- Email: [email protected]
Effect of photoperiod on flower stalk elongation in celeriac (Apium graveolens L. var. rapaceum (Mill.) DC.)
SCIENTIA HORllClnTuM Scientia Horticulturae63 (1995) 143-154
Effect of photoperiod on flower stalk elongation in celeriac ( Apium graveolens L. var. rapaceum ( Mill.) DC.) R. Booij *, E.J.J. Mews DLOResearch Institute for Agrobiology and Soil Fertility CAB-DLO),P.O. Box 14, 6700 AA Wageningen,Netherlands
Accepted3 April 1995
Abstract
The effect of photoperiod on elongation of the flower stalk in celeriac (Apium graveolens L. var rapaceum (Mill.) DC.) was studied by subjecting plants, after initiation of the primary umbel on the apex, to photoperiods between 8 and 24 h at a temperature of 16°C. The increase in length of the flower stalk with time could be described by a logistic curve. The final length of the stalk increased with increasing photoperiod, but did not increase further with photoperiods above 14 h. The stalk elongation rate increased with increasing photoperiod up to 18 h, whed a maximum elongation rate of 4.2 cm day - ’ was reached. Plants kept at a photoperiod of 8 or 10 h flowered normally, but without formation of the flower stalk, if the treatment started before initiation of the primary umbel on the apex but after thermoinduction for flowering was completed. Only additional low temperatures, before the start of the photoperiodic treatment, or a longer photoperiod resulted in elongation of the flower stalk. Time of flowering of the primary umbel was not affected by length of the photoperiod, only time of flowering of the secondary umbels was delayed in shorter photoperiods. When no stalk elongation was observed, the primary umbel developed directly from the bulb and no laterals developed. The results showed that the requirements for flowering and bolting were different in celeriac. For stalk elongation a longer period of low temperatures is required than for flowering. However, the low temperature needed for stalk elongation could be replaced by a long photoperiod. Keywords: Apium graveolens; Bolting; Celeriac; Celery; Daylength;
l
Corresponding
Flowering;
author.
0304-4238/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDI 0304-4238(95)00803-9
Photoperiod;
Stem elongation
144
R. Boo@ E.J.J. Meurs /Scientia Horticulturae 63 (1995) 143-154
1. Introduction
In commercial practice, celeriac (Apium gruveolens L. var rupaceum (Mill.) DC.) is grown for its stem tuber. Premature development of the flowering stalk (bolting) depresses yield and/ or quality. To avoid the risk of bolting it is necessary to analyse the effect of environmental factors on bolting. A number of developmental phases precede flowering, and the duration of each phase influences actual time of flowering (Bernier et al., 19811. Depending on the species, the following phases can be distinguished: juvenility, induction of flowering and development of the inflorescence. Environmental conditions mainly affect duration of the separate phases, and the effect depends on the sensitivity of the plant to such environmental factors. So, to analyse the effect of the environment on the time of flowering, one needs to analyse the relationship between environmental factors and length of each separate phase. Celeriac has a short juvenile phase (Booij and Meurs, 1993) and flowering is induced by low temperatures, with a small accelerating effect of longs day during induction (Booij and Meurs, 1994). Time of initiation of the main umbel on the apex depends on the final number of leaves, as determined during thermoinduction, and the leaf initiation rate (Booij and Meurs, 1993, 1994). The present paper focuses on the development of the inflorescence for in celeriac. The development of the flower stalk (bolting) is disastrous for yield, because assimilates will be directed towards the inflorescence and later to the seed. In most species that require low temperatures for flower induction, flowering and stalk elongation occur simultaneously, but in celeriac these two can be uncoupled by applying the appropriate photoperiod (Booij and Meurs, 1994). When plants are subjected to continuous long days after initiation of the primary umbel on the apex, the main flowering stalk elongates strongly. However, with a photoperiod of 10 h, no elongation of the main flowering stalk occurs and the main umbel develops directly from the bulb (Booij and Meurs, 1994). The uncoupling of flowering and bolting was discussed for other species by Vince-Prue (1985), and has since been attained by applying growth regulators. Hiller and Kelly (1979) showed that, in carrots, high temperatures after thermoinduction prevented flower stalk elongation without affecting flowering. This indicates that temperature requirements for flower induction differ from those for stalk elongation. In the present paper, the relationship between flower stalk elongation, flowering and photoperiod was further elaborated. The aim of the study was threefold. First, to establish the relationship between length of the photoperiod and stalk elongation rate, final stalk length and time of flowering, when applied after initiation of the primary umbel on the apex. Second, to test whether differences exist in low temperature requirement for umbel initiation on the one hand, and formation of the flower stalk on the other. Third, to examine the interaction between photoperiod and developmental stage of the inflorescence on flowering and bolting characteristics.
R. Booij, EJJ.
Meurs/Scientia
Horticulturae 63 (1995) 143-154
145
2. Materials and methods Two consecutive experiments of photoperiod was studied.
were carried out in 1991 and 1992, in which the effect
2.1. Pi-e-treatment Seeds of Apium graveolens L. var rapaceum (Mill.) DC. cultivar ‘Monarch’ (Hild, Marbach, G) were sown in cellular trays filled with potting compost and raised in a temperature-controlled greenhouse at a temperature of 20 + 1°C. Plants were transplanted in 5 1 pots filled with a sandy clay soil, when they had approximately four visible leaves. After transplanting, pots were transferred outside, but sheltered from rain, until the first frosts occurred. Watering and fertilisation were provided at adequate levels. To prevent frost injury, plants were transferred at the end of the season to a greenhouse, which was kept close to outside temperatures, but at a minimum of 0°C until the start of the treatment. 2.2. Treatment Photoperiodic treatments were given in a greenhouse controlled at a temperature of 16 f 1°C. The greenhouse was divided into compartments, which received natural light, supplemented with light from 400 W HP1 (Philips) lamps (photosynthetically active radiation (PAR) 180 pmol rnw2 s- ’ at plant level) and tungsten lamps (PAR 1.7 pmol m-2 s-1 > from 08:OO to 16:00 h. At 16:00 h the compartments were covered with black cloth, but for photoperiods longer than 8 h the tungsten lamps remained switched on until the required photoperiod was reached. At the start of treatment, six plants were randomly taken and dissected. The floral stage of the apex was scored according to the scale given by Booij et al. (1992). Twice a week, the length of the flower stalk of each plant (from top of the tuber to base of the terminal umbel) was measured and assessed for whether the primary umbel or a secondary umbel had reached anthesis. At the termination of the experiment, the numbers of leaves and bracts on the elongated stalk were counted. 2.3. Experiment 1 The experiment was carried out to determine the effect of a range of photoperiods after initiation of the primary umbel on time of flowering and on elongation characteristics of the flower stalk. Seeds were sown on 16 April 1991 and plants were placed outside on 27 May 1991. Plants were kept in the unheated greenhouse from 6 December 1991 until 15 January 1992, when the photoperiodic treatments started. Photoperiods of 8, 10, 12, 14, 16, 18, 20 and 24 h were applied and each treatment was applied to 12 plants. The experiment was terminated when all plants flowered on 15 April 1992.
