
similar way.

In all the above studies, photosynthesis was reduced to
60 to 90% within the three days following the application.
Inhibition was maintained for several days, and recovered to
normal levels approximately 10 days after the treatment.
Higher doses of terbacil caused leaf yellowing, but the
symptoms disappeared a few days after treatment. Other
photosynthetic inhibitors tested have shown good performance
as thinning agents but they cause irreversible damage to the
foliage at the effective dose required to be active for

thinning.

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Publ., NY State Agr. Exp. Sta., Geneva, NY. pp. 13-17.

Van Rensen J .J .S. 1989. Herbicides interacting with
photosystem II. In: Herbicides and plant metabolism. Soc.
Exp. Biol. 38: 21-28. A.D. Dodge (eds.).

Voss M. , G. Renger and P. Graber. 1984. Fluorimetric detection
of reversible and irreversible defects of electron
transport induced by herbicides in intact leaves. In:
Advances in photosynthetic research. Vol 4:53-60. C.
Sybesma (ed.).

Warrington I.J., D.S. Tustin, C.J. Stanley, P.M. Hirst and
W.M. Cashmore. 1990. Light transmission characteristics
and changes in specific leaf weight within six
contrasting 'Granny Smith' apple canopies. In: 3rd
International meeting on "Regulation of photosynthesis in
fruit crops". Perugia. Italy. pp. 29-36.

Watson R.L. and J .A. Landsberg. 1979. The photosynthetic
characteristics of apple leaves (cv. 'Golden Delicious')
during their early growth. In: R. Marcelle, H. Clijsters
and. M. ‘Van Poucke (eds.). Photosynthesis and. plant
development. pp. 39-48.

Zelich I. 1971. Photosynthesis, photorespiration and plant
productivity Academic Press. New York.

INTRODUCTION

INTRODUCTION

The significance of photosynthesis to crop production is
widely accepted. Although increasing the rate of
photosynthesis could increase yield, there is no direct
evidence to support this relationship. Similarly, a reduction
in photosynthetic capacity does not always result in a yield
reduction. Previous studies have not clearly identified the
period during the growing season when a reduction in carbon
assimilation reduces the current season's and/or the next
year's fruit. production. Circumstantial evidence for 'the
contention that photosynthesis limits yield includes:
enhancement of growth and productivity by atmospheric CO2
enrichment (Baker, 1965: Collins, 1976: Wittwer, 1970:
Heinicke, 1963, 1966: Landsberg'et‘al., 1975: Monteith, 1976):
decreased crop yields following shading, through reduced fruit
set.and size (Boardman, 1977: Heinicke, 1963: Moreshet et al.,
1975: Hansen, 1977: Beers et al., 1987; Flore and Sam, 1986;
Sanchez et al., 1989: Jackson et al., 1991, McAvoy et al.,
1989: Doud and Ferree, 1980: Jackson and Palmer, 1977: Byers
et al., 1984, 1990a, 1990b): and.the effect of leaf injury and
early defoliation on fruit set, fruit size and fruit quality
(Ferree, 1978: Ferree et al., 1986; Campbell et al., 1990:
Hare et al., 1992: Nyrop et al., 1993: Jones, 1993). Likewise,
any factor that inhibits Pn may affect flower bud formation
for the next season (Autchter et al. , 1926: Paddock and

Charles, 1928: Jackson and Palmer, 1977: Monselise and

50

51
Goldschmidt, 1982: Gur, 1985).

The purpose of this study was to establish the
relationship between leaf Pn and yield in apple. Two main
objectives were proposed:

1. To determine if a reduction in Pn over a certain
threshold in trees carrying heavy vs. light crop loads could
cause a decrease in current and future crop yield and:

2. If a reduction.in.yield occurs, when.during the season
an inhibition of Pn may limit current or future crop
production.

Parallel and supportive experiments were conducted to
find the appropriated terbacil dose that caused a 50-60%
inhibition of Pn during a 15-20 day period and the time
required for recovery of the leaves' photosynthetic potential.
The relationship between Pn and Chlorophyll a fluorescence was

determined, on trees grown under greenhouse conditions.

MATERIALS AND METHODS

This research was conducted in 1993-1994. During this
period a main field experiment was conducted in conjunction

with supportive experiments.

Field experiments
The main field experiment was at the Clarksville

Horticultural Experiment Station, Clarksville, Michigan.

52
W. Ten-year-old apple trees (Mam domestic:
Borkh.) cv. Redchief 'Delicious' on MM106, planted in north-
south rows and spaced 3.0 x 6.0 m grown in a Bixby sandy loam
soil were used for the field study. The trees were pruned
prior to initiation of the experiment, and not summer pruned
again until the last evaluation was performed.

Trees were blocked into two categories: heavy and light
crop load. Crop load was considered heavy when a tree bore an
average of 3 to 4 fruits per cluster on 80-90% of its spurs.
The light crop load was 40 to 50% smaller than the heavy load,
i.e., an average of 2 fruits per cluster.

Hand thinning was performed on June 17, 1993 only on
trees carrying an excessive number of fruits and on the high
fruit load postharvest treatment. Trees were hand-thinned 5 to
6 weeks after full bloom. Pesticides, fertilizer, and
irrigation ‘were applied according to commercial
recommendations (Mich. Ext. Bul. E-154, Fruit Pesticide
Handbook) and were standard practices for apples grown in the

West Central part of Michigan.

Irggrmgnrsr Heavy and light crop load trees were sprayed at
selected times during the growing season with the
photosynthetic inhibitor terbacil [(5-chloro-3-(1,1-
dimethylethyl)-6-methyl-2,4(1H,3H)-pyrimidinedione)]. Terbacil
at 63 ppm plus X-77 at 1.25 ml 1'1 was applied to trees bearing

both high and low crop loads at the following times: 1) June

53
2 (15 DAFB), 2) June 17 (30 DAFB), 3) July 15 (60 DAFB), 4)
August 4 (so DAFB), 5) August 25 (100 DAFB), 6) October 8 (145
DAFB - post harvest). Trees were sprayed to the drip point
using a high pressure 150 L sprayer. Terbacil was applied as
an aqueous (dilute) high volume spray. In order to obtain full
coverage, trees received an average of 8 L of solution/tree at
the beginning of the season (first treatment), increasing to
14 L/tree by the third application. All the treatments were
compared with both a non thinned and a hand thinned control.
The post harvest treatment (145 DAFB) was hand thinned on June
17, 1993 (30 DAFB). Full bloom occurred on May 17, 1994. The
experimental design was a randomized complete block. Each
treatment was applied to whole, single-tree plots with four

replications (blocks).

ns.

Inhibition of photosynthesis was corroborated after each
treatment by measuring leaf chlorophyll fluorescence the day
following application and again one week later. A Morgan CF-
1000 chlorophyll fluorescence measurement system (P.K. Morgan
Instruments, Inc., Andover, MA) was used. Leaves were dark
acclimated for 15 min using acclimation cuvettes, then
irradiated with 1000 umol m'2 s'1 PPFD actinic light.
Chlorophyll kinetics were then recorded over a 60 s period.
Data are reported as the ratio of Fv (variable

fluorescence) /Fm (maximum fluorescence) , which can be directly

54

related to quantum efficiency.

