Journal of Horticultural Science & Biotechnology (2007) 82 (6) 875–884
Long-day control of flowering in everbearing strawberries
By A. SØNSTEBY1* and O. M. HEIDE2
Arable Crops Division, Section Kise, Norwegian Institute for Agricultural and Environmental
Research, NO-2350 Nes Hedmark, Norway
2
Department of Ecology and Natural Resource Management, Norwegian University of Life
Sciences, P. O. Box 5003, NO-1432 Ås, Norway
(e-mail: [email protected])
(Accepted 14 August 2007)
1
SUMMARY
Photoperiod and temperature control of flowering in a number of perpetual-flowering or everbearing strawberry
cultivars of widely varying pedigree has been studied in controlled environments. Flower bud initiation in the cultivars
‘Flamenco’, ‘Ridder’, ‘Rita’ and ‘Rondo’ was significantly advanced by long-day (LD) conditions at temperatures of
15°C and 21ºC; while, at 27ºC, flowering took place under LD conditions only. Some plants of the seed-propagated
F1-hybrid ‘Elan’, raised at 21°C, also flowered under short-day (SD) conditions at 27°C, but reverted to the vegetative
state after a few weeks when maintained under these conditions. When vegetative plants growing in SD at 27°C were
transferred to LD conditions at the same temperature, they consistently initiated flower buds and started flowering
after about 4 weeks. At such a high temperature, flowering could thus be turned on and off by switching between SD
and LD conditions. This applied to all the cultivars studied. Also the cultivar ‘Everest’, which was tested only at 21°C,
produced similar results. Night interruption for 2 h was effective in bringing about the LD response. At 9°C, flowering
was substantially delayed, especially in ‘Flamenco’ and, at this temperature, flowering was unaffected by photoperiod.
Runner formation was generally promoted by high temperature and SD conditions, but the photoperiodic effect
varied between experiments. We conclude that everbearing strawberry cultivars, in general, whether of the older
European-type or the modern Californian-type originating from crosses with selections of Fragaria virginiana ssp.
glauca, are qualitative (obligatory) LD plants at high temperature (27°C), and quantitative LD plants at intermediate
temperatures. Only at temperatures below 10°C are these cultivars day-neutral.
T
he physiology of flowering in cultivated strawberry
(Fragaria ananassa Duch.) has been the subject of
extensive research for nearly a century. While the
environmental control of flowering in single-cropping
(June-bearing) strawberry cultivars is well established
and documented (for reviews see Guttridge, 1985; Taylor,
2002), the situation is still rather confusing for cultivars
that produce more than one crop annually. These
cultivars are variably referred to as everbearers,
perpetuals, rebloomers and remontants (Galletta and
Bringhurst, 1990). Furthermore, modern American
octoploid everbearers, mostly derived from crosses
between wild Fragaria virginiana ssp. glauca Staudt
selections and single-cropping Fragaria ananassa, are
frequently referred to as day-neutrals or day-neutral
strawberries (Galletta et al., 1981, Galletta and
Bringhurst, 1990). Thus, Durner et al. (1984)
distinguished between everbearers [being older
everbearers with a long-day (LD) flowering response],
and day-neutrals (being modern everbearers with a dayneutral flowering response), and this terminology and
classification has generally been adopted in the
American literature (Galletta et al., 1981; Durner et al.,
1984; Nicoll and Galletta, 1987; Durner and Poling, 1988;
Galletta and Bringhurst, 1990; Sakin et al., 1997; Dale
et al., 2002). Bringhurst et al. (1989) stated that they
“prefer to use the term day-neutral rather than
everbearer because it is more descriptive of what is really
*Author for correspondence.
happening in strawberries”. Some workers, like Nicoll
and Galletta (1987), even distinguished between what
they termed “strong, intermediate and weak dayneutrals”. However, the rationale and validity of this
classification may be questioned.
