Annals of Botany 95: 583–591, 2005
doi:10.1093/aob/mci058, available online at www.aob.oupjournals.org
Perfect Syncarpy in Apple (Malus · domestica ‘Summerland McIntosh’)
and its Implications for Pollination, Seed Distribution and
Fruit Production (Rosaceae: Maloideae)
C O R Y S . S H E F F I E L D 1, 2,*, R O B E R T F . S M I T H 1 and P E T E R G . K E V A N 2
1
Atlantic Food and Horticulture Research Centre, Agriculture and Agri-Food Canada, 32 Main Street,
Kentville, Nova Scotia, Canada B4N 1J5 and 2Department of Environmental Biology,
University of Guelph, Guelph, Ontario, Canada N1G 2W1
Received: 26 July 2004 Returned for revision: 22 September 2004 Accepted: 29 October 2004 Published electronically: 20 January 2005
Background and Aims The gynoecium of the domestic apple, Malus · domestica, has been assumed to be
imperfectly syncarpic, whereby pollination of each stigmatic surface can result in fertilization within only one of
the five carpels. Despite its implied effect on fruit quantity and quality, the resulting influence of flower form on seed
set and distribution within the apple fruit has seldom been investigated. Instead, poor fruit quality is usually
attributed to problems with pollination, such as low bee numbers and/or ineffective pollinators within apple
agro-ecosystems. The objective of this study was to determine the true nature of gynoecial structure and its influence
on fruit production in the apple cultivar ‘Summerland McIntosh’.
Methods A stigma-excision method was used to determine the effects of uneven pollination among the five stigmas
on fruit quantity (as measured by fruit set), and quality (seed number and distribution). In addition, flowers were
examined microscopically to determine pollen tube pathways.
Key Results Fruit set, seed number, seed distribution, and the microscopic examination of flower gynoecial
structure reported in this study indicated that the gynoecium of the cultivar Summerland McIntosh is perfectly
syncarpic and not imperfectly syncarpic as previously thought.
Conclusions Pollination levels among the five stigmas need not be uniform to obtain full seed development within
Summerland McIntosh fruit; even if one stigmatic surface is adequately pollinated, a full complement of seeds is
likely. The importance of perfect syncarpy in recognizing true causes of poor fruit quality in apple is discussed.
Cory S. Sheffield, Robert F. Smith and Peter G. Kevan For the Department of Agriculture and Agri-Food,
Government of Canada ª Ministry of Public Works and Government Services Canada 2005
Key words: Malus · domestica, apple, pollination, flower structure, pollen-tube pathway, perfect syncarpy, seed distribution,
fruit quality.
INTRODUCTION
Apples have been part of the human diet for thousands of
years and cultivation practices have existed since at least
1000 BC (Morgan and Richards, 2002). Intense management
of apple, Malus · domestica Borkh. (Rosaceae: Maloideae),
as a horticultural crop is more recent, with many advancements for production occurring even in the last half century
(see treatments in Westwood, 1978; Childers, 1983; Morgan
and Richards, 2002). The reproductive requirements of the
domestic apple, therefore, have been a topic of horticultural
investigation for a long time and thorough understanding
has been gained (Brittain, 1933; McGregor, 1976; Westwood,
1978; Pratt, 1988; Sedgley and Griffin, 1989; Free, 1993;
Delaplane and Mayer, 2000). However, despite these investigations, there is still an incomplete understanding of apple
flower form and function with respect to the actual pollen
tube pathway and its influence on the formation and distribution of seeds within the fruit.
The female organ of a typical flower, the gynoecium, consists of one or more structural units commonly called carpels,
each having a stigma, a style, and an ovary containing the
ovules (Weberling, 1989; Endress, 1994; Raven et al., 1999).
* For correspondence. E-mail [email protected]
Endress (1982, 1994) reports that >80 % of taxa have
syncarpous gynoecia in which the carpels are congenitally
fused; the remaining taxa are split evenly between the apocarpous forms (with separate carpels) and those with a single
carpel (Endress, 1994). The syncarpous group contains taxa
with a range of degrees of inter-carpel communication, but
most forms have a compitum—a zone of inter-carpel communication where pollen tubes have the potential to cross over
and distribute evenly among carpels (Endress, 1982, 1994),
a condition which Endress (1990) termed ‘perfect syncarpy’.