Reproductive and vegetative growth. Trunk circumference and
trunk cross-sectional area (TCSA) 15 cm above the graft union
were determined for all the trees with a vernier caliper.
Change in TCSA were determined for the period of study.

At the time of each terbacil treatment, 10 current season
shoots on both the east and west sides of each tree were
selected and tagged. Shoot growth was measured at 7-10 day
intervals. Final shoot growth was determined on July 28, 1993,
after terminal all buds had set. In the year following
treatment (June 27, 1994) trees were summer pruned and the
fresh weight of one-year-old watersprouts (or suckers) were

determined. The average value/cm2

TCSA was compared among
treatments.

Flower density [(number of flower clusters/cross-
sectional area of the.branch (BCSA)] was evaluated in 1994 for
all trees to determine the effect of the previous year's
terbacil treatments on return bloom.

Fruit growth was determined by selecting 20 fruit per
tree and measuring fruit diameter at 7-10 day intervals from
15 DAFB until fruit maturity. Diameters were measured at the
equatorial zone of each fruit in an east-west orientation,
with a precision caliper.

Fruit set was determined as the number of fruit per cm2

area (BCSA) at the base of two branches on opposite sides of

55
the tree in both 1993 and 1994. In 1993, fruit drop was
calculated.by counting the number of fruit.that abscised. This
number was also related to the number of fruit at harvest to
calculate the percentages of fruit set and fruit.drop for each
treatment.

Trees were harvested at fruit maturity on October 7,
1993. Fruit from counted, weighed and graded and average fruit
weight was calculated. Six size categories according to the
commercial standards for fruit diameter as follows: Cat I >
8.9 cm: Cat II < 8.9 cm to > 8.3 cm: Cat III < 8.3 cm to > 7.6
cm: Cat IV < 7.6 cm > 7.0 cm: Cat V < 7.0 cm to > 6.4 cm: Cat
VI < 6.4 cm. Fruit less than 6.4 cm were consider as "cull"
fruits. Crop density (CD = number of fruits/TCSA) was
calculated for each treatment.

A.random.sample of ten fruits in the 3rd size category (<
8.3 cm to > 7.6 cm) from each tree were visually rated for
percentage and degree of red color. The intensity of red
pigmentation was rated on a scale of 1 to 4, where 1 = light
and 4 = dark red. Percent soluble solids was determined for
each fruit using a portable refractometer. Flesh firmness was
measured on three sides of each fruit with a hand presiometer.
Fruit density was estimated by measuring the volume of a
sample of ten fruits per tree. Each sample was weighed and
then placed into a plastic net with a weight attached to
prevent the apples from floating. The water displacement was

measured as a measure of sample volume. Density was determined

56

according to the formula: density = weight/volume.

Cold hardiness.

Deep winter hardiness was evaluated for current season
shoots from all the trees that were sampled every month from
harvest time until budbreak the next year (from Oct. 15, 1993
to Mar. 01, 1994) . Samples were evaluated according to methods
of Bittenbender and Howell (1974) . Three shoots from the
medium position of each tree were randomly selected from all
treatments and replications. Shoots were cut into two inch
sections and then subjected to a controlled temperature
reduction (3° C/hr) in a freezing chamber. Samples were
exposed to temperatures ranging from -13 to -53 0C and then
visually evaluated for cambium browning 7 days after keeping
the samples at room temperature. Tso values, or the temperature
(”C) required to kill half of the samples, were determined for

each treatment.

Terbacil concentration experiment.

In 1993, two separate supportive experiments, one in the
field and other in the greenhouse, were performed. The first
experiment was conducted at the Horticultural Teaching and
Research Center at Michigan State University, East Lansing,

MI.

57

Five shoots from five 12-years-old Red 'Delicious' on
Malling-Merton 106 (MM106) trees in south-north oriented rows
at approximate spacing of 7.0 m x 2.80 m were selected at
random, blocked, tagged. and. sprayed. with. different
concentrations of terbacil plus surfactant (X-77 at 1.25 ml L‘
1). Each shoot was considered as a replication. A hand pump
sprayer was used for the applications. Shoots were sprayed
with. Sinbar (terbacil) plus surfactant. at the following
concentrations: 1) 0 ppm (control), 2) 12.5 ppm, 3) 25.0 ppm,
4) 50 ppm, 5) 100 ppm, 6) 200 ppm, 7) 400 ppm, and 8) 800 ppm.
Control shoots were sprayed with water'plus surfactant at 1.25
ml L”. A randomized complete block experimental design with
five replications was used. Shoots were sprayed to the point
of drip on May 19, 1993.

Chlorophyll fluorescence was measured at regular
intervals following treatment as described previously. The
photosynthetic inhibition caused by terbacil was determined
over a 22-day period. Visual symptoms of leaf injury for the

different herbicide concentrations were recorded.

Greenhouse experiment

The greenhouse experiment was performed in the Plant and
Soil Science Greenhouses at Michigan State University, East
Lansing.
Dormant one-year-old apple trees, [(Mgiug domesriga Borkh.]

cv. 'Golden Delicious' on M9 rootstock were planted in 8 L

58

plastic pots with a soil mix (7 field soil : 1 sand : 1
organic matter). All trees were cut 10 cm above the graft
union and placed in an environmentally controlled greenhouse
(day and night means 18 and 13°C, respectively). Peter's
soluble 20N-20P-20K fertilizer (500 ug/L) was applied every
three weeks and trees were watered every two days. Pesticides
were applied as necessary.

Following six weeks of active growth when shoots had 15-
20 expanded leaves, 15 trees were selected for each treatment
and one leaf in the median position of each tree was tagged
and dipped in a solution of terbacil containing X-77
surfactant at 1.25 m.L4. Concentrations were 1) 0 ppm (water
plus surfactant control): 2) 50 ppm: and 3) 100 ppm. At daily
intervals for a 12 day period gas exchange and chl
fluorescence were measured for each of the treated leaves.
Chlorophyll fluorescence was evaluated as described
previously. Photosynthesis (A) was determined using an ADC
LCA-2 portable photosynthesis system (Analytical Development
Company, Hoddesdon, UK) under the following conditions: flow
rate = 0.4 L/min, leaf temperature range 27 to 30°C, inlet
relative humidity 23%, ambient co2 330-340 p1 L" and PAR >
1000 umol m’2 s". Leaf photosynthesis was calculated as
previously described (Moon and Flore, 1986).

A randomized complete block experimental design with 15
replications (trees) was used. Correlations between gas

exchange and chlorophyll fluorescence measurements were

59

calculated.