Whereas the LD flowering response of older
everbearing cultivars was clearly demonstrated by
Darrow and Waldo (1934), and verified by Downs and
Piringer (1955), the day-neutral flowering response of
modern Californian everbearing cultivars has never been
demonstrated convincingly. One complicating factor is
the strong interaction of photoperiod with temperature,
which has been demonstrated in floral initiation of all
everbearing cultivars. Durner et al. (1984) examined the
flowering response of “everbearing” (EB) and “dayneutral” (DN) cultivars over a range of temperatures
(18°/14°C, 22°/18°C, 26°/22°C, or 30°/26ºC; day/night)
and with two photoperiods (9 h SD, or 9 h with a 3 h
night interruption = LD). Although they concluded that
SD conditions promoted flowering at 18°/14°C and at
22°/18ºC in EBs, while DNs flowered independently of
daylength conditions at these temperatures, the
differences were small and inconsistent. However, at the
higher temperatures, flowering was inhibited entirely by
SD conditions in both groups. Likewise, Nishiyama and
Kanahama (2000) demonstrated that floral initiation in
the everbearing cultivar ‘Summerberry’ was inhibited by
photoperiods of 13 h or less at 30°/25°C (day/night)
temperatures, while it was promoted by photoperiods of
14 h or longer at the same temperatures. In a subsequent
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Long-day strawberries
report by the same authors (Nishiyama and Kanahama,
2002) these findings were extended to the Californian
cultivar ‘Hecker’, which is of the so-called “strong dayneutral” type. They concluded that both cultivars
behaved as quantitative LD plants at intermediate
temperatures (22°/18ºC), and as qualitative LD plants at
high temperatures (30°/26ºC). Recently, we also
demonstrated that the everbearing F1-hybrid ‘Elan’ is a
quantitative LD plant at low and intermediate
temperatures (9° – 21ºC), while flowering is almost entirely
suppressed by SD at high temperature (27ºC; Sønsteby
and Heide, 2007). A critical photoperiod of approx. 15 h
for early flowering at 18ºC demonstrated that this
flowering response is truly photoperiodic in nature, and
not merely an effect of the additional light under LD
conditions, as suggested by Guttridge (1985).
The poor runnering capacity of everbearing
strawberry cultivars represents a severe problem for
their propagation and use (Battey et al., 1998; Dale et al.,
2002). However, as in single-cropping cultivars, flowering
and runnering also have contrasting environmental
requirements in everbearing cultivars, and Nicoll and
Galletta (1987) stated that there was an apparent
negative correlation between the strength of the
everbearing habit and the runnering capacity. Sønsteby
and Heide (2007) demonstrated that runnering in seedpropagated plants of ‘Elan’ ceased with the onset of
flowering, and that runnering was strongly promoted by
SD and high temperature conditions that are inhibitory
to flowering in this cultivar. These results suggest that the
vegetative state of the plant is a prerequisite for good
runner formation, and that the poor runnering capacity
of everbearing cultivars is a consequence of their
abundant and persistent flowering behaviour.
Based on these findings, we considered it important to
study the environmental control of flowering and
runnering in a wider range of everbearing strawberry
cultivars with different pedigrees, in order to verify the
LD flowering response of everbearing strawberry
cultivars in general, and the inverse relationship between
flowering and runnering control in these cultivars. The
results of such investigations are presented here.
MATERIALS AND METHODS
Plant material and cultivation
The six everbearing cultivars listed in Table I were
used for these experiments. In order to avoid premature
flower bud formation during propagation, young runner
tips were used for propagation. They were collected in
the field in July 2006 and rooted at 21ºC in saturated
humidity under natural LD (18 – 19 h), or 12 h SD
conditions in Experiment 1 and Experiment 2,
respectively. After rooting, the plants remained in the
same temperature and daylength conditions for another
3 weeks until they had developed two-to-three unfolded
leaves and the experiments were started. The seedpropagated F1-hybrid ‘Elan’ was germinated and raised
at 21°C for 4 weeks in SD, as described by Sønsteby and
Heide (2007). Throughout the experiments, all plants
were grown in natural daylight compartments for 10 h d–1
from 08.00h to 18.00h and were then moved into
adjacent growth rooms with darkness or low-intensity
incandescent light (about 7 µmol quanta m–2 s–1) for
daylength manipulation. Plants thus received almost the
same daily light integral under both daylengths.
Whenever the photon flux density in the daylight
compartments fell below 150 µmol m–2 s–1 on cloudy days,
an additional 125 µmol quanta m–2 s–1 were added
automatically by Philips HPT-I 400 W lamps. Otherwise
the plants were grown as described by Sønsteby and
Heide (2007).