146
R. Booij, E.JJ. Meurs/Scientia Horticulturae 63 (1995) 143-154
2.4. Experiment 2 The aim of the experiment was to examine the interaction between photoperiod and an additional low temperature treatment after completion of thermoinduction for flowering (Experiment 2(a)) and between photoperiod and the stage of development of the primary umbel at the start of the photoperiodic treatment on flowering and elongation of the main flower stalk (Experiment 2(b)). For both objects seeds were sown on 8 April 1992 and plants were placed outside on 27 May 1992. 2.4.1. Experiment 2(a) On 2 November 1992, 24 plants were transferred to the greenhouse (16°C) and were subjected to photoperiods of 8, 10, 12 or 16 h, while another 30 plants were transferred to a low temperature room at 6 f 1°C (PAR 80-100 pmol mm2 s-l for 8 h day-‘, supplied by Philips TL 55 lamps plus incandescent lamps). After 47 days, six of these plants were dissected and 24 were transferred to the greenhouse, where they were subjected to the photoperiodic treatments described above (six plants per treatment). 2.4.2. Experiment 2(b) The plants remained outside until they were transferred to the unheated greenhouse on 20 December 1992, to prevent frost injury. On 4 January 1993, photoperiodic treatments started on one-third of the plants. The remaining plants stayed in the greenhouse (16°C) at ambient photoperiod (under 9 h). After 14 days, a further group comprising one-third of the original number of plants, were subjected to the photoperiodic treatments, and after 28 days the remaining one-third were also subjected to treatment. Each photoperiod treatment was applied to six plants and photoperiods were the same as in Experiment 2(a). Both experiments were terminated when all plants flowered on 20 April 1993.
3. Results 3.1. Experiment 1 3.1.1. Stalk elongation At the start of the photoperiodic treatment, the mean floral stage of the apex was 1.8 f 1.2 (Table 1). Elongation of the flower stalk became visible, first at the longer photoperiods, from 20 days after the start of the treatment. The increase in mean length of the flower stalk could be accurately described (II2 2 0.99) by a logistic curve for all treatments (Fig. 1). The equation (Lane et al., 1987) for the fitted curve is Y= a + c-1 + e-b(t-m))-1
(1)
where Y is length, t is time, c is the final length, m is the time when the stalk reached half its final length, b is the relative increase in length and a is the lower asymptote (in our case 0).
R. Booij, E.J.J. Meurs/Scientia
Horticulturae 63 (1995) 143-154
Table 1 Mean (k SEM) floral stage a of the plant at the start of the photoperiodic
treatments
Experiment
Date
Floral stage
1 2(a) 2(a) 2(b) 2(b) 2(b)
15 January 1992 2 November 1992 4 January 1993 4 January 1993 18 January 1993 1 February 1993
1.8 f 1.2 0.2 f 0.5 3.3 f 1.4 3.3 + 0.8 3.7*0.5 6.0& 1.1
147
a 0, vegetative apex; 1, elongation of apical dome; 2, formation of secondary primordia; 3, formation of peduncles of the umbellets; 4, elongation peduncles and initiation of pedicels; 5, pedicel formation of the florets; 6, initiation of the tepals and stamen; 7, formation of ovary (Booij et al., 1992).
The elongation rate was highest when the flower stalk reached half of its final length. The relationships between photoperiod and some of the parameters of the logistic curve are given in Fig. 2. Final length of the flower stalk increased strongly with increasing photoperiod, up to a photoperiod of 14 h (Fig. 2(a)). A further increase in photoperiod did not result in longer stalks. The maximum rate of stalk elongation increased with increasing photoperiod up to 16 h. A further increase in photoperiod did not increase the rate any further (Fig. 2(b)). The time (days after start of the treatments) when half of the final length is reached depends on the time when elongation starts, the rate of elongation and the final length. The time when the flower stalk reached half of its final length advanced slowly with increasing photoperiod up to a photoperiod of 14 h, followed by a relatively strong advance between 14 and 16 h and a slower advance again for photoperiods longer than 16 h (Fig. 2(c)>. The advance in the time when stalk elongation was halfway, which occurred between 14 and 16 h (Fig. 2(c)) is due to the effect of photoperiod on the start of elongation (Fig. 1). 3.1.2. Flowering Time of flowering of the primary umbel could not be established in all plants, because, especially at the longer photoperiods, the florets in the primary umbel turned brown before reaching anthesis. Therefore, in this experiment, time of flowering was based on time of flowering of the first secondary umbel. Time of flowering advanced linearly with increasing photoperiod, up to a -photoperiod of 20 h, a still longer
20
40
60
a0
Time (days after start of the treatment)
Fig. 1. Experiment 1. Relationship between time (days after start of the treatment) and length (cm) of the flower stalk at photoperiods of 8 Cm), 10 CO), 12 (+), 14 CO), 16 (~1, 18 (A), 20 (0) and 24 (0) h.
148
R. Booij, EJJ.
Meurs / Scientia Horticulturae 63 (1995) 143-I 54
~t/‘-‘~~’
0
12
16
Photoperiod
20
24
c
12
16
Photoperiod
20 (h)
12
16
20
Photoperiod
50
6
6
(h)
24
100
50-0 8
24
(h)
-IO
12
16
20
d
24
Photoperiod
Fig. 2. Experiment 1. Relationship between length of the photoperiod (h) and (a) final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day- ’ 1, (c) time when half the final length of the flower stalk was reached (days after start of the treatment) and (d) time when the first secondary umbel flowered (days after start of the treatment) ( 0 1 and the total number of leaves plus bracts on the main flower stalk (A ). In (a)-(c), estimates of the parameters of the logistic curves are presented, which were fitted through the data of Fig. 1. Standard errors of the estimates were smaller than the size of the symbol.