A third field experiment was conducted in 1994 at the
Horticultural Teaching and Research Center at Michigan State
University, East Lansing, to determine the possible effect of
terbacil on leaf chlorophyll content. Five shoots of Redchief
'Delicious' trees on MM106 spaced approximately 4.50 m x 3.0
m, were selected, tagged and sprayed to the point of drip with
terbacil at 63 ppm plus X-77 at 1.25 ml L’1 using a hand pump
sprayer. Every day for a period of 15 days A and chlorophyll
fluorescence (both measured as described above) were evaluated
and compared with control leaves which had received water plus
X-77 alone at the same dose as treated. The measurements were
conducted on leaves near the middle of the shoot. One leaf per
shoot was collected at each time of Pn and chlorophyll
fluorescence measurement. Chlorophyll content was determined
according to the method of Moran (1982). Two discs (0.328 cm
diameter) were punched from the lamina of each leaf using a
paper holepunch, and were pooled as one sample. Chl was
extracted in 7 m1 N,N-dimethylformamide in darkness at 5°C for
36 hours. Absorbance of extracts was read at 664, 647, and 625
nm on a Hitachi U-3110 UV/Vis spectrophotometer (Hitachi Ltd. ,
Tokyo). Calculations for chl a, chl b and P chl were made

according to Moran (1982).

t ' ti alcu ations.

60
All data were subjected to analysis of variance (ANOVA).
When necessary, data were transformed by x + 0.5 for the
statistical analysis. The relationship between Pn (Y) and

Fv/Fm (X) was analyzed by simple regression analysis.

RESULTS

agree; 9: rgrbacil on thg rate of phorgsyrrhggig,

Concentration response curve. Quantum efficiency as determined
by chlorophyll fluorescence was inhibited by terbacil, the
degree and length of inhibition being directly related to the
concentration applied (Figure 1). The reduction in quantum
efficiency (Fv/Fm) that resulted from dosages of 50 ppm and
higher was approximately 60% for all treatments during the 5
days following application. The effect of terbacil at 12.5 ppm
was not significantly different from the control 10 days after
its application or thereafter. Doses of 100 ppm and higher
reduced photosynthesis significantly for 15 days, whereas
twenty-two days after treatment only 400 and 800 ppm caused a
significant reduction in Fv/Fm. Phytotoxicity symptoms in
leaves appeared 10 days after treatment.with 50 ppm.or higher,
but disappeared in the 50 ppm treatment 20 to 25 days after
application. Necrosis was noticed in those leaves that
received 100 ppm or higher. In these, symptoms were
irreversible and persisted until fall.

When terbacil at 63 ppm plus surfactant was sprayed on
apple shoots under field conditions A and Fv/Fm was inhibited
for 12 days (figure 2).

Three days after treatment leaves showed a reduction of 68%

and 63% in Pn and Fv/Fm, respectively.

61

62

Figure 1. Effect of terbacil concentration on Fv/Fm (% of
control) 1 to 22 days after treatment, Red
'Delicious', HTRC.

Mean separation within dates by DMRT P<0.05.

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Figure 2. Effect of terbacil (63 ppm) on Fv/Fm and A of

Redchief 'Delicious' at HTRC.

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Leaves gradually recovered fellowing terbacil application.
Thirteen days after treatment the reductions were 3.7 % and
34.3 % for A and Fv/Fm, respectively. Eighteen days after
treatment, the leaves regained their photosynthetic capacity.

When Pn and FV/Fm were measured in 'Golden Delicious'
apple leaves (PSG) both parameters were significant correlated
(r = 0.689) on an exponential scale (Y= 3.21 x (10.24)‘)

(Figure 3).

Main experiment

The reduction in Fv/Fm by terbacil (63 ppm) on the main
field experiment at Clarksville was approximately 50% 1 day
after its application on the first date of application, and
30-40% 1 week later. However, the percentage reduction was
lower when treatment was applied 100 or 145 DAFB (Table 1).
Phytotoxicity symptoms were:observed.only in leaves treated 30
DAFB (field experiment). Intervenal leaf‘yellowingwappeared.in
young leaves 8 to 10 days after treatment, and symptoms

disappeared 10 to 15 days later.

Chlorophyll content. Terbacil reduced chl a and total
leaf chl content, but altered neither P chl (Table 2) or the
chl a to b ratio (data not shown). Chl a and total leaf chl

returned to control levels within 13 days.

67

Figure 3. Relationship between Pn (Y) and Fv/Fm (X) during the
12 days following application of terbacil at
concentrations of 50 and 100 ppm to 'Golden

Delicious' at PSG.

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Table 2. The effect of Terbacil treatment (63 ppm) on Redchief ‘Delicious’leaf chl a, b, P
chl, and total chl content over time at HTRC.

 

Time following treatment (days)

 

(Days) 1 3 5 7 9 13
Chl a content (pg cm'z)

Untreated 52.3a 53.8a 54.13 52.3a 52.7a 53.4a

(control)

Treated 48.3b 49.8b 49.0b 48.3b 48.8b 58.8a
Chl b content (pg cm'z)

Untreated 12.2a 13.2a 12.8a 13.9a 13.7a 13.6a

(control)

Treated 12.7a 14.0a 12.1a 14.0a 14.03 13.9a
P chl content (pg cm'z)

Untreated 12.2a 13.9a 12.8a 9.8a 9.1a 8.0a

(control) -

Treated 12.7a 14.8a 12.1a 10.03 8.0a 8.1a

Total chl content (pg cm'z)

Untreated 76.7a 80.9a 79.7a 76.0a 75.5a 75.03

(control)

Treated 73.7b 78.6b 73.2b 72.3b 71 .8b 74.8a

 

Means are average of 5 replicates. Mean separation within columns and parameters by Student's t-test,

P<0.05.

71

Irrir_§gr. Fruit abscission was induced by terbacil (63
ppm) applied 15 and 30 DAFB to heavily cropping trees, as
indicated by the number of fruits dropped/cmz of trunk cross
sectional area (TCSA), the percentagezof fruit dropped (Figure
4, Figure 5), and by the number of fruits/cmgibranch cross
sectional area (BCSA) retained (Figure 6). Fruit diameter 15
and 30 DAFB was 9.8 i 1.1 mm and 24.5 i 1.4 mm, respectively.
Fruit trees sprayed 15 DAFB abscised earlier than did control
fruits; June drop began on June 23 in the latter, on June 15
in the former. Terbacil treatment 60 DAFB (fruit diameter 45
i 0.78 mm) had increased fruit drop on trees with a heavy
fruit load as of July 28, one week after treatment (data not
shown). However, response‘was much less than that observed for
earlier applications. Although terbacil application for the
first and second treatments resulted in a reduction. of
fruits/cm2 BCSA, response in trees having a low crop load was
much less than in those with a high crop load, and fruit
retention was the only parameter to be significantly affected
by treatment (Figure 7, Figure 8). Just prior to harvest (129
DAFB - Sep. 23), the number of fruits/cm2 BCSA was
significantly lower for low crop than for high crop treated
15, 30 and 60 DAFB, and as well as for low crop trees treated
with terbacil was applied 15 and 30 DAFB (Figure 9). Treatment
after 30 (low crop) or 60 days (high crop trees) did not
reduce cropload. Hand thinning 30 DAFB reduced final cropload

in both sets of trees.

72

Figure 4. Effects of timing of terbacil application and
cropload on fruit drop of Redchief 'Delicious' at

CHES, as Of 28 July 1993 (72 DAFB).

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Figure 5. Total fruit dropped as percentage of total number of
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Figure 6. Effect of terbacil (63 ppm) treatment and timing on
fruit set (number of fruit/cm?- BCSA), 'Redchief

Delicious', CHES.