However, ‘syncarpy’ is also used to describe taxa in which
the pollen tube transmitting tissues of each carpel remain
separate throughout their entire length despite the carpels
being congenitally fused externally. In a sense, these taxa
have gynoecia that are effectively apocarpous (Carr and
Carr, 1961; Williams et al., 1993). To distinguish this form
of syncarpy, Carr and Carr (1961) used the term ‘pseudo
syncarpy’, although P. K. Endress (Institute of Systematic
Botany, University of Zurich, Switzerland; pers. comm.) suggests ‘imperfect syncarpy’ to describe taxa with congenitally
united carpels with no compitum.
Apple flowers are typical for the rose subfamily
Maloideae, which have been described as syncarpous
(which, in a broader sense, includes imperfect syncarpy)
Cory S. Sheffield, Robert F. Smith and Peter G. Kevan For the Department of Agriculture and Agri-Food,
Government of Canada ª Ministry of Public Works and Government Services Canada 2005
584
Sheffield et al. — Perfect Syncarpy in Apple
(Pratt, 1988; Roher et al., 1994). However, within the
Maloideae, considerable variation in the extent of connation
among carpels has been reported, including apocarpous
forms (Roher et al., 1991, 1994), and forms apparently
without a compitum (Gorchov and Estabrook, 1987;
Grochov, 1988). In Malus, each of the five styles bears a
single stigma and is basally fused with the other styles for a
portion of its length. The styles are the solid type with a core
of transmitting tissue through which the pollen tubes grow
inter-cellularly (Cresti et al., 1980; Sedgley, 1990). The
gynoecium of apple is believed to be imperfectly syncarpous (Carr and Carr, 1961; Cresti et al., 1980; Anvari and
Stösser, 1981; Pratt, 1988; Weberling, 1989) and, like most
maloids (Cambell et al., 1991; Rohrer et al., 1994), each
carpel contains two ovules which have the potential to form
two seeds or ten seeds per fruit, although there are differences among cultivars (McGregor, 1976; Westwood, 1978;
Faust, 1989; Free, 1993). Therefore, to produce an apple
with a full complement of seeds, it has been assumed that at
least two viable pollen grains must be transferred from a
compatible cultivar to each of the five receptive stigmatic
surfaces (Torchio, 1985).
Because of imperfect syncarpy in apple, differences in
the levels of pollination among the five stigmas should have
a direct effect on fruit quality and quantity due to variable
production and distribution of seeds (Carr and Carr, 1961).
The number and distribution of seeds within a developing
apple affects its shape and weight (Brittain, 1933; Brittain
and Eidt, 1933; Free, 1993; Brault and de Oliveira, 1995;
Keulemans et al., 1996). Furthermore, flowers and developing fruit that are not pollinated or that are poorly fertilized
usually drop soon after bloom (Free, 1993). Most dropped
apples collected during June and July have fewer developing seeds than those that stay on the tree (Brittain and Eidt,
1933; Brain and Landsberg, 1981). However, Lee (1988)
suggests caution in interpreting the relationship between
seed number and fruit drop due to intra-plant variation
in spur quality, stating that the same tree may have both
many-seeded fruit which drop and few-seeded ones which
remain. In addition, Ward et al. (2001) also found that the
date of drop was not related to the number of seeds of
dropped fruit in some cultivars.
Several factors may result in pollination differences
between the stigmas. Normally the subdivided styles of
apple flowers are the same length which places the stigmatic
surfaces on the same plane for visitation by pollinators
(Fig. 1). The stigmatic surfaces and styles are often tightly
arranged into a column, which increases the likelihood of
bees successfully pollinating all five surfaces during a single
visit. Occasionally the stigmas may be spread apart or the
sexual column may be damaged or deformed, which could
result in asymmetric fertilization and seed distribution, leading to early fruit drop or misshapen, inferior fruit.