Three experiments were carried out in the Ås
phytotron. In Experiment 1, only ‘Rita’ was used, and
plants were exposed to 10 h SD and 24 h LD conditions
at four constant temperatures (9°C, 15°C, 21°C or 27°C)
for 5 weeks. Plants were then transferred to 21°C and
24 h LD to record flower and runner development.
Experiment 2 included all six cultivars, and the same
photoperiod and temperature conditions as used in
Experiment 1. However, because of very poor runner
formation, a limited number of ‘Everest’ and ‘Ridder’
plants were available, and these cultivars were therefore
included at only one or two temperatures: 21°C for
‘Everest’, and 15°C and 27°C for ‘Ridder’. In this
experiment, all plants were exposed to these
combinations of photoperiod and temperature for
10 weeks. Experiment 3 compared the effects of SD
(10 h) and LD (24 h) with those of night interruption for
1 h or 2 h in the middle of the 14 h night in ‘Elan’. The
temperature in this experiment was maintained at 21°C
throughout the experiment, which lasted for 10 weeks.
Experimental design, data observation and analysis
Experiments 1 and 2 were fully factorial, of a split-plot
design, with temperatures as the main plots, and
photoperiod and cultivar as sub-plots. All Experiments
were replicated in three randomised blocks, each with
five plants (Experiment 1 and Experiment 2) or eight
plants (Experiment 3), making a total of 15 or 24 plants
per treatment. At the start of the Experiments, all
runners were removed, and leaf numbers and the petiole
length of the last fully-developed leaf were recorded on
each plant. The progress of flowering (time of first
anthesis in each plant) was observed twice a week, and
the number of new leaves, runners and open flowers
TABLE I
Origin and description of the everbearing strawberry cultivars used for the investigation
Cultivar
‘Elan’
‘Everest’
‘Flamenco’
‘Ridder’
‘Rita’
‘Rondo’
†
Origin (Breeder)
ABZ Seeds, The Netherlands (G. C. M. Bentvelsen)
Edward Vinson Ltd. UK
East Malling Research, UK (D. Simpson)
Norw. Univ. Life Sciences, Norway (J. Øydvin)
Norw. Univ. Life Sciences, Norway (J. Øydvin)
Norw. Univ. Life Sciences, Norway (J. Øydvin)
‘Rapella’ is a Dutch everbearing cultivar.
EMR 77 is a breeding line involving germplasm from The Netherlands, France and California.
‘Frida’ is a vigorous high-yielding Norwegian single-cropping cultivar with a complex pedigree.
‡
§
Parents
‘Fern’ ‘Rapella’†
‘Evita’ ‘Irvine’
‘Evita’ EMR 77‡
‘Rita’ ‘Elan’
‘Evita’ ‘Polka’
‘Elan’ ‘Frida’§
Type
F1-Hybrid
Clone
Clone
Clone
Clone
Clone
A. SØNSTEBY and O. M. HEIDE
were recorded once a week. Flowers and runners were
removed as they were recorded. The height of the first
inflorescence, measured from the base to the primary
flower, was recorded in each plant at first flower anthesis.
The number of flowers in the first inflorescence, and the
total number of inflorescences on each plant, were
recorded at the end of the Experiments.
All experimental data were subjected to analysis of
variance (ANOVA) by standard procedures using a
MiniTab® Statistical Software programme package
(Release 14; Minitab, Inc., State College, PA, USA).
RESULTS
Experiment 1
Leaf lamina and petiole growth were promoted
significantly by LD and high temperature during the
5-week treatment period, as usual (Guttridge, 1985; data
not shown). Flower bud initiation and flowering were
advanced by LD and high temperature conditions
(Figure 1). At 27°C, the earliest plants in LD had just
reached anthesis at the end of the treatment period and,
after another 2 weeks in LD at 21ºC, they all flowered;
whereas only 75% of plants from SD conditions
flowered, with an average delay of approx. 30 d. Longdays also advanced flowering at 21°C and 15°C, although
all plants from SD conditions also flowered at these
temperatures. All plants from 9°C also flowered in both
daylengths and, at this temperature, the earliness of
flowering was unaffected by photoperiod. ANOVA of
the days-to-anthesis data showed a significant flowering
advancement effect (P < 0.05) of both temperature and
LD, as well as their interaction. Furthermore, the number
of flowers per plant (Figure 1), and the number of
inflorescences per plant (data not shown), were
significantly higher in plants from LD than in those from
SD conditions, especially at high temperatures. Thus, at
27ºC, the number of flowers after 12 weeks was fivetimes higher in LD than in SD (Figure 1), while the
difference declined with decreasing temperature, and
disappeared at 9°C, yielding a highly significant
photoperiod temperature interaction (P < 0.01).