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Figure 7. Effect of terbacil on fruit retained.
Number of fruit/cm2 BCSA through the season (1993)

for high crop load Redchief 'Delicious' at CHES.

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Figure 8. Effect of terbacil (63 ppm) on fruit retained.
Number of fruit/cmgiBCSA through the season (1993)

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Figure 9. Effect of crop load and terbacil (63 ppm) applied 15
to 100 days after full bloom (DAFB) on fruit
retention on September 23, 1993, Redchief

'Delicious' at CHES.

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84

Fruit growth-size. Regardless of the crop load, the final
fruit size of the king fruit was not affected by terbacil
treatments (Figures 10, 11) . Fruit growth followed a sigmoidal
curve characteristic of pome fruits. However, terbacil
inhibited normal fruit growth for the following week only when
applied 15 DAFB (June 1) in low crop load trees or 30 DAFB
(June 17) in the heavy crop load trees (Figure 11, Table 3).
From June 17 to June 23, the percent increase in size of
fruits treated 30 DAFB on trees carrying a heavy crop was
9.73%, whereas in control plants it was 20.5%. During this
period, fruits from plants treated 15 DAFB increased in
diameter 48.3%. Inhibition of growth was observed only when
terbacil was applied 15 DAFB on the low crop trees (Figures
12, 13, Table 3). However, that inhibition was of a lower
magnitude than the observed 30 DAFB in fruits of heavy loaded
trees.

Although final fruit size of the tagged king fruits was
not significantly affected by terbacil treatments (figure 13) ,
higher percentage of large fruits (Cat I) were harvested from
trees of high load crop treated with terbacil 15 DAFB.
Likewise, a greater proportion of small fruits (Cat VI) was
observed when terbacil was applied 30 and 60 DAFB (Figure 14,
Table 4). Terbacil applied 100 DAFB did not increase the
percentage of small fruit produced (Cat VI), and increased the
number of medium sized fruit (Cat IV) (Figure 14, Table 4). No

significant trend for large sized fruit distribution was found

85

on the trees with a low crop load (Figure 15, Table 5),
although all terbacil treatments reduced the percentage of
fruits in the largest size category. This also can be observed
when analyzing the average fruit weight at harvest and the
percentage of fruits larger than 8.3 cm in diameter (Cat I +
Cat II). Regardless of the crop load, those trees who received
terbacil 60, 80 and 100 DAFB had the lower percentage of
larger fruits (Table 6).

i d. Terbacil applied 15 and 30 DAFB
significantly reduced yield. Crop density (number of
fruits/cm2 of TCSA) and harvested yield efficiency (kg of
fruit produced/cm? TCSA) were greatly decreased by the first
two treatments, especially when crop load was high (Figures
16, 17, Tables 7, 8). Later applications of terbacil became
progressively less effective in reducing fruit number and
total weight, and the applications at 100 DAFB and after were
completely ineffective (Figures 16, 17). Although reductions
were significant regardless of crop load the effect was more
pronounced when crop load was high (Tables 7, 8).

g;gi§_gggli§y; Neither fruit soluble solids nor fruit
firmness was affected by any terbacil treatment regardless of
the crop load (Figures 18, 19). No differences were found in
fruit specific«gravity (Figure 20) or in fruit color (data not
shown). Percent of red surface color and color intensity were
similar' for all treatments. Red surface color intensity

averaged 3.5 (4.0 = dark red) (data not shown) for all the

86
treatments.

W... Terbacil treatment did not affect
total shoot terminal length significantly (Figure 21). Shoot
growth was slightly greater for the low crop trees (26.23 cm
i 1.027), including control plants, than for the heavy crop
trees (23.94 cm i 1.08). No differences in the final shoot
length/cm2 of TCSA was found among treatments (data not
shown). Terbacil applied 30 DAFB almost completely inhibited
shoot growth on the heavy crop loaded trees for one week
(Figure 23, Table 9), and was similar to the inhibition
observed in fruit growth. During the week following treatment
shoot growth rate averaged 0.08 mm/day vs. 1.80 mm/day in
control plants. Both heavy and low crop loaded treatments
showed an earlier cessation of shoot growth (July 15) when
terbacil was applied 15 and 30 DAFB. Following later treatment
shoots continued growing for almost two more weeks until July
28 (Figure 22, Figure 23). The final number of leaves per
shoot was not significantly affected by treatment. Trees
carrying heavy crop load had an average of 21.6 i 0.9 unfolded
leaves, while light crop loaded plants had 21.7 i 0.6. In all
treatments spur shoots stopped growing on July 6, when they
had an average of 6.83 i 0.808 mature leaves. Whereas total
shoot growth.was similar for all the treatments, total weight

2 TCSA) was significantly higher than

of watersprouts (kg/cm
the control for all heavy crop trees in which thinning was

significant (terbacil at 15, 30 DAFB; hand thinned 30 DAFB).

87

Figure 10. Cumulative fruit diameter (mm) for Redchief
'Delicious' king fruit in low crop trees treated
with terbacil (63) ppm at different times during the

season .

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89

Figure 11. Cumulative fruit diameter (mm) for Redchief
'Delicious' king fruit on high crop trees treated
with terbacil at 63 ppm at different times during

the season.

90

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91

Figure 12..Absolute fruit.growth.(percentage of fruit.diameter
increment between dates) of Redchief 'Delicious'
king fruit on low crop trees treated with terbacil

(63 ppm) at different times during the season.

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93

Figure 13..Absolute fruit.growth.(percentage of fruit.diameter
increment between dates) of Redchief 'Delicious'
king fruit on high crop trees treated with terbacil

(63 ppm) at different times during the season.

94

 

 

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Figure 14. The effect of terbacil (63 ppm) applied to
Redchief 'Delicious' at different times during the
growing season on percentage of fruit in six

categories on trees with a high initial crop load.

96

 

 

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97

Figure 15. The effect of terbacil (63 ppm) applied. to
Redchief 'Delicious' at different times during the
growing season on percentage of fruit in six

categories on trees with a low initial crop load.

98

 

 

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103

Figure 16. The effect of terbacil (63 ppm) application at
different times of the season on the number of fruit
(fruit/c1112 TCSA) at harvest for Redchief

'Delicious' at CHES.

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105

Figure 17. The effect of terbacil (63 ppm) application at
different times during the season on final yield

(Kg/cm2 TCSA) of Redchief 'Delicious' at CHES.

106

 

 

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Figure 18. The effect of crop load and terbacil (63 ppm)
application at different times during the season on
fruit soluble solid content at harvest for 'Redchief

Delicious' at CHES.

111

 

 

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Figure 19. The effect of terbacil (63 ppm) application at
different times during the season on fruit firmness
at.harvest.for high.and low loaded trees onRedchief

'Delicious' at CHES.

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Figure 20. The effect of terbacil (63 ppm) application at
different times during the season on fruit density
at harvest for high and low loaded.trees of Redchief

'Delicious' at CHES.

115

 

 

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116

Figure 21. The effect of terbacil (63 ppm) application at
different times during the season on final shoot
length on high and low crop loaded trees of

Redchief 'Delicious' at CHES.

117

 

 

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Figure 22. The effect of terbacil (63 ppm) application at
different times of the season on shoot growth of
Redchief 'Delicious', CHES, on trees with a low

crop load.