The findings of Beaumont (1927) and Visser and
Verhaegh (1987) suggest that the flowers of some cultivars
of apple may have a compitum. Unfortunately their findings
have been largely overlooked and most pomologists assume
that apple flowers have an imperfectly syncarpous gynoecium. Ward et al. (2001), for example, investigated the
relationships of seed number and fruit weight to day of
F I G . 1. A solitary bee, Andrena sp. (Hymenoptera: Andrenidae) visiting a
Summerland McIntosh apple (Malus · domestica) blossom. Note the central
stigmas covered with pollen.
drop in the cultivars ‘Smoothee Golden Delicious’, ‘Redchief
Delicious’ and ‘Commander York’. In that study, a
stigma-excision technique similar to that of Beaumont
(1927) and Visser and Verhaegh (1987) was used to prescribe seed number in the resulting fruit—it was assumed
that at most two seeds would result for every stigma left
intact and pollinated. Although seeds per fruit and seed
distribution for each stigma treatment was not presented
in that study (Ward et al., 2001), R. P. Marini (Virginia
Polytechnic Institute and State University, VA; pers. comm)
indicated that in some fruit more seeds were present than
expected.
The objective of the present study was to determine
the true nature of gynoecial structure in the apple cultivar
‘Summerland McIntosh’, specifically by comparing the
effects of uneven pollination among the five stigmas on fruit
quantity (as measured by fruit set), and quality (seed number
and distribution). In addition, flowers were examined microscopically to determine the location and structure of the
pollen transmitting tissue.
MATERIALS AND METHODS
Collection of pollen for hand pollination and
determination of pollen viability
In both years of study (2002 and 2003), branches with several flower clusters from different apple Malus · domestica
Borkh. (Rosaceae, Maloideae) cultivars, maintained as
breeding stock at the Atlantic Food and Horticulture Research Centre, Kentville, Nova Scotia (45 050 N, 64 280 W),
were collected and placed into a greenhouse compartment
with the temperature maintained continuously above 18 C
and ambient light conditions. Branch ends were snipped
diagonally and quickly placed into 4-L jars of water. At
the balloon stage of flowering, petals were peeled away and
the swollen anthers were removed from the filaments by
rubbing the open flower on wire mesh, following the procedures of Galletta (1983). Anthers were collected in a glass
Petri dish and allowed to dehisce for 24–48 h. Dehisced
585
Sheffield et al. — Perfect Syncarpy in Apple
anthers were placed into a glass vial and crushed to release
more pollen. The vial was sealed, placed in a jar with
anhydrous calcium sulfate (DrieriteTM) and kept in a cool,
dry place until used (within 1–5 d).
In 2003, viability of a pollen sub-sample was determined
using the MTT [3-(4,5 dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide; Sigma M 2128] (Rodriguez-Riano
and Dafni, 2000) and DAB (Sigma FastTM 3,30 diaminobenzidine tablets; Sigma D-4168) techniques outlined by Dafni (2001). A control of non-viable pollen was
prepared for viability analysis simultaneous to the treatment; pollen was killed by spreading a small amount of
the pollen mixture into a 70 % ethanol droplet on a glass
microscope slide, which was then heated with a flame. This
procedure was repeated twice. Control and treatment pollen
samples were placed on glass microscope slides and the
reagents MTT or DAB were applied following Dafni
(2001). The droplets were mixed and spread out to minimize
pollen clumping and to facilitate drying, and the slides were
placed on a slide warmer to dry. This procedure was
repeated twice. Randomly selected fields of view
were examined with a compound microscope at ·100
magnification. The total of viable and non-viable pollen
grains was counted in each field of view for a total count
of at least 300 pollen grains. Non-viable pollen grains,
which stay light coloured, were distinguished from viable
ones, which turn a dark colour (violet-purple-brown in
MTT; brown-purple-red in DAB), indicating the presence
of dehydrogenases or peroxidases, respectively (Dafni,
2001). Percentage viability was calculated for both reagents.