FIG. 1
Effects of temperature and photoperiod on flowering of the strawberry
cultivar ‘Rita’. Runner tips were rooted and raised for 4 weeks at 21°C
in natural Summer daylight (18 – 19 h) before the resulting plants were
exposed to the conditions shown for 5 weeks (weeks 0 – 5), then
transferred to 21°C and 24 h LD conditions for a further 7 weeks for
flower development. The data show cumulative flower numbers per
plant for 15 plants in each treatment.
877
On the other hand, stolon (runner) formation was
greatly enhanced by SD conditions, especially at 27°C
(the main effects of photoperiod and temperature were
both significant at P = 0.05). Runnering and flowering
were thus inversely affected by photoperiod (Figure 2).
Only at 9°C was runner formation unaffected by
photoperiod, conferring a highly significant interaction
(P = 0.002) between photoperiod and temperature in
stolon formation (Figure 2). Similarly, leaf formation was
strongly enhanced by SD conditions at 27ºC (approx.
three-times higher in SD than in LD), while it was
unaffected by photoperiod at 9°C and 15°C (interaction
significant at P = 0.008). The increased leaf number
under SD conditions at high temperatures was
accompanied by increased branching in SD, with the
additional number of leaves thus being formed mainly
on branch crowns (data not shown).
Experiment 2
In all cultivars, petiole length (canopy height) was
strongly enhanced by LD conditions at all temperatures,
with a maximum enhancement at 15°C. Petiole length
also increased markedly with increasing temperature,
although in LD, an optimum or a levelling-off occurred
at 15°C (data not shown). Leaf formation, on the other
hand, was enhanced by SD, except at 9°C, and increased
almost linearly across the range of temperatures (data
not shown). For both parameters the effect of
photoperiod and temperature, and their interaction,
were highly significant. There were also highly significant
differences among cultivars in these parameters. ‘Rita’
had, by far, the highest leaf number and the shortest
petioles, while ‘Rondo’ represented the opposite
situation.
Flowering was highly significantly promoted and
advanced by LD and high temperature in all cultivars
tested (Figure 3). At 27°C, all plants of ‘Flamenco’,
‘Ridder’ and ‘Rita’ flowered profusely in LD, whereas no
flowering took place in SD, even after 10 weeks under
these conditions. In ‘Elan’ and ‘Rondo’, on the other
hand, a few plants also flowered in SD at 27°C, but these
plants gradually ceased flowering and, by week 10, all
FIG. 2
Effects of temperature and photoperiod on stolon formation in the
strawberry cultivar ‘Rita’. Runner tips were rooted and raised for
4 weeks at 21°C in natural Summer daylight (18 – 19 h) before the
resulting plants were exposed to the conditions shown for 5 weeks
(week 0 – 5), then transferred to 21°C and 24 h LD conditions for a
further 7 weeks for stolon development. The data show cumulative
stolon numbers per plant for 15 plants in each treatment.
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Long-day strawberries
FIG. 3
Effects of temperature and photoperiod on flowering of six everbearing strawberry cultivars (Panels A – F). Runner tips were rooted and raised in
12 h SD at 21°C for 4 weeks before the resulting plants were exposed to the various conditions indicated for 10 weeks. The data show the cumulative
percentage of flowering plants over the treatment period. Values are for 15 plants in each treatment.