photoperiod did not accelerate time of flowering further (Fig. 2(d)). The number of leaves and bracts on the main stalk was about 9 and was not affected by photoperiod (Fig. 2(d)). So, the effect of photoperiod on stalk elongation was solely due to an effect on length of internodes. 3.2. Experiment 2 Also in this experiment, the relationship between time and mean length of the flowering stalk was described by logistic curves (R* > 0.98). Only the effects of treatments on the parameters of the equation are given here (Eq. (1)). 3.2.1. Experiment 2(a) At the start of the experiment, the floral stage of the apex was little advanced (Table l), because most of the plants still had a vegetative apex (floral stage 0). After the additional low temperature treatment, the floral stage of the apex increased significantly (Table 1). In the case of plants subjected to the photoperiodic treatments without the additional low temperature treatment, the primary umbel developed directly from the bulb at photoperiods of 8 and 10 h (Fig. 3(a)). At a photoperiod of 12 h, about half of the plants developed a short flower stalk, while in the other half, the primary umbel developed directly from the bulb. All plants subjected to a 16 h photoperiod showed an elongated flower stalk, irrespective of the additional low temperature treatment. All plants that received an additional low temperature treatment before being transferred to the photoperiodic treatments formed an elongated flower stalk. In plants
R. Booij, E.J.J. Meurs/Scientia
100
a
I
016
10 12 14 16
Photoperiod
Horticulturae
b
54 I
i,6
10 12 14 16
Photoperiod(h)
63 (1995) 143-154
120
I
95/ 6
149
c
10 12 14 16
Photoperiod (h)
Fig. 3. Experiment 2(a). Relationships between length of the photoperiod (h) with (0) or without (m) an additional low temperature treatment, and (a) the final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day-‘) and (c) time when half the final length of the flower stalk was reached (days from 2 November 1992). The estimated parameters of the logistic curves are presented, which were obtained by curve fitting through the data of the weekly stalk length measurements. Standard errors of the estimates were smaller than the size of the symbol.
without an additional low temperature treatment, a photoperiod up to 12 h did not affect the final length of the flower stalk and only at 16 h a strong elongation was obvious (Fig. 3(a)). If plants had received an additional low temperature treatment, final length of the flower stalk increased continuously with increasing photoperiod and at 16 h the final length was close to the final length of plants which did not receive the additional low temperature (Fig. 3 (a)). So, the additional low temperature stimulated final length of the flower stalk most pronounced at the shorter photoperiods. The same pattern was observed for the effect on maximum elongation rate (reached when the stalk attained half its final length) (Fig. 3(b)). The final length and the maximum elongation rate of cold-treated plants were similar to the values found in Experiment 1 (Figs. 2 and 3). On plants which received the additional low temperature treatment, photoperiod advanced slightly the time at which the stalk reached half its final length, but in plants which did not receive this treatment, increasing photoperiod caused a marked reduction in this parameter (Fig. 3(c)). Time of flowering of the primary umbel was hardly affected by photoperiod, with or without the additional low temperature treatment (Fig. 4(a)). The additional low temperature treatment caused the time of flowering to be only slightly later than in plants which did not receive the treatment, although the former plants had grown for 2 months at 6°C instead of 16°C (Fig. 4(a)). The time of flowering of the secondary umbel was also not affected by photoperiod after the additional low temperature treatment (Fig. 4(b)). Without this treatment, time of flowering of secondary umbels was advanced when the photoperiod was increased from 12 to 16 h (Fig. 4(b)). At 8 and 10 h no laterals were formed, because the flower stalk did not elongate. 3.2.2. Experiment 2(b) Natural photoperiod increased during January from 8 to 9 h only. Postponement of the photoperiodic treatment, therefore, corresponds with a delay in subjecting plants to longer photoperiods. This delay resulted in a further developed inflorescence at the time of transfer to longer photoperiods (Table 1). In the case of plants subjected directly to longer photoperiods, final length of the flower stalk (Fig. 5(a)) and maximum elongation
1.50
R. Boo& E3.J. Meurs/Scientia Horticulturae 63 (1995) 143-154 wilhwt
3160 Fz 0140 E 120 F 100
a
wHh
A7-lf-a 6
10
12
16
6
10
12
16
Photoperiod with
without =160 ,% 0140
b
-
f 120 F 100 6
10
12
16
6
10
12
16
Photoperiod(h) 3
n
160 m" 9 140 g 120
T2
6
10
12
e
m-m nnnn
fin
i= ioo-
T3
16
6
10
12
16
6
10
12
16
Photoperiod(h) 12
Tl
= 160 cc 0140
l3
d
if 120 i= Inn ,“_
6
10
12
16
6
10
12
16
6
10
12
16
Photoperiod
Fig, 4. The effect of photoperiod c) and the secondary umbel (b, (Experiment 2(a)) and varying photoperiodic treatment started (n = 6).
on time (days from 2 November 1992) of flowering of the primary umbel (a, d) for plants with or without an additional low temperature treatment (a, b) times (4 January 1993 (Tl), 14 (T2) or 28 (T3) days later) when the (c, d) (Experiment 2(b)). Vertical bars indicate standard error of the mean
rate (Fig. 5(b)) increased with increasing photoperiod, which was most evident when the photoperiod was increased from 12 to 16 h. The time at which the flower stalk reached half its final length was only markedly advanced when the photoperiod was increased from 12 to 16 h (Fig. 5(c)). When the start of the treatment was delayed by 2 or 4
95 -6
10121416
Photoperiod(h)
-6
10 12 14 16 Photoperiod
(
6
10 12 14 16
Photoperiod(h)
Fig. 5. Experiment 2(b). Relationships between length of the photoperiod (h) and (a) final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day-‘) and (c) time (days from 2 November 1992) when half of the final length was reached. Photoperiodic treatments were started on 4 January 1993 ( W), 14 ( 0 ) or 28 ( +) days later. The estimated parameters of the logistic curves are presented, which were obtained by curve fitting through the data of the weekly stalk length measurements. Standard errors of the estimates were smaller than the size of the symbol.
R. Boo& E.J.J. Meurs/Scientia Horticulturae 63 (1995) 143-154
1.51
weeks, photoperiods had a similar effect on final length (Fig. 5(a)) and maximum elongation rate (Fig. 5(b)). However, the overall mean was lower after the last transfer date (Figs. 5(a) and (b)). When the transfer to longer photoperiods was delayed, the effect of photoperiod on the time at which the flower stalk reached half its final length was less (Fig. 5(c)). This was most pronounced at 16 h (Fig. 5(c)). No effect of photoperiod on this parameter was observed after the last transfer (Fig. 5(c)). At the time of the last transfer, the flower stalk was l-2 cm, indicating that elongation had already started. This indicates that the effect of photoperiod on the time at which the flower stalk reached half its final length, in earlier transfers was due to elongation starting earlier at 16 h than at shorter photoperiods (Fig. 5(c)). This is in agreement with the results of Experiment 1, which showed that increasing the photoperiod from 14 to 16 h had a pronounced effect on time at which the flower stalk reached half its final length (Fig. 2(c)). There was no significant effect of photoperiod on time of flowering of the primary umbel (Fig. 4(c)). Also, flowering of the first secondary umbel was hardly delayed when the start of the photoperiodic treatment was postponed. Only at a photoperiod of 16 h was flowering of the first secondary umbel significantly earlier than at shorter photoperiods (P < 0.05; Fig. 4(d)).