Stigma receptivity period for hand pollination studies
Stigma receptivity of ‘Summerland McIntosh’ flowers
at different stages of development was investigated in
2002 using a method which rated oxygen bubble generation
on stigmatic surfaces. Receptive stigmatic surfaces produce
peroxidase enzymes (Zeisler, 1938; Galen and Kevan, 1980;
Dafni, 1992) which break down hydrogen peroxide, generating oxygen bubbles (Galen and Plowright, 1987; Dafni,
1992). Flowers at various stages of development were collected in plastic bags and immediately placed into a cooler
containing ice packs. A ‘blind’ design was used to evaluate
the level of oxygen generation where the evaluator had no
knowledge of stage of flowering. It was assumed that the
rate of bubble production from the stigmatic surface in
hydrogen peroxide was directly related to its level of receptivity. A grading scale of 1–5 was developed to rank receptivity (1 = no bubble production; 5 = very rapid bubble
production). The flowers were randomly selected for evaluation. The styles were then removed from each flower just
above the point of emergence from the hypanthium and
passed to the evaluator who placed the stigmatic ends
into a depression slide containing fresh 3 % hydrogen peroxide (after Galen and Kevan, 1980). The evaluator graded
and recorded the level of bubble production for each flower.
Stigma excision and pollination experiments
A 3-ha orchard at the Agriculture and Agri-Food Canada
research farm in Canard, Kings Co., Nova Scotia (45 070 N,
64 280 W) was used for the experiments. The orchard
consisted of alternating north-to-south double rows of
18-year-old ‘Summerland McIntosh’ (semi-dwarf ‘MM 106’
root stock, pruned to modified central leader) and 8-year-old
‘Royal Court Cortland’ (semi-dwarf ‘MM 106’ root stock)
apple trees, with 6-m spacing between rows, and 45-m tree
spacing within rows.
A randomized complete block (CB) design was used. The
blocks were three (2002) and five (2003) randomly selected
‘Summerland McIntosh’ trees. On each tree, six limbs were
selected based on flowering potential. Six levels of pollination treatment (i.e. none, one, two, three, four or five stigmas
remain) were randomly assigned to each of the six limbs
on each tree. Previously opened, damaged, unhealthy and
under-developed flowers were removed. All remaining
flowers at, or slightly beyond, the balloon stage had their
styles snipped and cauterized (using forceps heated with a
mini-torch) approx. 3–5 mm below the stigmatic surface to
leave the desired stigma number. The remaining stigmas
were then hand pollinated using the eraser end of a pencil
coated with the previously collected pollen mixture. This
procedure was repeated on two consecutive days to ensure
pollination of open flowers. The total number of flowers
receiving the pollination treatments remaining on each
branch was recorded. Branches were then covered with
approx. 45 · 50 cm Delnet1 apertured film bags (DelStar
Technologies, Inc., Middletown, DE) for 3–4 weeks to
minimize insect feeding damage.
Percentage fruit set was determined for each of the branches on all trees by counting the developing fruit remaining
4 weeks after petal fall. Percentage fruit set data were subject to arcsine transformation (Zar, 1999) for normalization and to achieve homoscedascicity of variance prior
to balanced analysis of variance (ANOVA) (Minitab, 2000).
At harvest in mid-September, all fruits were collected and
placed in cold storage at approx. 4 C until fruit quality was
determined. Fruits were cut in half just above the equatorial
axis, and the number of plump seeds per carpel and their
distribution within the fruit was determined. The number of
seeds per fruit was analysed with ANOVA (generalized
linear model procedures) (Minitab, 2000). The number of
seeds produced per pollination treatment was also compared
with those expected using chi-square analysis for contingency tables. Expected values were determined by first
multiplying the maximum number of seeds expected per
fruit for each of the k pollination treatments (i.e. two
seeds per remaining stigma) by the number of fruit
which developed for each treatment (i), to obtain the
value Si. These values were then subject to the following
transformation:
!
X
k
Si T
Si
i¼1
where T is the total seeds produced in all the fruit for all
treatments. This procedure was done to balance the observed
and expected totals in the contingency table for analysis
while maintaining the relative proportions of expected
seeds for each treatment. All tests were conducted at the
5 % level of probability.