119

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Figure 23. The effect of terbacil (63 ppm) application at
different times during the season on shoot growth of
Redchief 'Delicious' , CHES, on trees with a high

crop load.

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122
Likewise, the degree of watersprout formation decreased
progressively as treatment was delayed (Figure 24) . No greater
tendency was observed for watersprout production in the low
cropped trees. However, in those trees that received terbacil
earlier in the season (15 and 30 DAFB) and in the hand-thinned

control the production of watersprouts was higher.

gold hardiness. No differences were observed in the T“,
among treatments between November 1993 and April 1994 (Table
10).

zgturg bloom-firgit set, Terbacil applied at 30, 60, 80
and 100 DAFB significantly inhibited return bloom the
following season (1994) as indicated by the number of flower
clusters/cmzlof BCSA whereas the 15 DAFB treatment promoted
flowering (Figure 25). In the light-cropping trees only 2
treatments significantly affected flowering. Terbacil
applications at 30 and 145 DAFB (hand thinned 30 DAFB)
promoted flowering (Figure 25). Final fruit set, measured on
July 20, 1994 was higher in trees treated with terbacil 15
DAFB and in those hand thinned and treated with terbacil 145
DAFB. In contrast terbacil treatments 30 and.60 DAFB inhibited
flowering (Figure 26). In low crop trees, the only treatment
that affected fruit set in 1994 was application of terbacil 3O

DAFB in 1993. This reduced set significantly.

123

Figure 24. The effect of terbacil (63 ppm) application at
different times during the season on water sprout

production of Redchief 'Delicious' at CHES.

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125

Figure 25. The effect of terbacil (63 ppm) application at
different times during the season on return to bloom
(cluster flowers/ cmz BCSA) the following year
(1994) on low and heavy crop load trees of

Redchief 'Delicious' at CHES.

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127

Figure 26. The effect of terbacil (63 ppm) application at
different times during the season on final fruit set
(number of fruit/cm2 BCSA) the following year (1994)
on low and high crop load trees of Redchief

'Delicious' at CHES.

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DISCUSSION

Several experiments have shown the effectiveness of
terbacil as a photosynthetic inhibitor on fruit crops.
Photosynthesis in a variety of different fruit trees was
inhibited for varying lengths of time by concentrations from
50 to 2000 ppm (Byers et al., 1984, 1895; DelValle et al.,
1985). However, the degree of plant responses in terms of 1)
magnitude of inhibition, 2) foliar damage and 3) time of
recovery varied. Environmental factors, as well as stage of
development of the different organs of the plant, play a very
important role in the response obtained. The same dose applied
to the same species, and sometimes to the same varieties, may
have different effects (Byers et. a1, 1984, 1990a, 1990b).

The environment prior to application can have a profound
effect on cuticle development, in particular epicuticular wax
deposition, chemistry and fine structure, which influence the
retention and penetration of foliar applied sprays (Baker,
1974). In the main field experiment, the late treatments (100
and 145 DAFB) caused less Fv/Fm reduction (Table 1) than did
earlier applications. The cuticle of older leaves is less
permeable and thicker, and herbicide absorption is decreased
(Kirkwood, 1983; Unrath, 1981; Bukovac et al., 1979). In
addition, wax deposition and cuticle thickness increase with
leaf age. Therefore it is not surprising that the degree of

inhibition in this study was not constant; the second

130

131

treatment had the greater effect in reducing Fv/Fm. This
treatment was the only one in which phytotoxicity was
observed. The environmental conditions at the time of
treatment may have been responsible for this response. The day
terbacil was applied (June 15) the relative humidity and
temperature were high (Appendix, Figure 1), and it was cloudy.
An important factor that influences the effect of dose is the
'duration of exposure' (Streibig, 1992). The time of exposure
of this treatment was longer than for the others: furthermore
the herbicide did not dry rapidly, which could cause greater
uptake. Slower drying time usually results in greater
activity attributed to both extended wetting time and
increased chemical activity on the leaf surface (Unrath,
1981).

Symptoms of herbicide injury disappeared approximately 20
days after application. Many of the uracils produce symptoms
that dissipate after a short period of time (Van Rensen,
1989). Some of them are either weakly bound to the receptor
molecule in the thylakoid membrane (Izawa and Good, 1965), or
metabolized by the plants (Herholdt, 1968).

As expected inhibition of photosynthesis was extended as
concentration increased (dose response curve, Figure 1) .
Leaves treated with 12.5, 25 and 50 ppm recovered their
photosynthetic capacity 15 days after the herbicide
application. The data also reveal different degrees of

inhibition according to the concentration applied. This

132
differential response could be observed after 5 days of
treatment. At that time, the leaves that received the lower
concentrations began to recover their photosynthetic capacity,
while those that received 100 ppm or higher amounts had a
value 40% of that of the control.

An analysis of leaf tissue from the second experiment in
which terbacil was applied at 63 ppm indicated that the
herbicide degraded chl a (Table 2), whereas chlorophyll a
content remained similar to that of the control leaves 13 days
after treatment. This was coincident with the increase in Pn
observed (Figure 2). Photosynthetic inhibition was almost nil
18 days after terbacil application. However, after'l3 days the
Pn of treated leaves was only 3.7% less than the control,
while Fv/Fm was 34.3% lower than untreated leaves. Similar
effects of terbacil (78 ppm) were found by Hubbard, et
al.(1994, unpublished data) on photosynthesis in tart cherry.
This difference observed may have resulted from the high
sensitivity of the fluorimetric detection in revealing the
photochemical efficiency of PSII (Gleiter and Renger, 1993).
This method also detects the level of metabolism-
detoxification of the herbicide by the photosystem.
Measurement of chlorophyll a fluorescence has been reported to
be an accurate method for evaluating PSII (Krause and Weiss,
1984; Pannels et al., 1987; Miles and Daniels, 1973; Schreiber
et a1, 1977; Richard et al., 1983; Gleiter and Renger, 1993:

Voss et al., 1984). Fv/Fm has provided excellent results for

133
the investigations of inhibitors that act at the acceptor site
of photosystem II in sugar beet, soya, dwarf bean and cotton
(Voss et al., 1984). On the basis of my data, I can infer that
chlorophyll a fluorescence is an accurate method for the
measurement of'photosynthetic status of the leaf. Pn.and.Fv/Fm
were significantly correlated (Figure 3). Interestingly, full
PSII integrity does not seem to be necessary for maximum or
near maximum Pn, implying that excess electron transport is
occurring. This might be a useful tool as an early detection

method for inhibition of Pn by biotic or abiotic stress.