4. Discussion The reduction in final stalk length at shorter photoperiods after a low temperature treatment was described for a number of species, such as Alopecurus prufensis (Heide, 1986), cabbage (Heide, 19701, celery (Pressman and Negbi, 19801, Chinese cabbage (Suge and Takahashi, 1982; Elers and Wiebe, 1984), leek (Dragland, 19721, Pea pratensis (Heide et al., 1987) and red beet (Heide, 1973). When photoperiod varies directly after a low temperature treatment (thermoinduction), it can interfere with thermoinduction, e.g. by affecting the stability of the induction (Vince Prue, 1975). The effect of photoperiod on stalk elongation per se is shown only when applied after initiation of the inflorescence. In the experiments of Heide (1986) and Heide et al. (1987), photoperiodic treatments were certainly started after initiation of the inflorescence and show, therefore, a direct effect of photoperiod on elongation of the flowerstalk. The effect of photoperiod on stalk elongation rate has rarely been studied. As far as stalk elongation rate is concerned, celeriac can, therefore, be regarded as a quantitative long-day plant with a critical photoperiod of 16 h (Roberts and Summerfield, 1987). Hanisova and Krekule (1975) found just the opposite, namely that stalk elongation was retarded by long days. The results of the present study and those of an earlier paper (Booij and Meurs, 1994) show clearly that long days promote stalk elongation in celeriac. These results are also in agreement with results found by Pressman and Negbi (1980) and Roelofse et al. (1989) in celery, where short days after thermoinduction reduced stalk elongation. It is therefore most likely that the results of Hanisova and Krekule (1975) were not due to the photoperiodic treatment, but to the accompanying higher temperature during their continuous long day treatment.
152
R. Booij, EJJ. Meurs/Scientia
Horticulturae 63 (1995) 143-154
The small effect of an additional low temperature on time of anthesis (Fig. 4(a)) may be due to the relationship between temperature during thermoinduction and the final number of leaves (Booij and Meurs, 1993). Assuming that thermoinduction for flowering was completed before the plants were transferred inside, the final number of leaves was determined at that time (Booij and Meurs, 1993). As leaf initiation rate is weakly affected by temperature (Booij and Meurs, 19931, initiation of the final leaf, followed by initiation of the primary umbel, may have taken place at almost the same time, namely towards the end of the additional low temperature treatment, so that the inflorescence developed mainly at the same temperature. The requirements for flowering seem to be different from the requirements for stalk elongation, as only the main flower stalk developed in shorter photoperiods, when the plants had received additional low temperatures. Also in carrots the low temperature requirement for stalk elongation was greater than for flowering (Hiller and Kelly, 1979). When carrots were subjected to high temperatures after a low temperature treatment, the length of the flowering stalk was severely reduced and at the highest temperature the main umbel developed directly from the root, but flowering was not affected. These results are in agreement with those we obtained with celeriac, although, as shown here the low temperature needed for stalk elongation could be replaced by a long photoperiod (Fig. 3(a)). Hiller et al. (1979) showed that the reduction in stalk elongation in carrot could be overcome by applying gibberellic acid (GA,) as reported by Hanisova and Krekule (1975) for celeriac. The present results showed that the failure in stalk elongation due to insufficient exposure to low temperatures, could also be counteracted by long days. The long days might give rise to gibberellin synthesis (Vince Prue, 1985). The involvement of gibberellins is also suggested by the appearance of browning of the primary umbel in Experiment 1, which was only obvious at the longer photoperiods (data not shown). This phenomenon resembles ‘tipbum’, and is due to calcium deficiency. Pressman et al. (1993) found a relationship between vemalisation, photoperiod, gibberellin synthesis and tipbum in Chinese cabbage. Tipburn became most obvious in vemalised plants, which were subjected to a long photoperiod after vemalisation. Vince Prue (1985) discussed the differences between requirements for flower initiation and stalk elongation as two different processes, but the author only mentioned flowering with stalk elongation and stalk elongation without flowering. Results obtained by Hanisova and Krekule (19751, Hiller and Kelly (1979), and those obtained here, show that the opposite situation, flowering without stalk elongation, also exists. The present results complicate prediction of bolting in the field. Low temperatures accelerate flower induction (Booij and Meurs, 19931, but a longer period of low temperatures is required for elongation of the flower stalk than for flower induction. However, as shown here, long days can replace the additional low temperature requirement. In natural conditions, after early sowing, low temperature induces flowering and whether elongation of the flower stalk occurs, depends on timing. If induction is completed in long days (June), elongation of the flowering stalk will follow rapidly. Because temperatures generally increase with time from June, a situation can develop in which flower induction is completed, but the low temperature requirement for flower stalk elongation is not met. Because photoperiod shortens from July, the lack of low temperatures needed for stem elongation can not be compensated for by photoperiod.
R. Booij, E.J.J. Meurs/Scientia
Horticulturae
63 (1995) 143-154
153
The combination of shorter days and higher temperatures will prevent bolting and enhance the proportion of plants in which the primary umbel develops directly from the bulb. Zwart-Roodzant (1990) showed that within a crop, plants with elongated flower stalks are first to become obvious and later in the season plants without elongation of the flowering stalk. In practice, only elongated flower stalks are a problem, because only then is yield and quality reduced.
Acknowledgements We thank Dr. A. J. Haverkort for his comments on the manuscript.
References Bemier, G., Kinet, J.M. and Sachs, R.M., 1981. The Physiology of Flowering, Vol. I. The Initiation of Flowers. CRC Press, Boca Raton, FL, 568 pp. Booij, R. and Meurs, E.J.J., 1993. Flower induction and initiation in celeriac (Apium graveolens L. var. rapaceum (Mill.) DC): effects of temperature and plant age, Sci. Hortic., 55: 227-238. Booij, R. and Meurs, E.J.J., 1994. Flowering in celeriac (Apium graveolens 1. var rapaceum (Mill.) DC.): effects of photoperiod. Sci. Hortic., 58: 271-284. Booij, R., Meurs, E.J.J., Thiel, F. and Boekestein, A., 1992. Cryo-scanning electron microscopy of the apex of celeriac (Apium graveolens L. var. rapaceum (Mill.) DC) during initiation of the inflorescence. Sci. Hortic., 51: 309-320. Dragland, S., 1972. Effects of temperature and day-length on growth, bulb formation and bolting in leeks (Allium porrum L.). Meld. Norg. Landbrukshogsk., 51(46): 1-14. Elers, B. and Wiebe, H.J., 1984. Flower formation of Chinese cabbage. I. Response to vernalization and photoperiods. Sci. Ho&., 22: 219-131. Hanisova, A. and Krekule, J., 1975. Treatments to shorten the development period of celery (Apium graveolens L.). J. Hortic. Sci., 50: 97-104. Heide, O.M., 1970. Seed-stalk formation and flowering in cabbage. I. Day-length, temperature and time relationships. Meld. Norg. Landbrukshogsk., 49(27): 1-21. Heide, O.M., 1973. Environmental control of bolting and flowering in red garden beets. Meld. Norg. Landbrukshogsk., 52 (15): 1-15. Heide, O.M., 1986. Primary and secondary induction requirements for flowering in Alopecwus pratensis. Physiol. Plant., 66: 251-256. Heide, O.M., Bush,’ M.G. and Evans, L.T., 1987. Inhibitory and promotive effects of gibberellic acid on floral initiation and development in Poa pratensis and Bromus inermis. Physiol. Plant., 69: 342-350. Hiller, L.K. and Kelly, W.C., 1979. The effect of post-vernalization temperature on seedstalk elongation and flowering in carrots. J. Am. Sot. Hortic. Sci., 104: 253-257. Hiller, L.K., Kelly, WC. and Powell, L.E., 1979. Temperature interactions with growth regulators and endogenous gibberellin-like activity during seedstalk elongation. Plant Physiol., 63: 1055-1061. Lane, P., Galwey, N. and Alvey, N., 1987. GENSTAT5. An Introduction. Oxford University Press, Oxford, 163 pp. Pressman, E. and Negbi, M., 1980. The effect of day length on the response of celery to vernalization. J. Exp. Bot., 31: 1291-1296. Pressman, E., Shaked, R. and Aracan, L., 1993. The effect of flower-inducing factors on leaf tipbum formation in Chinese cabbage. J. Plant Physiol., 141: 210-214. Roberts, E.H. and Summerfield, R.J., 1987. Measurement and prediction of flowering in annual crops. In: J.G. Atherton (Editor), Manipulation of Flowering. Butterworths, London, pp. 17-50.