were entirely vegetative (Figure 4A). However, when
vegetative, SD-treated plants at 27°C were exposed to
LD at the same temperature for another 5 weeks, all
consistently started to flower after about 4 weeks
(Figure 4A). At 21°C, flowering in LD was almost as
early as at 27°C; but, at that temperature, more plants
flowered in SD compared with 27°C, particularly in
cultivars ‘Elan’ and ‘Rita’ (Figure 3C, F). Also at 15°C,
full flowering took place under LD conditions, except in
‘Flamenco’, although after a delay of a few weeks
compared with the higher temperatures. At this
temperature (15°C), several plants flowered under SD
A. SØNSTEBY and O. M. HEIDE
FIG. 4
Effect of photoperiod on flowering in five everbearing strawberry
cultivars. After being raised in 12 h SD at 21°C for 4 weeks, the resulting
plants were first exposed to 10 h SD for 10 weeks (weeks 0 – 10), then
transferred to 24 h LD for another 5 or 7 weeks, as indicated. The
temperature was maintained at 27°C throughout the experiment
(Panel A), or was first kept at 15°C for 10 weeks then raised to 27°C for
the rest of the period (Panel B). Data show the number of flowers
produced per plant per week over the experimental period. Values are
means of 15 plants in each treatment.
conditions. However, when transferred to LD at 27°C
they first developed the flowers that had been initiated
in SD at 15°C, then flowering gradually declined,
whereupon a new flush of flowers appeared that
obviously had been initiated after transfer to LD at 27°C
(Figure 4B). Also in ‘Everest’, which was studied only at
21°C, flowering was significantly advanced by LD
conditions. Furthermore, while all plants flowered under
LD conditions, only 50% flowering took place under SD
conditions (Figure 3A). However, when subsequently
transferred to SD at 27°C, plants completely ceased
flowering after a few weeks (data not shown). Both
temperature and LD effects were paralleled in the total
number of flowers produced during the 10-week
treatment period (Figure 5).
In the absence of fully orthogonal data for all cultivars
across the range of temperatures, three different ANOVA
analyses (with different temperatures and cultivars
represented) were performed. In all cases, analyses
revealed highly significant main effects of both
photoperiod and temperature, as well as their interaction
(P < 0.001) for all flowering parameters (% flowering
plants, number of inflorescences, flowers per plant, and
days to anthesis). There was also a highly significant
cultivar effect on all these parameters and, for the number
of flowers per plant, there was also a highly significant
cultivar photoperiod interaction (P < 0.001). Thus,
‘Flamenco’ had a more stringent photoperiodic control of
flowering than ‘Elan’ (Figures 3 – 5). The most abundant
879
flowering occurred in ‘Rita’ and ‘Ridder’, and, in general,
at temperatures of 21°C and 27°C (Figure 5). At 15°C,
flowering was delayed by several weeks compared with
the higher temperatures, particularly in ‘Flamenco’ and
‘Rondo’ (Figure 3). However, when the 15ºC plants were
transferred to 27°C and LD conditions after 10 weeks,
they increased their flowering rapidly, and their final
number of flowers exceeded those of the corresponding
plants from 21°C and 27°C (data not shown).
Stolon formation was significantly enhanced by high
temperatures in all cultivars, usually with an optimum at
21°C. However, in contrast to the situation in ‘Rita’ in the
previous experiment, more runners were formed in LD
than in SD in all cultivars (Figure 6). The only exceptions
to this were ‘Elan’ plants at 27°C which, after a delay, had
a strong and sustained increase in stolon formation in
SD. The cultivars also varied significantly in their
runnering ability (P = 0.01); ‘Everest’ having the poorest,
and ‘Elan’ the best runner formation (Figure 6).
None of the plants grown at 9°C flowered within the
10-week treatment period, regardless of photoperiodic
conditions. However, when subsequently transferred to
21°C and LD conditions to assess flowering ‘aftereffects’, the cultivars varied significantly in their
flowering behaviour (Figure 7). Whereas ‘Rondo’, and
particularly ‘Elan’, flowered early and rapidly after
transfer, indicating that advanced flower primordia had
been formed at 9°C, flowering of ‘Flamenco’ was delayed
and slow, indicating that initiation in this cultivar had
occurred mainly after transfer to the higher temperature
(cf. Figures 3 – 5). The total number of flowers per plant
was significantly less in ‘Flamenco’ than in the other
cultivars (P < 0.05), mainly as an effect of delayed
flowering. Although ‘Rondo’ and ‘Elan’ plants from LD
tended to have earlier and better flowering than those
from SD, there was no significant after-effect of
photoperiod on flowering at 9°C. In all cultivars, only a
few stolons were formed at 9°C, and there was no effect
of photoperiod on stolon formation at this temperature
(Figure 7).
