Annals of Botany 80 : 547–552, 1997

Phases of Development to Flowering in Opium Poppy (Papaver somniferum L.)

under Various Temperatures
Z H O N G C H U N W A N G*, M A R Y C. A C O C K and B A S I L A C O C K
USDA-ARS, Remote Sensing and Modeling Laboratory, BeltsŠille, MD 20705, USA

Received : 12 March 1997 Accepted : 2 July 1997

Development up to flowering in opium poppy (PapaŠer somniferum L.) has been divided into four phases from
emergence to anthesis which mark changes in its sensitivity to photoperiod : a photoperiod-insensitive juvenile phase
(JP), a photoperiod-sensitive inductive phase (PSP), a photoperiod-sensitive post-inductive phase (PSPP) and a
photoperiod-insensitive post-inductive phase (PIPP). To predict flowering time under field conditions, it is essential
to know how these phases are affected by temperature. Plants were grown in artificially-lit growth chambers and
received three different temperature treatments : 15}10, 20}15 and 25}20 °C in a 12 h thermoperiod. Plants were
transferred within each temperature regime from a non-inductive 9 h to an inductive 16 h photoperiod or Šice Šersa
at 1–4 d intervals to determine the durations of the four phases. Temperature did not affect the duration of the first
two phases (i.e. JP lasted 3–4 d and PSP required 4–5 d). The most significant effect of temperature was on the
duration of PSPP which was 28, 20 and 17 d at 15}10, 20}15 and 25}20 °C, respectively. The temperature effect on
PIPP was small (maximum difference of 3 d between treatments) and the data too variable to indicate a significant
trend. Our results indicate that PSPP is the only phase that clearly exhibits sensitivity to temperature.
# 1997 Annals of Botany Company

Key words : Days to flower, opium poppy, PapaŠer somniferum L., phases of flower development, photoperiod,
temperature.