Sheffield et al. — Perfect Syncarpy in Apple
586
5
1·00
Grd 1
Grd 2
Grd 3
Grd 4
Grd 5
Mean
4
0·60
3
0·40
2
0·20
1
Mean grade (± s.e.)
Proportion of grade
0·80
0
0·00
Tight bud
Loose bud
Balloon Fresh open
Stage of flowering
Old open
Petal fall
F I G . 2. Proportion of stigma receptivity grades in Summerland McIntosh apple (Malus · domestica) flowers at various developmental stages and their
respective mean grade (6 s.e.).
Gynoecium structure and the pollen-tube pathway
RESULTS
Pollen viability and stigma receptivity
The viability of the pollen mixture used in 2003 was determined to be high using both the DAB (922 % 6 40 s.d.)
and MTT (940 % 6 75 s.d.) techniques. It was assumed
that the pollen mixture used in 2002 had similarly high
viability. Freshly opened flowers had the largest proportion
of high stigma receptivity as measured by oxygen generating activity, and had the highest mean receptivity grade
(Fig. 2). Peroxidase activity was measured in all stages of
flower development.
Fruit set
Significant differences were observed among the pollination treatments for percentage fruit set in 2002 (F = 2243,
d.f. = 5, P < 0001), but no differences were observed among
the trees (F = 023, d.f. = 2, P = 0801). Treatment data
from the trees were pooled and means were separated with
Tukey’s HSD test (P = 005) (Zar, 1999). The zero-stigma
100
Percent fruit set (± s.e.)
Twenty flowers were collected and fixed in 3 : 1 ethanol :
acetic acid for 20–24 h (Kearns and Inouye, 1993). Flowers
were then rinsed in 50 % ethanol for 05 h, and then stored in
70 % ethanol at 4 C. Flowers were dissected longitudinally
to determine floral form, specifically the length of various
sections of the gynoecium, and transversally to determine
the location and structure of the pollen transmitting tissue
within the styles. Measurements were made using a binocular microscope with an ocular micrometer.
2002
2003
80
BC
C
BC
b
b
60
B b
BC
b
b
40
20
A a
0
0
1
2
3
4
Number of stigmas pollinated
5
F I G . 3. Mean percentage fruit set (6 s.e.) for Summerland McIntosh apple
(Malus · domestica) for each pollination treatment in 2002 and 2003. Bars
sharing letters within a year are not significantly different (Tukey’s HSD
test, P = 005); analysis based on arcsine-transformed data.
pollination treatment had almost no fruit set and differed
from the remaining treatments, and the one-stigma pollination treatment differed significantly from only the twostigma pollination treatment (Fig. 3). In 2003, the same trend
was observed with significant differences observed among
the pollination treatments (F = 1215, d.f. = 5, P < 0001) but
not the trees (F = 150, d.f. = 4, P = 0241). Similar to 2002,
the 0-stigma pollination treatment set no fruit, and differed
from all other treatments (Fig. 3). No differences were
detected among the remaining treatments (Tukey’s HSD
test, P = 005).
587
Sheffield et al. — Perfect Syncarpy in Apple
8
500
2002
2003
Expected seeds AB b
b
B
AB
b
A
6
a
4
Total seeds
Expected seeds
2002
400
B b
Number of seeds
Mean number of seeds (± s.e.)
10
300
200
100
2
0
200
0
1
2
3
4
Number of stigmas pollinated
2003
5
F I G . 4. Mean number of seeds per fruit (6 s.e.) and expected seeds per fruit
for Summerland McIntosh apple (Malus · domestica) for each pollination
treatment in 2002 and 2003. Bars sharing letters within a year are not
significantly different (Tukey’s HSD test, P = 005).
Number of seeds
0
0
Seed production and distribution
In 2002, significant differences in mean seeds per fruit
were found among the pollination treatments (F = 286,
d.f. = 4, P = 0026), but not the trees (F = 171, d.f. = 2,
P = 0185). The data from the trees were subsequently
pooled and analysed with Tukey’s HSD test (P = 005).