Experiment 3
In order to study further the photoperiodic nature of
the LD response of everbearing strawberry, the effects of
1 h and 2 h night interruptions were compared with those
of 10 h SD and 24 h LD in ‘Elan’ at 21°C. Flowering was
promoted and advanced by LD, and a 2 h interruption in
the middle of the 14 h night significantly promoted
flowering compared with SD, while a 1 h night break had
no significant effect on flowering (Figure 8), although
significantly promoting vegetative growth (Table II).
Stolon formation also was significantly enhanced by LD
and by a 2 h night interruption, while the effect of a 1 h
night interruption was non-significant (Table II).
DISCUSSION
These experiments confirm and strengthen our
previous findings that everbearing or perpetual
flowering strawberry cultivars are long-day plants
(LDPs) (Sønsteby and Heide, 2007), rather than dayneutral plants, as was generally assumed (Smeets, 1980;
Galletta et al., 1981; Durner et al., 1984; Nicoll and
Galletta, 1987; Durner and Poling, 1988; Galletta and
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Long-day strawberries
FIG. 5
Effects of temperature and photoperiod on flowering of six everbearing strawberry cultivars (Panels A – F). Runner tips were rooted and raised under
12 h SD conditions at 21°C for 4 weeks before the resulting plants were exposed to the various conditions indicated for 10 weeks. Data show the
cumulative number of flowers per plant produced over the treatment period. Values are the means ± SE of 15 plants in each treatment.
Bringhurst, 1990; Sakin et al., 1997; Dale et al., 2002). Not
only did the cultivar ‘Elan’, used in our previous
experiments, show this response, but a range of other
everbearers with widely varying pedigrees, also showed
the same or an even stronger LD flowering response
(Figure 3). However, as also reported by Nishiyama and
Kanahama (2000; 2002), this photoperiodic effect is
strongly temperature-dependent and increases with
increasing temperature (Figures 3 – 5). The fact that a
night interruption is effective in causing the LD response
(Figure 8; Table II), proves beyond any doubt that the
response is truly photoperiodic in nature. It is clear,
however, that an interruption of several hours is required
for a full response. Even a 2 h interruption was far less
effective than continuous light, and a 1 h break had only
a marginal effect on flowering (Figure 8; Table II). That
A. SØNSTEBY and O. M. HEIDE
881
FIG. 6
Effects of photoperiod and temperature on stolon formation of six everbearing strawberry cultivars (Panels A – F). Runner tips were rooted and
raised under 12 h SD conditions at 21°C for 4 weeks before the resulting plants were exposed to the various conditions indicated for 10 weeks. Data
show the cumulative number of stolons per plant produced over the treatment period. Values are the means ± SE of 15 plants in each treatment.
LD plants, in general, are less rhythmic and require much
longer night interruptions for their photoperiodic
response than do SD plants, is a well known fact that was
observed by early work on photoperiodism (Hamner,
1940; Thomas and Vince-Prue, 1997). Nevertheless, 3 h
night interruptions have been used successfully as a LD
treatment to select for perpetual-flowering strawberries
(Durner et al., 1984; Nicoll and Galletta, 1987).
The notion that modern everbearing strawberries are
day-neutral plants seems to have originated from the
Summer-flowering selection technique, used for the
identification of progenitors exhibiting the perpetualflowering trait. Commonly, such populations are planted
in a glasshouse in late Summer and their flowering
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Long-day strawberries
FIG. 7
‘After-effects’ of photoperiod at 9°C on flowering and stolon formation under subsequent LD conditions (24 h) at 21°C in three everbearing
strawberry cultivars. The plants had previously been exposed to 10 h SD or 24 h LD conditions at 9°C for 10 weeks (week 0 – 10), during which time
no flowering or runnering took place. Data show the cumulative percentage of flowering plants (Panels A, C, E) and the cumulative numbers of
flowers and stolons produced per plant (Panels B, D, E) during the subsequent 9-week LD period at 21°C. Values are for 15 plants in each treatment.
behaviour is observed during the subsequent Spring and
Summer (e.g., Sakin et al., 1997). Alternatively, seedlings
are planted in Spring and tested for their ability to flower
during the first Summer (Barritt et al., 1982). Under both
conditions, plants with a perpetual-flowering trait are
easily distinguished from single-cropping SD types by
their ability to flower during the long days of Summer.