Photoperiod alone cannot adequately predict flowering

INTRODUCTION
The onset of flowering in the opium poppy (PapaŠer
somniferum L.) is influenced by photoperiod (Acock, Wang
and Acock, 1996). The critical photoperiod (the photoperiod
below which flowering is delayed) for opium poppy is near
16 h (Gentner, Taylorson and Borthwick, 1975 ; Acock et
al., 1996). However, flower development of poppy plants is
not sensitive to photoperiod throughout the period from
sowing to first flowering (Wang, Acock and Acock, 1997).
Wang et al. (1997) divided the interval between emergence
and first flower into four phases : (1) a photoperiod-
insensitive (juvenile) phase (JP), in which poppy plants were
insensitive to photoperiod during the first 4 d after emerg-
ence ; (2) a photoperiod-sensitive inductive phase (PSP), in
which plants required a minimum of four 16-h inductive
cycles for rapid flowering ; (3) a photoperiod-sensitive post-
inductive phase (PSPP), in which plants required approx.
nine additional inductive cycles for flowering to occur
without delay ; and (4) a photoperiod-insensitive post-
inductive phase (PIPP), in which flowering time was no
longer influenced by photoperiod. Further studies indicated
that the duration of JP was a function of photoperiod
(Wang et al., unpubl. res.). Plants transferred from a 9 h to
an 11-, a 12-, or a 14-h photoperiod had a longer JP and
required more inductive cycles (i.e. longer PSP and PSPP)
before they reached the start of PIPP than those transferred
to a 16 h photoperiod.
* For correspondence. Fax ­301 504 5823, e-mail zwang!asrr.
arsusda.gov
0305-7364}97}100547­06 $25.00}0
time because temperature also influences floral development.
The optimum daily mean temperature for poppy growth
and development is between 16–20 °C (Acock, Pausch and
Acock, 1997). Low temperatures delay poppy development
(Bernath and Tetenyi, 1981). However, whether temperature
affects all four phases has not been established. The current
experiment was designed to determine how the durations of
these phases change when plants are grown at different
temperatures. The specific objectives of the experiment
were : (1) to determine whether the duration of JP depends
on temperature ; (2) to identify phases of floral initiation
and development that are temperature sensitive ; and (3) to
determine the magnitude of the influence of temperature for
each phase of development. The data obtained will provide
essential information required for predicting flowering time
of poppy plants in field conditions.
MATERIALS AND METHODS
Plant culture and treatments
Seeds of PapaŠer somniferum (cv. album DC) were sown in
3±75 l black plastic pots filled with a Jiffy Mix growing
medium (Jiffy Products, Batavia, IL, USA) consisting of
Canadian sphagnum peat and vermiculite (1 : 1, v}v).
Dolomitic lime was added to adjust the pH of the medium
to 6±0. Six ‘ reach-in ’ controlled environment chambers
(Environmental Growth Chambers, Inc., Chagrin Falls,
OH, USA) were used, with 34 pots in each chamber. Each
chamber was provided with a combination of six high
bo970490 # 1997 Annals of Botany Company
548 Wang et al.—Temperature Effects on Phases of DeŠelopment to Flowering
pressure sodium and six metal halide lamps that were
arranged alternately in three rows. Photosynthetic photon
flux density inside the growth chambers was maintained at
1000³100 µmol m−# s−" at the top of the plant canopy by
adjusting a high intensity discharge dimmer. Stern’s Miracle-
Gro fertilizer (15±0N-13±1P-12±4K) was applied weekly to
each pot in 250 ml of irrigation water at a nitrogen
concentration of 175 mg l−" during the first 3 weeks after
emergence and then applied twice a week during the
remaining experimental period. Plants were watered as
needed during the experiment and thinned to one per pot
20 d after emergence (DAE).
Three temperature treatments, 15}10, 20}15 and
25}20 °C, at a 12 h thermoperiod (0800–2000 h), were
applied to the six chambers (one temperature treatment for
two chambers). The range of temperatures selected are
common for most poppy growing regions worldwide during
the growing season. For each temperature treatment, one
chamber was programmed at a photoperiod of 9 h from
0800 to 1700 h, and the other programmed at a photoperiod
of 16 h from 0800–2400 h. The 9 h photoperiod was chosen
as a non-inductive photoperiod because it is short enough to
keep plants vegetative (Acock et al., 1996). The 16 h cycle
was chosen as an inductive photoperiod because it exceeds
the critical photoperiod for poppy (Acock et al., 1996) and
also because it can be compared with previous results
(Wang et al., 1997).
Transfer plans
The plants were transferred, three at a time, from a 9 h to
a 16 h photoperiod or Šice Šersa within each temperature
regime at different intervals.
For the plants transferred from a 9 h to a 16 h photoperiod
within each temperature treatment, transfers began on the
day of seedling emergence (0 DAE) and were made at 1 d
intervals until 5 DAE, after which time transfers were made
at 2 to 4 d intervals up to 28 DAE. Three plants in the 9 h
photoperiod at each temperature were never transferred and
were used as controls. After a plant was transferred from a
9- to a 16-h photoperiod, it was grown in the new 16 h
photoperiod until the first flower opened.
For the plants transferred from a 16 h to a 9 h photoperiod
within each temperature regime, transfers were made at 2 to
3 d intervals from 6 to 30 DAE. Three more transfers from
30 to 42 DAE were made at 4 d intervals for plants grown
at 15}10 °C. Three plants in the 16 h photoperiod at each
temperature were never transferred and used as controls.
After a plant was transferred, it was grown in the 9 h
photoperiod until the first flower opened or the experiment
was terminated at 93 DAE.
The day of emergence was defined as the day when the
two cotyledons had unfolded (Wang et al., 1997). The dates
on which seedlings emerged and the first flower opened were
recorded for each plant.
Phase determination
Linear equations were chosen to describe the relationship
between the days to flower and the days to transfer from one
photoperiod to another at each temperature. The de-
termination of the four phases from emergence to anthesis
was similar to the methods described by Wilkerson et al.
(1989) and reported previously (Wang et al., 1997). The
duration of JP for each temperature was determined by
transferring plants at different intervals from the non-
inductive 9 h to the inductive 16 h photoperiods after
seedling emergence. The end of JP was estimated by
intersection of two linear equations. One linear equation
with a zero gradient had intercept values of the average
flowering times for plants grown continuously in a 16 h
photoperiod at each temperature. The second linear equa-
tion with a non-zero gradient was obtained using the
flowering times from the 9- to the 16-h transfers. The
flowering times from the first few transfer dates that
decreased the r# value of the equation were omitted from the
second equation.
The duration of PSP for each temperature treatment was
determined by transferring plants at regular intervals from
the inductive 16 h to the non-inductive 9 h photoperiod
after seedling emergence. By subtracting the estimated
duration of JP from the minimum number of days required
for rapid flowering, the minimum duration of PSP was
estimated.
The end of PSPP was defined as the earliest day before
anthesis when flowering time was no longer influenced by
photoperiod, i.e. flowering times were the same as controls.
The duration of PSPP was then derived by subtracting the
estimated durations of the first two phases (JP and PSP)
from the day when PSPP ended.
The minimum duration of PIPP before the first flower
opened was calculated by subtracting the minimum days for
the first three phases (JP, PSP and PSPP) from the days to
flower in the 16 h photoperiod control groups at each
temperature.
The standard errors of the means (n ¯ 3) for days to
flower were calculated and presented for each transfer in
each temperature treatment. Due to the relatively large
difference in the duration of PIPP at 25}20 °C when
compared to our previous experiments (Wang et al., 1997),
values obtained from the 16 h to the 9 h transfers at
25}20 °C were combined (n ¯ 12) over four separate
experiments to generate the relationship between the days to
flower and the days to transfer.
RESULTS
Photoperiod-insensitiŠe juŠenile phase (JP)
A linear equation was chosen to describe the relationship
between the days to flower and the days to transfer from the
non-inductive 9 h to the inductive 16 h photoperiod at
15}10 °C (Fig. 1). The average flowering time for plants
grown continuously in a 16 h photoperiod at 15}10 °C was
46 d (Fig. 1). The first few transfers from 0 to 5 DAE did not
affect flowering time when compared with the 16 h non-
transferred plants. Later transfers delayed flowering times
to approx. 52, 62 and 72 d when transfers were made at 10,
20 and 30 DAE, respectively. The end of JP, defined as the
day at intersection of the two linear equations, was 4 DAE
in the 15}10 °C treatment (Fig. 1).
 Wang et al.—Temperature Effects on Phases of DeŠelopment to Flowering 549
80 25/20°C
15/10°C 64