Significant differences were observed between the onestigma and three-stigma pollination treatments, and
between the one-stigma and five-stigma pollination treatments, but not among the other treatments (Fig. 4). In
2003, the same trend was observed with significant differences found among the pollination treatments (F = 515,
d.f. = 4, P = 0001), but not among the trees (F = 038,
d.f. = 3, P = 077). The 1-stigma pollination treatment
differed from all other treatments (Tukey’s HSD test,
P = 005) (Fig. 4).
In both years, the mean number of seeds per apple
exceeded those expected from an imperfectly syncarpous
arrangement in the one-, two- and three-stigma pollination
treatments, but was less than expected for the five-stigma
treatment (Fig. 4). Similarly, the total seeds produced was
also significantly higher than expected for imperfect syncarpy for the one-, two- and three-stigma pollination treatments, but less for the five-stigma pollination treatment
(2002: c2 = 2023, d.f. = 4; 2003: c2 = 1215, d.f. = 4; data
pooled across trees in each year) (Fig. 5). The percentage of
fruits with seed-bearing carpels from the different pollination
treatments also did not correspond to those expected from an
imperfectly syncarpous arrangement, as the majority of fruit
from all treatments had five carpels bearing seeds (Table 1).
No mature fruits had more than two seedless carpels.
Gynoecium structure
The external fused portion of the styles, as measured
from the hypanthium to the area of stylar separation, of
Summerland McIntosh flowers is approx. 3 mm in length
100
1
2
3
4
Number of stigmas pollinated
5
F I G . 5. Total seeds and expected seeds in Summerland McIntosh apple
(Malus · domestica) for each pollination treatment in 2002 (data pooled
for three trees) and 2003 (data pooled for five trees). Significant differences
were found between the number of seeds observed and expected (2002:
c2 = 2023, d.f. = 4; 2003: c2 = 1215, d.f. = 4).
T A B L E 1. The distribution of seed-bearing carpels for each
pollination treatment in 2002 and 2003
Year
2002
2003
% Fruit with 0, 1, 2, 3, 4 or
5 seed-bearing carpels
No. of
stigmas
pollinated
No. of
fruit
0
1
2
3
4
5
0
1
2
3
4
5
0
1
2
3
4
5
0
17
29
36
30
38
0
17
18
12
18
13
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
35.3
10.3
–
3.4
–
–
41.2
5.6
–
–
–
–
23.5
17.2
13.9
13.3
26.3
–
23.5
–
16.7
11.1
23.1
–
41.2
72.5
86.1
83.3
73.7
–
35.3
94.4
83.3
88.9
76.9
Values indicate percentages of fruit with seed bearing carpels from each
treatment; highest percentage values within a row are in italic; bold in
two diagonal rows indicates the distribution of seeds in carpels expected
under imperfect syncarpy.
(Fig. 6). Internal microscopic examination indicated that
the compitum is much smaller, and is confined between
the upper part of the ovaries and the lower part of the
connate styles (Fig. 6).
Sheffield et al. — Perfect Syncarpy in Apple
588
A
Pollen tube
transmitting
tissue
Compitum
3 mm
Vascular
tissue
Ovule
F I G . 6. The gynoecium of Summerland McIntosh apple (Malus · domestica) displaying perfect syncarpy. ‘A’ indicates the most basal transverse section
examined by Cresti et al. (1980).