However, to our knowledge, the true day-neutral
flowering response of these plants has never been
demonstrated by direct experimentation.
In 1934, Darrow and Waldo demonstrated that
everbearing strawberry cultivars are LD plants forming
flower buds under the long days of Summer, and this was
later confirmed by Downs and Piringer (1955). However,
it has been argued that this LD behaviour is restricted to
old everbearing cultivars, mainly of European origin,
which are genetically distinct from the modern
Californian types, originating from crosses with
selections of Fragaria virginiana spp. glauca (e.g., Sakin
et al., 1997). In the American horticultural literature, old
A. SØNSTEBY and O. M. HEIDE
883
been raised at 21°C, and it is thus possible that some
plants had initiated inflorescences before the high
temperature treatment was started. This is supported by
the finding that they quickly reverted to the vegetative
state under continued SD conditions at 27°C and,
furthermore, that flowering was consistently re-initiated
by a subsequent transition to LD at the same
temperature (Figure 4A). ‘Flamenco’ had a strict LD
requirement also at intermediate temperatures and,
furthermore, had significantly delayed flowering at 15°C
compared with the other cultivars, suggesting a relatively
high temperature optimum for LD floral initiation in this
cultivar. Due to the limited availability of plants (poor
runnering ability), the commercially important ‘Everest’
was studied only at 21°C, and should, therefore, be
subjected to further studies. Nevertheless, the LD
response at 21°C was as strong in ‘Everest’ as in the other
cultivars (Figure 3; Figure 5) and, when subsequently
moved to SD at 27°C, ‘Everest’ completely ceased
flowering after a few weeks (data not shown).
During glasshouse production of everbearing
strawberry cultivars in the UK, it has been observed that
a sudden decline in flowering and fruiting may occur
during excessively hot periods in July and August, a
condition termed “thermodormancy”. Similar problems
have been encountered with everbearing cultivars in
continental areas of the USA characterised by extreme
Summer temperatures (Dale et al., 2002). Wagstaffe and
Battey (2006a, b), who studied the phenomenon in
‘Everest’, found that the optimum temperature for
flowering and fruiting was about 23°C, while
temperatures above 26°C were supra-optimal. They also
found that a low night temperature (13°C) effectively
ameliorated the negative effect of a high day
temperature (Wagstaffe and Battey, 2006b). These
temperatures agree well with the present results under
SD conditions, and the decreasing daylength during late
July and August may therefore be an important
contributing factor. Thus, the critical photoperiod for the
LD response of ‘Elan’ is about 15 h (Sønsteby and Heide,
2007), a daylength which is only 1 h less than midsummer
daylength in southern England. Considering the strong
photoperiodic effect involved, and the relative
ineffectiveness of the critical, compared with the optimal
daylength, it is anticipated that daylength extension, or a
few hours of night interruption, would eliminate the socalled “thermodormancy” (cf. Figure 4).
The results also confirm our previous finding
(Sønsteby and Heide, 2007) that runner formation is also
enhanced by high temperature in everbearing strawberry
cultivars, whereas the effect of photoperiod varied
between experiments (Figure 2; Figure 6). While the
results with ‘Rita’ in Experiment 1 confirmed that
FIG. 8
Effect of different photoperiodic treatments on flowering of ‘Elan’
strawberry. Plants were raised for 4 weeks under 10 h SD, then exposed
to the photoperiodic treatments indicated for 10 weeks. The
temperature was maintained at 21°C throughout. The photoperiodic
treatments consisted of regular SD and LD treatments (10 h and 24 h,
respectively) and a night interruption with low-intensity incandescent
light in the middle of the 14 h dark period (night) for 1 h (10 + 1 h) or
2 h (10 + 2 h), respectively. Data show the cumulative numbers of
flowers per plant. Values are the means ± SE of 24 plants in each
treatment.
and modern perpetual-flowering types have, therefore,
commonly been termed everbearing and day-neutral
cultivars, respectively (Darrow, 1966; Galletta et al., 1981;
Durner et al., 1984; Nicoll and Galletta, 1987; Durner and
Poling, 1988; Galletta and Bringhurst, 1990; Sakin et al.,
1997; Dale et al., 2002). However, the present results, as
well as those of Nishiyama and Kanahama (2000; 2002)
and Sønsteby and Heide (2007) using perpetualflowering cultivars of widely varying pedigree, clearly
demonstrate that there is no rationale for this distinction.