Days from emergence to flowering

72
Days from emergence to flowering

56
64

y = 41.6 + 1.03x 48
56
2
r = 0.89 y = 29.1 + 1.10x
r2 = 0.98
48 40

40
32

32
24
24
0 4 8 12 16 20 24 28 32
0 4 8 12 16 20 24 28 32 Days from emergence to transfer
Days from emergence to transfer F. 3. Days from emergence to flower as a function of days from
F. 1. Days from emergence to flower as a function of days from emergence to transfer for poppy plants grown at a 12 h thermoperiod
emergence to transfer for poppy plants grown at a 12 h thermoperiod (0800–2000 h) of 25}20 °C and transferred from a 9- to a 16-h
(0800–2000 h) of 15}10 °C and transferred from a 9- to a 16-h photoperiod. The broken line indicates the average number of days to
photoperiod. The broken line indicates the average number of days to flower (32±3 d) for plants that remained in a 16 h photoperiod. Vertical
flower (45±5 d) for plants that remained in a 16 h photoperiod. Vertical bars represent s.e. (n ¯ 3).
bars represent s.e. (n ¯ 3).
T     1. Estimates for the end of the juŠenile phase and
20/15°C
minimum number of inductiŠe day}night cycles required for
64 floral deŠelopment of poppy plants at 15}10, 20}15 and
25}20 °C
Days from emergence to flowering

56 Temperature (°C)

15}10 20}15 25}20

48
y = 32.7 + 0.99x Estimated end of the juvenile phase 4 4 3
(DAE*)
r2 = 0.94
40 Minimum number of days required for 8 8 8
rapid flower initiation (DAE)
Estimated end of photoperiod influence 36 28 25
on flowering (DAE)
32
Total number of days required for 46 37 32
flowering (DAE)

24
* DAE, days after emergence.

0 4 8 12 16 20 24
Days from emergence to transfer
F. 2. Days from emergence to flower as a function of days from
emergence to transfer for poppy plants grown at a 12 h thermoperiod
(0800–2000 h) of 20}15 °C and transferred from a 9- to a 16-h
photoperiod. The broken line indicates the average number of days to
flower (36±5 d) for plants that remained in a 16 h photoperiod. Vertical
bars represent s.e. (n ¯ 3).
There were also linear relationships between the days to
flower and the days to transfer at 20}15 °C (Fig. 2) and
25}20 °C (Fig. 3). Using the same procedures described
above, the end of JP was estimated to be 4 and 3 d for the
20}15 and 25}20 °C treatments, respectively. Estimates for
the end of JP for each temperature, the minimum number of
inductive days required for flower initiation, and the end of
28 32
photoperiod influence on flowering are summarized in
Table 1.
Photoperiod-sensitiŠe inductiŠe phase (PSP)
Plants grown at 15}10 °C and transferred from the
inductive 16 h to the non-inductive 9 h photoperiod at
8 DAE flowered after 68 d, whereas no plants transferred
prior to 8 DAE flowered during the course of the ex-
perimental period (93 DAE) (Fig. 4). It appeared that a 16 h
photoperiod for 8 DAE was critical for poppy plants to
initiate a rapid qualitative transition from vegetative to
reproductive development. Subtracting the estimated dur-
ation of JP from the pivotal day (8 d) resulted in an
estimated 4 d for PSP at 15}10 °C. Estimates of the durations
550 Wang et al.—Temperature Effects on Phases of DeŠelopment to Flowering
80 20/15°C
15/10°C 64