DISCUSSION
The gynoecia of most taxa within the Maloideae are typically described as syncarpous, but Rohrer et al. (1991,
1994) indicate that much variation exists in the level of
connation among the carpels, including at least three genera
which are strictly apocarpous. Connation among carpels
in the Maloideae is at two levels (Rohrer et al., 1994). At
the level of the ovaries, connation is normally congenital
(Endress, 1994). Most maloid genera have carpels that are
fully fused to each other at this level, but variable degrees
of fusion exist in some genera, including Pyrus (Rohrer
et al., 1994), of which some species have been described
as apocarpous (Sterling, 1965b). In the Maloideae, connation at the level of the ovaries is external (Rohrer et al.,
1994) which probably limits the degree of inter-carpel communication in some genera, leading to the assumption of
imperfect syncarpy in Malus (Carr and Carr, 1961; Cresti
et al., 1980; Anvari and Stösser, 1981; Pratt, 1988; Weberling, 1989), a condition which does exist in other genera
(Gorchov and Estabrook, 1987; Gorchov, 1988). However,
small openings may be present at the centre of the core
(Rohrer et al., 1994), which may allow some degree of
inter-carpel communication. The second level of connation
among carpels occurs in the styles (Rohrer et al., 1994),
which develop from the apical portions of the carpel primordial (Evans, 1999). Some genera (e.g. Pyrus) develop
styles which appear completely separate throughout their
length (Rohrer et al., 1994; Aldasoro et al., 1998). Both
congenital and post-genital fusion can lead to the formation
of a compitum within connate areas of the carpels, including
the styles (P. K. Endress, pers. comm.). However, Endress
and Igersheim (2000) indicate that the degree of post-genital
fusion is probably dependent on its time of commencement,
being more intensive in forms which fuse earlier in
development.
Several studies have presented microscopic examination
of carpel structure (Sterling, 1964, 1965a–c, 1966; Rohrer
et al., 1991, 1994; Evans, 1999) and, at least partially,
pollen tube pathways in the Maloideae (Stott, 1972; Cresti
et al., 1980; Gorchov, 1988; Embree and Foster, 1999;
Kaufmane and Rumpunen, 2002; Broothaerts et al., 2004).
However, no studies have traced the transmitting tissue
within each carpel in its entirety, from stigma to micropyle.
For instance, the microscopic/histochemical study by
Cresti et al. (1980) of Starkrimson apple clearly shows
five separate areas of transmitting tissue within a transverse
section of the gynoecium just below the point of stylar union
(indicated here in Fig. 6), supporting their claim of imperfect syncarpy. Unfortunately the authors did not continue to
examine tissue below the point of stylar union, as it is below
this level that the majority of perfectly syncarpous gynoecia
have a compitum (Endress, 1994). Endress (1994) reports
that in flowers with free stigmatic lobes (as in Malus), only
05 mm of joined transmitting tissue is required to evenly
distribute pollen tubes among carpels when not all stigmas
are pollinated.
The present findings support the notion that not all stigmas have to be pollinated to obtain uniform pollen tube
distribution and full fertilization in Summerland McIntosh.
Seed yield in the present study evidences the presence of
a compitum, hence perfect syncarpy, in the apple flower
which allowed pollen tubes growing down individual styles
to cross into any of the five carpels. Seed number was higher
than expected from an imperfectly syncarpic gynoecium
when four or fewer stigmas were pollinated (Figs 4 and 5).
It is believed that neither pollen viability nor incompatibility
contributed to the lower than expected seed yield observed
for the five-stigma pollination treatment in both years. This
was probably a result of unrealized seed development in
Sheffield et al. — Perfect Syncarpy in Apple
some fruit, as ovules do not always develop into seeds in
the Maloideae (Rohrer et al., 1991). Further evidence of
perfect syncarpy was provided by the even distribution of
seeds among the carpels within fruits from all treatments
receiving pollination (Table 1). High levels of fertilization
and seed development among the carpels resulted in >40 %
fruit set in both years (Fig. 3) when at least one stigma was
pollinated. Only flowers which were not pollinated failed to
set fruit.
Other studies have indicated that several apple cultivars
may have gynoecia that are perfectly syncarpic (Beaumont,
1927; Visser and Verhaegh, 1987, and references therein).
Perfect syncarpy is considered a derived condition within
the angiosperms (Endress, 2001), and several evolutionary
advantages over apocarpous and imperfectly syncarpous
gynoecia have been recognized (Williams et al., 1993;
Endress, 1982, 1994). Among these are greater seed set
through more regular pollen tube distribution, economy
in flower construction, and increased gametophyte selection
among pollen grains in a unified transmitting tract (Endress,
1982, 1994).