154
R. Booij, EJJ. Meurs/Scientia Horticulturae 63 (1995) 143-1.54
Roelofse, E.W., Hand, D.W. and Hall, R.L., 1989. The effect of daylength on the development of glasshouse celery. J. Hortic. Sci., 64: 283-292. Suge, H. and Takahashi, H., 1982. The role of gibberellins in the stem elongation and flowering of Chinese cabbage, Brassica campestris var. pekinensis in their relation to vernalization and photoperiod. Rep. Inst. Agric. Res. Tohoku Univ., 33: 15-34. Vince-Pure, D., 1975. Photoperiodism in Plants. McGraw-Hill, London, 444 pp. Vince-Prue, D., 1985. Photoperiod and hormones. In: R.P. Pharis and D.M. Reid (Editors), Hormonal Regulation of Development, III. Role of Environmental Factors. Springer, Berlin, pp. 308-364. Zwart-Roodzant, M.H., 1990. Bolting in celeriac. Verslag proefstation voor de akkerbouw en de groenteteelt in de vollegrond no. 12, PAGV, Lelystad, 47 pp. (In Dutch.)
Effect of photoperiod on flower stalk elongation in celeriac ( Apium graveolens L. var. rapaceum ( Mill.) DC.) R. Booij *, E.J.J. Mews DLOResearch Institute for Agrobiology and Soil Fertility CAB-DLO),P.O. Box 14, 6700 AA Wageningen,Netherlands
Accepted3 April 1995
Abstract
The effect of photoperiod on elongation of the flower stalk in celeriac (Apium graveolens L. var rapaceum (Mill.) DC.) was studied by subjecting plants, after initiation of the primary umbel on the apex, to photoperiods between 8 and 24 h at a temperature of 16°C. The increase in length of the flower stalk with time could be described by a logistic curve. The final length of the stalk increased with increasing photoperiod, but did not increase further with photoperiods above 14 h. The stalk elongation rate increased with increasing photoperiod up to 18 h, whed a maximum elongation rate of 4.2 cm day - ’ was reached. Plants kept at a photoperiod of 8 or 10 h flowered normally, but without formation of the flower stalk, if the treatment started before initiation of the primary umbel on the apex but after thermoinduction for flowering was completed. Only additional low temperatures, before the start of the photoperiodic treatment, or a longer photoperiod resulted in elongation of the flower stalk. Time of flowering of the primary umbel was not affected by length of the photoperiod, only time of flowering of the secondary umbels was delayed in shorter photoperiods. When no stalk elongation was observed, the primary umbel developed directly from the bulb and no laterals developed. The results showed that the requirements for flowering and bolting were different in celeriac. For stalk elongation a longer period of low temperatures is required than for flowering. However, the low temperature needed for stalk elongation could be replaced by a long photoperiod. Keywords: Apium graveolens; Bolting; Celeriac; Celery; Daylength;
l
Corresponding
Flowering;
author.
0304-4238/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDI 0304-4238(95)00803-9
Photoperiod;
Stem elongation
144
R. Boo@ E.J.J. Meurs /Scientia Horticulturae 63 (1995) 143-154
1. Introduction
In commercial practice, celeriac (Apium gruveolens L. var rupaceum (Mill.) DC.) is grown for its stem tuber. Premature development of the flowering stalk (bolting) depresses yield and/ or quality. To avoid the risk of bolting it is necessary to analyse the effect of environmental factors on bolting. A number of developmental phases precede flowering, and the duration of each phase influences actual time of flowering (Bernier et al., 19811. Depending on the species, the following phases can be distinguished: juvenility, induction of flowering and development of the inflorescence. Environmental conditions mainly affect duration of the separate phases, and the effect depends on the sensitivity of the plant to such environmental factors. So, to analyse the effect of the environment on the time of flowering, one needs to analyse the relationship between environmental factors and length of each separate phase. Celeriac has a short juvenile phase (Booij and Meurs, 1993) and flowering is induced by low temperatures, with a small accelerating effect of longs day during induction (Booij and Meurs, 1994). Time of initiation of the main umbel on the apex depends on the final number of leaves, as determined during thermoinduction, and the leaf initiation rate (Booij and Meurs, 1993, 1994). The present paper focuses on the development of the inflorescence for in celeriac. The development of the flower stalk (bolting) is disastrous for yield, because assimilates will be directed towards the inflorescence and later to the seed. In most species that require low temperatures for flower induction, flowering and stalk elongation occur simultaneously, but in celeriac these two can be uncoupled by applying the appropriate photoperiod (Booij and Meurs, 1994). When plants are subjected to continuous long days after initiation of the primary umbel on the apex, the main flowering stalk elongates strongly. However, with a photoperiod of 10 h, no elongation of the main flowering stalk occurs and the main umbel develops directly from the bulb (Booij and Meurs, 1994). The uncoupling of flowering and bolting was discussed for other species by Vince-Prue (1985), and has since been attained by applying growth regulators. Hiller and Kelly (1979) showed that, in carrots, high temperatures after thermoinduction prevented flower stalk elongation without affecting flowering. This indicates that temperature requirements for flower induction differ from those for stalk elongation. In the present paper, the relationship between flower stalk elongation, flowering and photoperiod was further elaborated. The aim of the study was threefold. First, to establish the relationship between length of the photoperiod and stalk elongation rate, final stalk length and time of flowering, when applied after initiation of the primary umbel on the apex. Second, to test whether differences exist in low temperature requirement for umbel initiation on the one hand, and formation of the flower stalk on the other. Third, to examine the interaction between photoperiod and developmental stage of the inflorescence on flowering and bolting characteristics.