The importance of Pn on fruit set is well documented.
Studies in which light levels were reduced within the canopies
- with the consequent reduction.in.Pniduring'bloom.and shortly
after - indicate the importance of photosynthate supply for
fruit retention ( Doud and Ferree, 1980; Jackson and Palmer,
1977; Auchter et al., 1926; Byers et al., 1990a, 1984, 1990b,
Flore and. Sams, 1986). Similar effects, have been found
following 1) early defoliation of spur leaves (Ferree and
Palmer, 1982; Arthley and Wilkinson, 1964; Lewelyn, 1966;
Lakso, 1984), and 2) application of photosynthetic inhibitors
(Byers et al. 1984, 1985, 1990a, 1990b, Del Valle et al.
1985). Moreover, a possible mechanism for apple fruit
abscission during June drop is the competition for essential
metabolites among individual fruitlets and between fruitlets

and vegetative shoots (Abbott, 1960; Quinlan and Preston,

134
1971; Wardlaw, 1968). Early’ development. of‘ apple flower
clusters after budbreak also utilizes stored reserves of
carbohydrates and nutrients (Hansen, 1971; Hansen and
Grauslund, 1973).

Our results showed a high dependence of fruitlets and
growing fruits on substrate produced by the leaves. High fruit
drop was induced by terbacil application. Although all
references known support inhibition of fruit development by
photosynthetic inhibition soon after bloom, some discrepancies
exist as to the effect of later treatments. Variable results
have been reported in reference to fruit diameter and
abscission. Byers et al. (1990a) , and Byers et al. (1986)
demonstrated thinning of fruits of 8 to 33 mm in diameter when
plants were shaded 10 to 30 DAFB, or terbacil was applied soon
after full bloom. We found that tree with heavy crop loads
were thinned by low concentration of terbacil until 60 DAFB,
when diameter was approximately 45 mm (Figures 7, 8 and 9).
Greatest effect on fruit abscission were caused by the first
and second treatment (15 and 30 DAFB).

In our study an interaction of crop load was observed. In
trees carrying low numbers of fruits, fruit abscission was
lower than in high crop trees. However, when comparing the
time of abscission of fruit between heavy and light crop
trees, we observed that fruit abscission continued at a low
rate until September 23 (time of the last evaluation)(Figures

7, 8).

135

In plants treated 15 DAFB, fruit drop followed the same
pattern as in the controls (see slope of graph in Figure 8).
This is evident if we compare the number of fruits/cmz BCSA on
August 7 and September 23. Fruits from trees treated 15 DAFB
continued abscising at a higher rate than those from trees
treated 30 DAFB. On September 23 the number of fruits/ cm?
BCSA of light crop trees treated 15 DAFB was almost 40% higher
than that of heavy loaded plants treated at the same time
(Figure 9) . More extreme was the difference observed with the
second treatment. Fruit number/cm2 of BCSA of low loaded trees
treated 30 DAFB was approximately double than in heavy loaded
ones (Figure 9) . Obviously fruits were more dependent on
photosynthates during the early stage (until 30 DAFB); but
when availability was decreased in two different situations,
high and low demand, the trees' response was different in
regulating the number of fruits it was capable of supporting.
The effect was more marked in plants carrying high numbers of
fruits, where demand exceeded supply. In other words, when
photosynthesis was inhibited, carbohydrate supply was not
enough to maintain a heavy demand. In addition, fruit and
shoot growth rate was markedly reduced on heavy cropping trees
treated 30 DAFB (Table 3, Table 9) . During the early phase
fruit growth depends on the carbohydrates transported from
spur leaves near them. Shoot leaves do not exhibit net
carbohydrate export to the tree until 3-4 weeks AFB (Lakso,

1934).

136

Terbacil applied 15 DAFB inhibited fruit growth the week
following treatment only in low crop trees (Table 3, Figures
10 and 11), whereas the same treatment 30 DAFB inhibited fruit
growth only in high crop trees (Table 3, Figures 11 and 13).
Unsprayed fruits on heavy cropping trees grew in diameter an
average of 1.0 mm/day, while fruits treated 30 DAFB» grew'only
0.40 mm/day. This can be observed in the slopes of the fruit
growth curves (Figures 11, 13).

The different response caused by the treatments 15 and 30
DAFB on fruits in heavy loaded trees was unexpected. A
possible explanation is that fruits have the greatest demand
(sinks) for current photosynthate in mid-June (Hansen, 1977),
when we inhibited photosynthesis was inhibited by terbacil.
Grochowska (1973) and Priestley ( 1969) reported a dramatic
fall in starch levels in fruit-bearing apple spurs in the 5th
- 6th week AFB (end of June - beginning of July).

Natural fruit drop did not begin in control plants until
June 23 (36 DAFB) . At that time, an adequate carbohydrate
supply was required not only for fruit and vegetative growth,
but also for flower induction-initiation (Westwood, 1978;
Buban and Faust, 1982; Faust, 1989). Additional energy was
required by the leaves to repair the damage caused to the
photosynthetic apparatus. This metabolic activity may have
affected the rate of carbohydrate consumption.

The different response observed in low loaded trees,

where terbacil applied 15 DAFB was the only treatment that

137
inhibited fruit growth (Table 3), may reflect an effect of the
previous tree history. At the early stages of fruit
development, when growth was dependent on both current and
stored carbohydrate, a shortage in the latter accomplished to
an inhibition in Pn, could have resulted in a decrease in

fruit growth rate.

When terbacil was applied 30 DAFB, the effect on shoot
elongation was greater than on fruit growth. In heavy loaded
trees shoot growth increment during the week following
terbacil treatment was 0.45 %, while in untreated trees was
8.13 %. That corresponded to growth rates of 1.80 mm/day and
0.08 mm/day for treated and control plants, respectively
(Table 9). Although reproductive and vegetative growth were
influenced by the Pn inhibition, fruits were evidently a
stronger sink for carbohydrates than shoots (Avery, 1969;
Hansen, 1971; Faust, 1989). According’to Daie (1985), absolute
growth rate of apple fruits reflects the daily rate of
carbohydrate accumulation, and can be considered as
representative of the 'sink strength'.

Fruit growth in apple is divided into two main periods:
cell division and cell enlargement. Both processes are
involved in determining the rate of growth and final potential
for fruit size. The cell division occurs during the first 4‘to
6 weeks following fertilization (Hulme, 1971).

The effect of Pn on fruit size is well known. Direct evidence

138

comes from the results of several shading experiments
(Jackson, 1968; Jackson and Palmer, 1977; Marini et al.,
1991). The dependence of fruit size on light penetration into
the trees was assessed by Heinicke (1966) who found a direct
correlation between fruit size and degree of light exposure.