Additional advantages may be gained with apically subdivided stigmatic surfaces for pollen capture (Howpage
et al., 1998). The flowers of Malus and most other
Maloideae attract a wide range of pollinators, and are not
specialized for a single group (Cambell et al., 1991). For
Malus, which has at least 44 bee visitors in Nova Scotia
(Sheffield et al., 2003), pollination efficacy among apoidean
visitors varies considerably (Boyle and Philogène, 1983;
Boyle-Makowski, 1987; Free, 1993, and references therein;
Goodell and Thompson, 1997; Vicens and Bosch, 2000).
However, subdivided stigmatic surfaces promote pollen
capture from a variety of positions, and accommodate differing foraging behaviours, albeit deposition may be uneven
among stigmas. Perfect syncarpy via the compitum allows
pollen tubes to be evenly delivered to ovules, despite
unequal deposition during pollination. As a result, total
pollen deposition by different bee visitors of Malus may
not be as indicative of potential fruit quality as previously
thought, and smaller or less effective floral visitors may be
contributing significantly to fruit production if at least one
stigmatic surface is adequately pollinated. More important
factors in determining seed set and fruit production in some
cultivars of apple are pollen viability, pollen compatibility
and pollen dispersal. The importance of these factors,
particularly with respect to orchard design, was recently
investigated by Kron et al. (2001a, b).
Visser and Verhaegh (1987) indicate that imperfect syncarpy may occur in some apple cultivars. Horticultural practices and breeding programmes have developed over 2000
apple cultivars worldwide (Morgan and Richards, 2002),
many of which show variability in fruit form (Rohrer
et al., 1991; Morgan and Richards, 2002). Differences in
floral form have also been reported among many cultivars
(Stott, 1972; Ferree et al., 2001). For instance, Stott (1972)
reports differences in the proportion of stylar fusion among
many apple cultivars. Some of the differences in floral form
among cultivars can be great enough to cause variation in
pollinator floral handling behaviour (Schneider et al., 2002),
in some instances to a level that pollinator effectiveness
589
(i.e. stigma contact) declines, as reported with the ‘sideworking’ behaviour of honey bees on ‘Delicious’ apples
(Robinson, 1979; Degrandi-Hoffman et al., 1985). It is possible that intensive cultivar development has created or
caused the loss of the compitum in some apple cultivars,
either through variable degrees of carpel separation at
the level of the ovaries or through reduced stylar fusion.
Gynoecial arrangements in the non-cultivated forms of
Malus (55 species reported in Phipps et al., 1990), including
the ancestor of the domesticated forms, M. sieversii
(Ledeb.) Roem. (Morgan and Richards, 2002), are presently
unknown. Clearly, gynoecial structure in apple cultivars
warrants further study as the presence or absence of a compitum directly influences fruit quality when pollination is
incomplete.
ACKNOWLEDGEMENTS
This study comprises part of the PhD research undertaken
by C.S.S. which was funded in part by the Agri-Focus 2000
Technology Development Program (Nova Scotia Department of Agriculture and Fisheries) and Agri-Futures-Nova
Scotia Association (Agriculture and Agri-Food Canada)
through the Nova Scotia Fruit Growers’ Association. This
paper is contribution number 2288 of the Atlantic Food and
Horticulture Research Centre. We thank Susan Rigby, for
experimental assistance during this project and for her
illustration, and the following for field assistance: Kim
Jansen, Meg Hainstock, Michelle Larson, Stephanie
Moreau, Derek Maske and Darrin Moran. For reviewing
the manuscript, we thank Dr Klaus Jensen, Atlantic Food
and Horticulture Research Centre–Agriculture and AgriFood Canada, Kentville, Nova Scotia, and two anonymous
reviewers. We also thank Dr Peter K. Endress, Institute of
Systematic Botany, University of Zurich, Switzerland for
clarification of floral morphology and terminology, and
Dr Rodger C. Evans, Acadia University Biology Department, Wolfville, Nova Scotia for his comments and for
providing a valuable piece of literature.
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