Days from emergence to flowering

72
Days from emergence to flowering

56 y = 65.2 – 1.02x
2
r = 0.75
64 y = 74.8 + 0.83x
2
r = 0.86 48

56
40

48
32

40 24

0 4 8 12 16 20 24 28 32
32
Days from emergence to transfer
0 4 8 12 16 20 24 28 32 36 40
Days from emergence to transfer F. 5. Days from emergence to flower as a function of days from
emergence to transfer for poppy plants grown at a 12 h thermoperiod
F. 4. Days from emergence to flower as a function of days from (0800–2000 h) of 20}15 °C and transferred from a 16- to a 9-h
emergence to transfer for poppy plants grown at a 12 h thermoperiod photoperiod. The broken line indicates the average number of days to
(0800–2000 h) of 15}10 °C and transferred from a 16- to a 9-h flower (36±5 d) for plants that remained in a 16 h photoperiod. Vertical
photoperiod. The broken line indicates the average number of days to bars represent s.e. (n ¯ 3).
flower (45±5 d) for plants that remained in a 16 h photoperiod. Vertical
bars represent s.e. (n ¯ 3).

25/20°C
T     2. Estimates of durations of the juŠenile phase (JP), 56
the photoperiod-sensitiŠe inductiŠe phase (PSP), the photo-
Days from emergence to flowering

period-sensitiŠe post-inductiŠe phase (PSPP) and the photo- y = 57.8 – 1.00x

period-insensitiŠe post-inductiŠe phase (PIPP) in poppy plants 48 r2 = 0.47
grown at 15}10, 20}15 and 25}20 °C

Estimated durations at different temperatures (d)