R. Booij, EJJ.
Meurs/Scientia
Horticulturae 63 (1995) 143-154
145
2. Materials and methods Two consecutive experiments of photoperiod was studied.
were carried out in 1991 and 1992, in which the effect
2.1. Pi-e-treatment Seeds of Apium graveolens L. var rapaceum (Mill.) DC. cultivar ‘Monarch’ (Hild, Marbach, G) were sown in cellular trays filled with potting compost and raised in a temperature-controlled greenhouse at a temperature of 20 + 1°C. Plants were transplanted in 5 1 pots filled with a sandy clay soil, when they had approximately four visible leaves. After transplanting, pots were transferred outside, but sheltered from rain, until the first frosts occurred. Watering and fertilisation were provided at adequate levels. To prevent frost injury, plants were transferred at the end of the season to a greenhouse, which was kept close to outside temperatures, but at a minimum of 0°C until the start of the treatment. 2.2. Treatment Photoperiodic treatments were given in a greenhouse controlled at a temperature of 16 f 1°C. The greenhouse was divided into compartments, which received natural light, supplemented with light from 400 W HP1 (Philips) lamps (photosynthetically active radiation (PAR) 180 pmol rnw2 s- ’ at plant level) and tungsten lamps (PAR 1.7 pmol m-2 s-1 > from 08:OO to 16:00 h. At 16:00 h the compartments were covered with black cloth, but for photoperiods longer than 8 h the tungsten lamps remained switched on until the required photoperiod was reached. At the start of treatment, six plants were randomly taken and dissected. The floral stage of the apex was scored according to the scale given by Booij et al. (1992). Twice a week, the length of the flower stalk of each plant (from top of the tuber to base of the terminal umbel) was measured and assessed for whether the primary umbel or a secondary umbel had reached anthesis. At the termination of the experiment, the numbers of leaves and bracts on the elongated stalk were counted. 2.3. Experiment 1 The experiment was carried out to determine the effect of a range of photoperiods after initiation of the primary umbel on time of flowering and on elongation characteristics of the flower stalk. Seeds were sown on 16 April 1991 and plants were placed outside on 27 May 1991. Plants were kept in the unheated greenhouse from 6 December 1991 until 15 January 1992, when the photoperiodic treatments started. Photoperiods of 8, 10, 12, 14, 16, 18, 20 and 24 h were applied and each treatment was applied to 12 plants. The experiment was terminated when all plants flowered on 15 April 1992.
146
R. Booij, E.JJ. Meurs/Scientia Horticulturae 63 (1995) 143-154
2.4. Experiment 2 The aim of the experiment was to examine the interaction between photoperiod and an additional low temperature treatment after completion of thermoinduction for flowering (Experiment 2(a)) and between photoperiod and the stage of development of the primary umbel at the start of the photoperiodic treatment on flowering and elongation of the main flower stalk (Experiment 2(b)). For both objects seeds were sown on 8 April 1992 and plants were placed outside on 27 May 1992. 2.4.1. Experiment 2(a) On 2 November 1992, 24 plants were transferred to the greenhouse (16°C) and were subjected to photoperiods of 8, 10, 12 or 16 h, while another 30 plants were transferred to a low temperature room at 6 f 1°C (PAR 80-100 pmol mm2 s-l for 8 h day-‘, supplied by Philips TL 55 lamps plus incandescent lamps). After 47 days, six of these plants were dissected and 24 were transferred to the greenhouse, where they were subjected to the photoperiodic treatments described above (six plants per treatment). 2.4.2. Experiment 2(b) The plants remained outside until they were transferred to the unheated greenhouse on 20 December 1992, to prevent frost injury. On 4 January 1993, photoperiodic treatments started on one-third of the plants. The remaining plants stayed in the greenhouse (16°C) at ambient photoperiod (under 9 h). After 14 days, a further group comprising one-third of the original number of plants, were subjected to the photoperiodic treatments, and after 28 days the remaining one-third were also subjected to treatment. Each photoperiod treatment was applied to six plants and photoperiods were the same as in Experiment 2(a). Both experiments were terminated when all plants flowered on 20 April 1993.
3. Results 3.1. Experiment 1 3.1.1. Stalk elongation At the start of the photoperiodic treatment, the mean floral stage of the apex was 1.8 f 1.2 (Table 1). Elongation of the flower stalk became visible, first at the longer photoperiods, from 20 days after the start of the treatment. The increase in mean length of the flower stalk could be accurately described (II2 2 0.99) by a logistic curve for all treatments (Fig. 1). The equation (Lane et al., 1987) for the fitted curve is Y= a + c-1 + e-b(t-m))-1
(1)
where Y is length, t is time, c is the final length, m is the time when the stalk reached half its final length, b is the relative increase in length and a is the lower asymptote (in our case 0).
R. Booij, E.J.J. Meurs/Scientia
Horticulturae 63 (1995) 143-154
Table 1 Mean (k SEM) floral stage a of the plant at the start of the photoperiodic
treatments
Experiment
Date
Floral stage
1 2(a) 2(a) 2(b) 2(b) 2(b)
15 January 1992 2 November 1992 4 January 1993 4 January 1993 18 January 1993 1 February 1993
1.8 f 1.2 0.2 f 0.5 3.3 f 1.4 3.3 + 0.8 3.7*0.5 6.0& 1.1
147
a 0, vegetative apex; 1, elongation of apical dome; 2, formation of secondary primordia; 3, formation of peduncles of the umbellets; 4, elongation peduncles and initiation of pedicels; 5, pedicel formation of the florets; 6, initiation of the tepals and stamen; 7, formation of ovary (Booij et al., 1992).
The elongation rate was highest when the flower stalk reached half of its final length. The relationships between photoperiod and some of the parameters of the logistic curve are given in Fig. 2. Final length of the flower stalk increased strongly with increasing photoperiod, up to a photoperiod of 14 h (Fig. 2(a)). A further increase in photoperiod did not result in longer stalks. The maximum rate of stalk elongation increased with increasing photoperiod up to 16 h. A further increase in photoperiod did not increase the rate any further (Fig. 2(b)). The time (days after start of the treatments) when half of the final length is reached depends on the time when elongation starts, the rate of elongation and the final length. The time when the flower stalk reached half of its final length advanced slowly with increasing photoperiod up to a photoperiod of 14 h, followed by a relatively strong advance between 14 and 16 h and a slower advance again for photoperiods longer than 16 h (Fig. 2(c)>. The advance in the time when stalk elongation was halfway, which occurred between 14 and 16 h (Fig. 2(c)) is due to the effect of photoperiod on the start of elongation (Fig. 1). 3.1.2. Flowering Time of flowering of the primary umbel could not be established in all plants, because, especially at the longer photoperiods, the florets in the primary umbel turned brown before reaching anthesis. Therefore, in this experiment, time of flowering was based on time of flowering of the first secondary umbel. Time of flowering advanced linearly with increasing photoperiod, up to a -photoperiod of 20 h, a still longer
20
40
60
a0
Time (days after start of the treatment)
Fig. 1. Experiment 1. Relationship between time (days after start of the treatment) and length (cm) of the flower stalk at photoperiods of 8 Cm), 10 CO), 12 (+), 14 CO), 16 (~1, 18 (A), 20 (0) and 24 (0) h.