Even the “strong day-neutral” cv. Hecker, used by
Nishiyama and Kanahama (2002), behaved as an
obligatory LD plant at high temperature. All these
results indicate that perpetual-flowering strawberry
cultivars, in general, are qualitative (obligatory) LDPs at
high temperatures (> 25°C) and quantitative LDPs at
intermediate temperatures (15° – 21°C). Only at
temperatures below 10°C do they appear to be more-orless day-neutral (Figures 3 – 5; Figure 7).
Although all everbearers proved to be LD plants,
there were some differences among cultivars in the
stringency of the LD flowering response. At high
temperatures (27°C), floral initiation had an obligatory
LD requirement in all cultivars, although almost 50% of
‘Elan’ plants also flowered in SD at 27°C (Figure 3).
However, it should be kept in mind that these plants had
TABLE II
Effects of photoperiodic treatment (SD, LD, or SD with a 1 h or 2 h night interruption) on flowering and growth of ‘Elan’ strawberry plants†
Photoperiod (h)
10
24
10 + 1
10 + 2
P value
Days to
anthesis
50 ab*
42 c
51 a
47 b
0.002
Infloresc. length
(cm)
9.9 a
20.3 c
17.2 b
22.3 c
< 0.001
Leaves before
flowering
8.3 a
6.8 b
8.5 a
7.4 b
0.01
Petiole length
(cm)
Leaves
per plant
Stolons
per plant
10.8 a
15.7 b
15.5 b
16.7 b
0.001
11.9 ab
10.4 b
12.5 a
11.1 ab
0.04
0.8 a
3.3 b
1.7 ab
3.0 b
0.04
†
Plants were raised in 10 h SD for 4 weeks, then exposed to the conditions specified for 10 weeks. Temperature was maintained at 21ºC throughout.
Data for 24 plants in each treatment were recorded after 10 weeks of treatment.
*
Mean values within each column followed by different lower-case letters are significantly different (P < 0.05)
884
Long-day strawberries
runnering is strongly enhanced by SD at high
temperature, the results with ‘Rita’ and the other
cultivars in Experiment 2 showed the opposite trend
(with the exception of ‘Elan’). It should be kept in mind,
however, that in Experiment 1 the plants were rooted
and raised under LD conditions, whereas those in
Experiment 2 were raised in SD, as were the ‘Elan’ plants
in Experiment 3 (Table II). Thus, it is possible that, in the
latter experiments, runners were initiated during the SD
period of propagation, and that only their development
was enhanced by the subsequent transition to LD
conditions. This possibility is supported by the fact that
runnering ceased as soon as flowering started in LD in
Experiment 2 (Figure 6). On the other hand, the ‘Elan’
plants in our previous report were already segregated
into SD and LD conditions from germination (Sønsteby
and Heide, 2007). Nevertheless, the photoperiodic effect
on runner initiation and development in everbearing
strawberries needs further corroboration. ‘Everest’ was
found to have a particularly poor runnering ability
compared with all the other cultivars studied, and a
method to improve the runnering capacity of this
cultivar is urgently needed.
In conclusion, the present results, together with those
of Nishiyama and Kanahama (2000; 2002) and Sønsteby
and Heide (2007), demonstrate that everbearing
strawberry cultivars, in general, are qualitative LD plants
at high temperature (27°C), and quantitative LD plants
at intermediate temperatures (15°C and 21°C). This
applies to modern Californian cultivars as well as to
older cultivars, mainly of European origin, and there is
thus no rationale for the classification of the former as
day-neutral plants.
We are indebted to the Research Council of Norway
for financing of this work through Project No.
161971/I10, and to Mr. Bjørn Hageberg for skillful
technical assistance.
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