40
Phases 15}10 °C 20}15 °C 25}20 °C

JP 4 4 3 32
PSP 4 4 5
PSPP 28 20 17
PIPP 10 9 7
Total 46 37 32 24

of these four phases for each temperature regime are
summarized in Table 2.
The minimum number of inductive day}night cycles
required for rapid flowering also appeared to be 8 DAE for
plants grown at 20}15 (Fig. 5) and 25}20 °C (Fig. 6) (Table
1). Thus, the minimum duration of PSP was estimated as 4
and 5 d at 20}15 and 25}20 °C, respectively (Table 2).
Photoperiod-sensitiŠe post-inductiŠe phase (PSPP)
The rate of flower development for plants transferred
from the 16 h to the 9 h photoperiod at 15}10 °C was
enhanced as the number of inductive cycles increased (Fig.
4). The days to flower decreased from 68 d for plants
transferred at 8 DAE to 58 d for plants transferred at
20 DAE. The time before anthesis when plants were no
longer sensitive to photoperiod, i.e. the point of the
0 4 8 12 16 20 24 28 32
Days from emergence to transfer
F. 6. Days from emergence to flower as a function of days from
emergence to transfer for poppy plants grown at a 12 h thermoperiod
(0800–2000 h) of 25}20 °C and transferred from a 16- to a 9-h
photoperiod. Each value of the days to flower was an average of 12
observations obtained from four separate experiments including this
one. The broken line indicates the average number of days to flower
(32±1 d) for plants that remained in a 16 h photoperiod. Vertical bars
represent s.e.
intersection between two linear equations, was calculated to
be 36 d (Table 1). Thus, by subtracting the durations of JP
and PSP, the minimum duration of PSPP was estimated as
28 d (Table 2).
Similar trends were obtained in the 20}15 (Fig. 5) and
25}20 °C treatments (Fig. 6). Plants were no longer sensitive
to photoperiod at 28 d for 20}15 °C and at 25 d for
 Wang et al.—Temperature Effects on Phases of DeŠelopment to Flowering
25}20 °C (Table 1). Therefore, the minimum duration of
PSPP was estimated as 28 d at 15}10 °C, 20 d at 20}15 °C
and 17 d at 25}20 °C (Table 2).
Photoperiod-insensitiŠe post-inductiŠe phase (PIPP)
The minimum duration of PIPP before the first flower
opened was calculated to be 10, 9 and 7 d at 15}10, 20}15
and 25}20 °C, respectively (Table 2). This was derived by
subtracting the minimum days for the first three phases
from the days to flower in the 16 h photoperiod control
groups at each temperature.
DISCUSSION
Our results indicate that the durations of the first two
phases, JP and PSP, were relatively constant and did not
change within the temperature range tested. Plants trans-
ferred from a 9- to a 16-h photoperiod within each of the
15}10, 20}15 and 25}20 °C treatments first demonstrated
transfer effects 3–4 DAE and required a minimum of 4–5
inductive cycles for the plant to flower. This result confirmed
previous findings that plants grown at 25}20 °C required at
least four inductive cycles in a 16 h photoperiod before they
would flower rapidly (Wang et al., 1997).
After the minimum inductive cycles for flowering were
given, additional inductive cycles, i.e. PSPP, hastened
flowering. The duration of PSPP was strongly temperature-
dependent and was the only phase that demonstrated a
significant decrease in duration with an increase in tem-
perature. Plants grown at 15}10 °C required 8 and 11 more
inductive cycles to reach the final phase (PIPP) than those
grown at 20}15 and 25}20 °C, respectively.
Temperature also seemed to affect PIPP. The duration of
PIPP estimated at 15}10 °C was 1 and 3 d longer than those
at 20}15 °C and 25}20 °C, respectively. However, the
duration of this phase at 25}20 °C was too variable among
the four separate experiments to confirm that the difference
among the three temperature treatments was significant. We
observed that plants grown at 15}10 °C required 1 to 3 more
days from the peduncle hook stage (USDA, ARS, System
Research Laboratory, 1992) to flower opening than those
grown at 25}20 °C. This indicates that the duration of PIPP
is not completely insensitive to temperature.
The results in opium poppy differed significantly from
those reported in rice, a short-day plant (Collinson et al.,
1992). In four rice cultivars tested in glasshouses, the cooler
temperature (28}20 °C) prolonged the durations of JP and
PIPP when compared to the warmer temperature regime
(32}26 °C), whereas the cooler temperature shortened the
duration of the photoperiod-sensitive inductive phase (equal
to the duration of PSP and PSPP in our study) in one
cultivar, but slightly prolonged this phase in another cultivar
(Collinson et al., 1992). Our results in opium poppy also
differed from those reported in soybean, another short-day
plant where the duration of JP was also temperature-
dependent (Jones and Laing, 1978 ; Hodges and French,
1985). It is not clear why the duration of JP in opium poppy
does not change with temperature compared with rice and
551
soybean. Unlike rice and soybean, opium poppy is a cool
rather than a warm season crop and may require very low
temperatures before differences are observed. Since our
lowest temperature treatment (15}10 °C) did prolong the
duration of PSPP and delay flowering time when compared
with the higher temperatures (20}15 and 25}20 °C), the
15}10 °C treatment should have been sufficiently low to
demonstrate a temperature effect on JP.
To maintain the same daily temperature for all transfers
within a temperature treatment it was necessary to maintain
some fixed thermoperiod for the two (9 and 16 h) photo-
periods. Such an asynchrony between photoperiod and
temperature has been reported to influence floral initiation
in some cultivars of sorghum, a short-day plant (Morgan,
Guy and Pao, 1987). Asynchrony of thermoperiods with
photoperiods promoted floral initiation compared with
controls with synchronous thermoperiods and photo-
periods. It is important to know from our experiment
whether the timing of the thermoperiod also influenced
floral initiation in opium poppy, a long-day plant. Such
information is important for the development of a model to
estimate poppy growth and floral development, and deserves
study in order to clarify the effects of temperature on
developmental phases.
In summary, the average number of days to flower by
plants grown continuously in a 16 h photoperiod was 32 d
at 25}20 °C. Flowering was delayed by 5 d at 20}15 °C and
by 14 d at 15}10 °C. However, the durations of the four
phases were not equally affected by temperature. The first
two phases, JP and PSP, were not shown to be temperature-
dependent. The third phase, PSPP, was the most sensitive to
temperature, but the temperature effect on this phase was
non-linear. The maximum difference in the duration of
PIPP was 3 d for the three temperature treatments and the
data too variable to indicate a significant trend. Our results
indicate that low temperatures delayed flowering mainly
because they prolonged the duration of PSPP.
A C K N O W L E D G E M E N TS
We thank Mr Robert Jones for his excellent technical
assistance.
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