148
R. Booij, EJJ.
Meurs / Scientia Horticulturae 63 (1995) 143-I 54
~t/‘-‘~~’
0
12
16
Photoperiod
20
24
c
12
16
Photoperiod
20 (h)
12
16
20
Photoperiod
50
6
6
(h)
24
100
50-0 8
24
(h)
-IO
12
16
20
d
24
Photoperiod
Fig. 2. Experiment 1. Relationship between length of the photoperiod (h) and (a) final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day- ’ 1, (c) time when half the final length of the flower stalk was reached (days after start of the treatment) and (d) time when the first secondary umbel flowered (days after start of the treatment) ( 0 1 and the total number of leaves plus bracts on the main flower stalk (A ). In (a)-(c), estimates of the parameters of the logistic curves are presented, which were fitted through the data of Fig. 1. Standard errors of the estimates were smaller than the size of the symbol.
photoperiod did not accelerate time of flowering further (Fig. 2(d)). The number of leaves and bracts on the main stalk was about 9 and was not affected by photoperiod (Fig. 2(d)). So, the effect of photoperiod on stalk elongation was solely due to an effect on length of internodes. 3.2. Experiment 2 Also in this experiment, the relationship between time and mean length of the flowering stalk was described by logistic curves (R* > 0.98). Only the effects of treatments on the parameters of the equation are given here (Eq. (1)). 3.2.1. Experiment 2(a) At the start of the experiment, the floral stage of the apex was little advanced (Table l), because most of the plants still had a vegetative apex (floral stage 0). After the additional low temperature treatment, the floral stage of the apex increased significantly (Table 1). In the case of plants subjected to the photoperiodic treatments without the additional low temperature treatment, the primary umbel developed directly from the bulb at photoperiods of 8 and 10 h (Fig. 3(a)). At a photoperiod of 12 h, about half of the plants developed a short flower stalk, while in the other half, the primary umbel developed directly from the bulb. All plants subjected to a 16 h photoperiod showed an elongated flower stalk, irrespective of the additional low temperature treatment. All plants that received an additional low temperature treatment before being transferred to the photoperiodic treatments formed an elongated flower stalk. In plants
R. Booij, E.J.J. Meurs/Scientia
100
a
I
016
10 12 14 16
Photoperiod
Horticulturae
b
54 I
i,6
10 12 14 16
Photoperiod(h)
63 (1995) 143-154
120
I
95/ 6
149
c
10 12 14 16
Photoperiod (h)
Fig. 3. Experiment 2(a). Relationships between length of the photoperiod (h) with (0) or without (m) an additional low temperature treatment, and (a) the final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day-‘) and (c) time when half the final length of the flower stalk was reached (days from 2 November 1992). The estimated parameters of the logistic curves are presented, which were obtained by curve fitting through the data of the weekly stalk length measurements. Standard errors of the estimates were smaller than the size of the symbol.
without an additional low temperature treatment, a photoperiod up to 12 h did not affect the final length of the flower stalk and only at 16 h a strong elongation was obvious (Fig. 3(a)). If plants had received an additional low temperature treatment, final length of the flower stalk increased continuously with increasing photoperiod and at 16 h the final length was close to the final length of plants which did not receive the additional low temperature (Fig. 3 (a)). So, the additional low temperature stimulated final length of the flower stalk most pronounced at the shorter photoperiods. The same pattern was observed for the effect on maximum elongation rate (reached when the stalk attained half its final length) (Fig. 3(b)). The final length and the maximum elongation rate of cold-treated plants were similar to the values found in Experiment 1 (Figs. 2 and 3). On plants which received the additional low temperature treatment, photoperiod advanced slightly the time at which the stalk reached half its final length, but in plants which did not receive this treatment, increasing photoperiod caused a marked reduction in this parameter (Fig. 3(c)). Time of flowering of the primary umbel was hardly affected by photoperiod, with or without the additional low temperature treatment (Fig. 4(a)). The additional low temperature treatment caused the time of flowering to be only slightly later than in plants which did not receive the treatment, although the former plants had grown for 2 months at 6°C instead of 16°C (Fig. 4(a)). The time of flowering of the secondary umbel was also not affected by photoperiod after the additional low temperature treatment (Fig. 4(b)). Without this treatment, time of flowering of secondary umbels was advanced when the photoperiod was increased from 12 to 16 h (Fig. 4(b)). At 8 and 10 h no laterals were formed, because the flower stalk did not elongate. 3.2.2. Experiment 2(b) Natural photoperiod increased during January from 8 to 9 h only. Postponement of the photoperiodic treatment, therefore, corresponds with a delay in subjecting plants to longer photoperiods. This delay resulted in a further developed inflorescence at the time of transfer to longer photoperiods (Table 1). In the case of plants subjected directly to longer photoperiods, final length of the flower stalk (Fig. 5(a)) and maximum elongation
1.50
R. Boo& E3.J. Meurs/Scientia Horticulturae 63 (1995) 143-154 wilhwt
3160 Fz 0140 E 120 F 100
a
wHh
A7-lf-a 6
10
12
16
6
10
12
16
Photoperiod with
without =160 ,% 0140
b
-
f 120 F 100 6
10
12
16
6
10
12
16
Photoperiod(h) 3
n
160 m" 9 140 g 120
T2
6
10
12
e
m-m nnnn
fin
i= ioo-
T3
16
6
10
12
16
6
10
12
16
Photoperiod(h) 12
Tl
= 160 cc 0140
l3
d
if 120 i= Inn ,“_
6
10
12
16
6
10
12
16
6
10
12
16
Photoperiod
Fig, 4. The effect of photoperiod c) and the secondary umbel (b, (Experiment 2(a)) and varying photoperiodic treatment started (n = 6).
on time (days from 2 November 1992) of flowering of the primary umbel (a, d) for plants with or without an additional low temperature treatment (a, b) times (4 January 1993 (Tl), 14 (T2) or 28 (T3) days later) when the (c, d) (Experiment 2(b)). Vertical bars indicate standard error of the mean
rate (Fig. 5(b)) increased with increasing photoperiod, which was most evident when the photoperiod was increased from 12 to 16 h. The time at which the flower stalk reached half its final length was only markedly advanced when the photoperiod was increased from 12 to 16 h (Fig. 5(c)). When the start of the treatment was delayed by 2 or 4
95 -6
10121416
Photoperiod(h)
-6
10 12 14 16 Photoperiod
(
6
10 12 14 16
Photoperiod(h)
Fig. 5. Experiment 2(b). Relationships between length of the photoperiod (h) and (a) final length of the flower stalk, (b) maximum elongation rate of flower stalk (cm day-‘) and (c) time (days from 2 November 1992) when half of the final length was reached. Photoperiodic treatments were started on 4 January 1993 ( W), 14 ( 0 ) or 28 ( +) days later. The estimated parameters of the logistic curves are presented, which were obtained by curve fitting through the data of the weekly stalk length measurements. Standard errors of the estimates were smaller than the size of the symbol.