Most of the studies indicate directly or indirectly that
competition for carbohydrates among sinks affects fruit size
mainly during the cell division period (Westwood 1968, Faust,
1989, Lakso et al. 1989). Early fruit thinning results in
larger fruit size supporting this hypothesis (Preston and
Quinlan, 1968; Quinlan. and. Preston, 1968; Abbott, 1965;
Cobianchi, 1973; Knight and Spencer, 1987). Although total
cell number is considered to be the primary factor determining
fruit size at harvest, but this relationship is not always
evident. Clearly supply of photosynthates is necessary during
cell enlargement for maximum fruit size, as the bulk of dry
weight accumulation occurs during the post cell division
period, after June drop (Archbold, 1992) . My data suggest that
carbohydrates are important in the achievement of large fruit
size in both early and late stages of fruit.development. Heavy
cropping trees treated with terbacil 15 DAFB had a higher
proportion of fruits in Cat I (> 8.9 cm) (Fig. 14, Table 4).
Although fruit cell count was not recorded the higher
percentage of large fruits probably reflects a higher cell
division following fruit thinning. Similar results were not

observed in the hand-thinned control, probably because the

139
fruit were thinned too late to affect size. Similar results
were obtained by Cook (1985) on Red 'Delicious' . Nevertheless,
my results also suggest that fruit size is reduced when
photosynthesis or carbohydrate supply is decreased, as
indicated by the following: 1) All low loaded trees to which
terbacil was applied had a low percentage of fruits in the
largest category (Fig. 15, Table 5).
2) Low crop loaded plants that were substantially thinned by
terbacil at 15 DAFB ‘would be expected to bear’ a high
percentage of Cat I (> 8.9 cm) fruits. However, these trees
had significantly lower number of these fruits than the
control. Likewise, the percentage of larger fruits observed (>
8.3 cm) was similar to the control (Table 6). The inhibition
of fruit growth observed may account for this result.
3) Independently of crop load a higher number of 'cull' fruits
were found when terbacil was applied from 30 to 100 DAFB. The
higher number observed in the heavy cropping controls may
indicate high fruit competition for carbohydrate supply.

My data supports previous observations (Byers et al
1990a, 1990b; Knight, 1981) that terbacil applied early
promoted fruit thinning but did not increased fruit diameter
in some experiments. Moreover, Byers et al. (1986) reported
that shading apples 20-30 DAFB did not cause fruit thinning,
but reduced fruit size. Rom and Ferree (1986) demonstrated
that shoot leaves supply the photosynthate needed for late

fruit enlargement. They found that shading apple shoots from

140

60 DAFB until maturity reduced fruit growth and resulted in
small size at harvest. Severe red mite infestation in July
also reduces apple fruit size (Beers et al., 1987).

Terbacil applied 15 and 30 DAFB significantly reduced the
number of fruits and total weight produced.per TCSA.at.harvest
on both heavy and light crop trees (Figures 16 and 17, Table
7 and 8). Since terbacil treatments had no effect on fruit
size on the low crop trees, and only a slight influence on the
heavy cropped trees, it appears that fruit number was more
responsible for the difference in total production than was
size. Similar results were reported by Knight (1981) and Byers
et al. (1990a, 1990b). This can also be observed. when
comparing the production of heavy cropping trees treated with
the herbicide 30 DAFB vs. 60 and 80 DAFB (Table 7). Although
these three treatments increased the percentage of fruits in
the small categories (Cat V and VI) (Table 4), the 60 and 80
DAFB treatments did not differ significantly from the control
in fruit number and total production per TCSA. These

treatments did not thin.

Fruit quality was not greatly affected by terbacil
treatment. Generally, fruit color has not been influenced
directly by terbacil application (Byers et al., 1984; 1990b).
Several studies indicate that color is affected by
environmental factors, being light exposure one of the most

important. Erez and Flore (1986) reported that color

141
development in peach fruits was a function of exposure to
solar radiation. Direct light to the fruit is needed in apples
for anthocyanin synthesis and, therefore, red color
development (Marini, 1985; Jackson et al., 1977; Barritt et
al., 1987; Jackson, 1968; Heinicke, 1966; Seeley et al.,1980;
Morgan et al., 1984; Izso and Rom, 1989; Campbell and Marini,
1992, Saks et al., 1990). Experiments in which fruits were
exposed to different light levels support this observation
(Proctor and Creasy, 1971; Greene and Lord, 1975). My data did
not show an extreme effect of inhibition of photosynthesis at
different times on color formation. Tselas et al. (1979)
reported a complete independence from photosynthesis in the
development of anthocyanin. in :maize roots. According’ to
Westwood (1978), a high level of carbohydrates in the fruit
during the preharvest period tends to increase the content of
anthocyanins. Walter (1967) pointed out that chromogen
(anthocyanin precursor) synthesis depends on a supply of
carbohydrates from green leaves. However, Redchief is a highly
colored variety (Brooks and Olmo, 1972). Most, if not all,
Redchief 'Delicious' strains do not present coloration
problems. In general, they start coloring earlier than many
other 'Delicious' strains and develop strong red color in

different environments (Mercier, 1976).

Fruit SSC (soluble solids concentration) are strongly

influenced by light exposure of leaves in the immediate area

142

of the fruit (Jackson et al., 1977; et al., 1983), implying
the importance of ;photosynthesis, and. therefore. of
carbohydrate supply, on this parameter. Numerous experiments
in which shade was applied from 45-60 DAFB until maturity
revealed a positive correlation between light (PPFD) and SSC
in fruits (Marini, 1985; Jackson et al., 1977; Jackson, 1968;
Seeley et al., 1980; Morgan et al., 1984; Campbell and.Marini,
1992; et al., 1983). However, Barritt et al. (1987) did not
find such a correlation. Marini et al. (1991) reported that
the SSC of peach fruits was only related to PPFD during the
first half of stage III of fruit growth. I observed no
difference among treatments in their effects on sugar
concentration. This may imply that a short period of Pn
inhibition is not sufficient to influence SSC. However, one
would have expected sugar concentration to be negatively
correlated with crop load.

Similarly, neither fruit firmness nor density was
affected by treatment. If the increase in size observed in
fruits from plants treated with terbacil 15 DAFB resulted from
a higher number of cells, a difference in both parameters
should have been observed. The fact that the comparisons among
treatments were among fruits of the same size (CAT III) may
have concealed such differences. A composite sample including
fruits from all size categories would have been more
appropriate. Early fruit thinning usually leads to an increase

in vegetative growth (Murneek, 1924). Photosynthetic

143

inhibition at different times of the season did no affect
final shoot length, regardless of crop load (Figures 21, 22
and 23). As was expected, shoot growth was greater in low crop
than in heavy crop trees. However, one would have expected a
greater mean shoot length in those trees in which terbacil
increased fruit drop. However, shoot growth ceased earlier in
both low and heavy loaded trees with terbacil 15 and 30 DAFB
(Figures 22 and 23). Quinlan and Preston (1968) found that
thinning did not affect shoot length in 'Sunset' apple, but
increased the number of shoots per tree. Although we did not
count the number of shoots produced, early terbacil treatment
increased watersprout production (more evident in heavy loaded
trees) (Fig. 24). Watersprouts were apparently stronger sinks
for carbohydrate allocation than were shoots. The latter, as
mentioned above, stopped growing 2 weeks earlier than shoots
on control and other treated trees.

Jackson (1968) mentions that upright-growing shoots
(watersprouts) can compete successfully with other sinks,
including fruits. Tymoszuk et al. (1986) found that
carbohydrates produced from watersprouts were not translocated
to apple fruitlets situated on neighboring spurs, but were
used by the apices of the watersprouts and eventually
incorporated into the bark.and wood of the main limbs near the
place of their production. No clear explanation emerged from
the analysis of watersprouts in those trees which carried low

crop.

144

The importance of carbohydrate storage in woody tissues
and its effects on winter hardiness has been extensively
investigated. Acclimation is an active metabolic process that
requires a product of photosynthesis (Chandler, 1954) . Several
reports have indicated that some correlation exists between
the levels of soluble sugars and starch in fruit trees and
their winter hardiness. Positive correlations have been
observed in apple (Williams and Raese, 1974), peach (Malcolm,
1975), and citrus (Mizuno et al., 1968). Fuchigami et al.
(1971) observed that dogwood plants did not acclimate when
depleted of reserves.

Early leaf loss has been reported as a detrimental factor
in tart cherry, causing delayed acclimation and more rapid
deacclimation, resulting in reduced bud survival (Howell and
Stackhouse, 1973) . Similarly, foliage should be in good
condition in late fall to produce the maximum photosynthate
possible. Any practice that extends growth into fall decreases
the hardiness of tissues. My experiment did not show any
difference in cold hardiness in any of the treatments (Figure
10). The T50 was similar for all of them.

Inhibition of photosynthesis early in the season
following terbacil treatments (15 and 30 DAFB) could not have
reduced hardiness due to the early thinning of fruits which
reduced the total carbohydrate for fruit and increased cold
resistance (Edgerton, 1966) . This was accomplished by an

earlier cessation of shoot growth. Lack of effect of the

145
treatments on. cold. hardiness *may indicate that: 1) the
inhibition of Pn.capacity for 14-20 day periods did not reduce
carbohydrate storage; 2) the acclimation was preordained by
the genetic constitution of the tree and the normal
environment the tree responds (Proebsting, 1978) or; 3) sugars
and starch do not influence cold hardiness response, as was
observed in some peach cultivars (Lasheen and Chaplin, 1977).
Although we did not analyze stored carbohydrates in our

experiment the first hypothesis appears to be more feasible.

The contribution of leaves, and hence of Pn, to flower
bud initiation has been established in.most plants (Monselise
and Goldschmidt, 1982). According to some researchers, the
flower induction-initiation process is governed by hormonal
balance (Buban and.Faust, 1982); others believe that it is the
result of changes in the distribution of nutrients inside the
apical meristem.(Kraus.and.Kraybill's.C/N’theory, 1918; Sach's
nutrient. diversion, theory, 1977). Bernier’ et. al. (1981)
considered a high C/N ratio to be essential for flowering. The
inhibiting effect of fruiting on flower-bud formation has been
associated with the presence of seeds (Chan and Cain, 1967),
which are a source of hormones (Luckwill and Silva, 1969;
Sinska et al., 1973) that may be transported to the spurs and
inhibit flower bud formation. Early fruit thinning increases
return bloom the following year (Faust, 1989; Ryugo, 1986).

However, several observers have pointed out the importance of

146
leaves and high photosynthetic levels in this process. The
negative effect of early defoliation or shading, has
demonstrated that a certain photosynthetic threshold is
necessary at the time of flower formation (Ryugo, 1986;
Auchter et al., 1926; Paddock and Charles, 1928; Jackson and
Palmer, 1977; Gur, 1985; Lakso, 1980).

A reduction.in Pn 30 DAFB, at the beginning of the flower
initiation period (Westwood, 1978), strongly reduced return
bloom the following year in heavy cropping trees (Figure 25).
Conversely, inhibition of Pn 15 DAFB, with reduced fruit set,
promoted flower formation in heavy-cropping trees. However,
flowering was lower in trees that received terbacil 30 DAFB
than in those hand-thinned at the same time. This agrees with
the results of Worley (1979) and Davis and Sparks (1974) in
pecans. They reported that a shortage in carbohydrate at the
time of flower initiation inhibited flower formation in this
species. On the other hand, Goldschmidt and Golomb (1982)
suggested that flower initiation was not energy intensive and
high levels of carbohydrates at this time were not highly
demanded in citrus. Grochowska (1973) found that a high.demand
in starch supply occurs in the 5th or 6th week after full bloom
in apple, and that time was coincident with our second
terbacil treatment. Although little information is available
about the sink-strength of flower initials, my data suggest
that during' this period fruits are stronger sinks ‘than

potential flower buds; and a decrease in carbohydrate supply

147
decreases flower bud initiation.

Sink strength, defined as sink activity times sink size
(Flore and Lakso, 1989), could have a marked effect on plants
carrying large numbers of fruits. Comparison of return bloom
and final fruit set the following year (Figure 26), indicates
that although terbacil inhibited flowering less when applied
60, rather than 30 DAFB these flowers were less capable of
setting fruits. In general, well formed buds are required to
obtain. good fruit set (Faust, 1989). The fact that no
difference was observed in winter hardiness among treatments
suggests that carbohydrate shortage reduced flower initiation
rather than cold hardiness.

The hypothesis that time of leaf abscission or reduced
competition for carbohydrates late in the season (Nyeki, 1980)
can reduce flower 'quality' and fruit set the following season

is not supported by my data.

Terbacil appears to be an useful tool to inhibit
photosynthesis and to investigate damage thresholds in fruit
crops. Among the advantages of its use we could mention:

1. Once the decrease in Pn caused by any insect or
disease is known, terbacil can be applied at any time during
the season to simulate their effects, avoiding the
difficulties of insect or disease infestation, leaf removal,
etc.

2. The degree and duration of inhibition can be regulated

148
by choosing the dosage to be applied.
3. Terbacil usage is easy to apply and is also an
inexpensive tool requiring no sophisticated equipment for its

application.

SUMMARY AND CONCLUSIONS

Although photosynthesis is recognized as the source of
energy and carbon for plant growth, in most cases there
appears to be no direct association between maximum leaf
photosynthesis and yield.

This study was an attempt to determine if a reduction in
Pn over a certain threshold, in trees carrying heavy vs. low

crops, can reduce current and/or future crop yield in apple.

The following general conclusions concerning the role of
Pn in plant growth-production were drawn:

1. A decrease in photosynthetic efficiency (47-69%)
during the first stages of plant growth (15 and 30 DAFB)
provoked a marked reduction in total yield regardless of
initial fruit load.

2. The reduction in yield resulted from a decrease in
fruit number that was not compensated for larger fruit size.
Although the treatment 15 DAFB treatment in heavy loaded trees
resulted in an increase in fruit size, the great decrease in
fruit set reduced total production.

3. Fruit and shoot growth may be compromised when Pn is
reduced 60 % , for a 20 days period, from mid—June to mid-July
in trees carrying a heavy crop. At this time of high demand,
stored carbohydrates are insufficient for both reproductive

and vegetative growth; these are therefore dependent on

149

150
current photosynthate.

4. An inhibition of Pn during the first phase of the cell
enlargement period may lead to the production of a high number
of 'cull' fruits.

5. No effect of Pn reduction on fruit quality (red.color,
SSC and firmness) was found.

6. A decrease in Pn for 20 days during mid June - mid
July (30-60 DAFB) strongly reduced flower induction-

initiation, and therefore fruit production the following year.

7. Reductions of'Pn.for 20 day periods at different.times
in the season did not alter wood carbohydrate storage; hence,
the trees' winter hardiness was not affected.

8. Fruits are stronger sinks for carbohydrates than are
new shoots, or buds.

9. The supportive experiments showed that photosynthetic
efficiency (Fv/Fm) is a good indicator of the leaves'
photosynthetic capacity. Fv/Fm and Pn were significantly

correlated.

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Appendix

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Figure 1. Temperature (°C) and precipitation (mm) at CHES

during the growing season 1993.

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