R. Boo& E.J.J. Meurs/Scientia Horticulturae 63 (1995) 143-154
1.51
weeks, photoperiods had a similar effect on final length (Fig. 5(a)) and maximum elongation rate (Fig. 5(b)). However, the overall mean was lower after the last transfer date (Figs. 5(a) and (b)). When the transfer to longer photoperiods was delayed, the effect of photoperiod on the time at which the flower stalk reached half its final length was less (Fig. 5(c)). This was most pronounced at 16 h (Fig. 5(c)). No effect of photoperiod on this parameter was observed after the last transfer (Fig. 5(c)). At the time of the last transfer, the flower stalk was l-2 cm, indicating that elongation had already started. This indicates that the effect of photoperiod on the time at which the flower stalk reached half its final length, in earlier transfers was due to elongation starting earlier at 16 h than at shorter photoperiods (Fig. 5(c)). This is in agreement with the results of Experiment 1, which showed that increasing the photoperiod from 14 to 16 h had a pronounced effect on time at which the flower stalk reached half its final length (Fig. 2(c)). There was no significant effect of photoperiod on time of flowering of the primary umbel (Fig. 4(c)). Also, flowering of the first secondary umbel was hardly delayed when the start of the photoperiodic treatment was postponed. Only at a photoperiod of 16 h was flowering of the first secondary umbel significantly earlier than at shorter photoperiods (P < 0.05; Fig. 4(d)).
4. Discussion The reduction in final stalk length at shorter photoperiods after a low temperature treatment was described for a number of species, such as Alopecurus prufensis (Heide, 1986), cabbage (Heide, 19701, celery (Pressman and Negbi, 19801, Chinese cabbage (Suge and Takahashi, 1982; Elers and Wiebe, 1984), leek (Dragland, 19721, Pea pratensis (Heide et al., 1987) and red beet (Heide, 1973). When photoperiod varies directly after a low temperature treatment (thermoinduction), it can interfere with thermoinduction, e.g. by affecting the stability of the induction (Vince Prue, 1975). The effect of photoperiod on stalk elongation per se is shown only when applied after initiation of the inflorescence. In the experiments of Heide (1986) and Heide et al. (1987), photoperiodic treatments were certainly started after initiation of the inflorescence and show, therefore, a direct effect of photoperiod on elongation of the flowerstalk. The effect of photoperiod on stalk elongation rate has rarely been studied. As far as stalk elongation rate is concerned, celeriac can, therefore, be regarded as a quantitative long-day plant with a critical photoperiod of 16 h (Roberts and Summerfield, 1987). Hanisova and Krekule (1975) found just the opposite, namely that stalk elongation was retarded by long days. The results of the present study and those of an earlier paper (Booij and Meurs, 1994) show clearly that long days promote stalk elongation in celeriac. These results are also in agreement with results found by Pressman and Negbi (1980) and Roelofse et al. (1989) in celery, where short days after thermoinduction reduced stalk elongation. It is therefore most likely that the results of Hanisova and Krekule (1975) were not due to the photoperiodic treatment, but to the accompanying higher temperature during their continuous long day treatment.
152
R. Booij, EJJ. Meurs/Scientia
Horticulturae 63 (1995) 143-154
The small effect of an additional low temperature on time of anthesis (Fig. 4(a)) may be due to the relationship between temperature during thermoinduction and the final number of leaves (Booij and Meurs, 1993). Assuming that thermoinduction for flowering was completed before the plants were transferred inside, the final number of leaves was determined at that time (Booij and Meurs, 1993). As leaf initiation rate is weakly affected by temperature (Booij and Meurs, 19931, initiation of the final leaf, followed by initiation of the primary umbel, may have taken place at almost the same time, namely towards the end of the additional low temperature treatment, so that the inflorescence developed mainly at the same temperature. The requirements for flowering seem to be different from the requirements for stalk elongation, as only the main flower stalk developed in shorter photoperiods, when the plants had received additional low temperatures. Also in carrots the low temperature requirement for stalk elongation was greater than for flowering (Hiller and Kelly, 1979). When carrots were subjected to high temperatures after a low temperature treatment, the length of the flowering stalk was severely reduced and at the highest temperature the main umbel developed directly from the root, but flowering was not affected. These results are in agreement with those we obtained with celeriac, although, as shown here the low temperature needed for stalk elongation could be replaced by a long photoperiod (Fig. 3(a)). Hiller et al. (1979) showed that the reduction in stalk elongation in carrot could be overcome by applying gibberellic acid (GA,) as reported by Hanisova and Krekule (1975) for celeriac. The present results showed that the failure in stalk elongation due to insufficient exposure to low temperatures, could also be counteracted by long days. The long days might give rise to gibberellin synthesis (Vince Prue, 1985). The involvement of gibberellins is also suggested by the appearance of browning of the primary umbel in Experiment 1, which was only obvious at the longer photoperiods (data not shown). This phenomenon resembles ‘tipbum’, and is due to calcium deficiency. Pressman et al. (1993) found a relationship between vemalisation, photoperiod, gibberellin synthesis and tipbum in Chinese cabbage. Tipburn became most obvious in vemalised plants, which were subjected to a long photoperiod after vemalisation. Vince Prue (1985) discussed the differences between requirements for flower initiation and stalk elongation as two different processes, but the author only mentioned flowering with stalk elongation and stalk elongation without flowering. Results obtained by Hanisova and Krekule (19751, Hiller and Kelly (1979), and those obtained here, show that the opposite situation, flowering without stalk elongation, also exists. The present results complicate prediction of bolting in the field. Low temperatures accelerate flower induction (Booij and Meurs, 19931, but a longer period of low temperatures is required for elongation of the flower stalk than for flower induction. However, as shown here, long days can replace the additional low temperature requirement. In natural conditions, after early sowing, low temperature induces flowering and whether elongation of the flower stalk occurs, depends on timing. If induction is completed in long days (June), elongation of the flowering stalk will follow rapidly. Because temperatures generally increase with time from June, a situation can develop in which flower induction is completed, but the low temperature requirement for flower stalk elongation is not met. Because photoperiod shortens from July, the lack of low temperatures needed for stem elongation can not be compensated for by photoperiod.
R. Booij, E.J.J. Meurs/Scientia
Horticulturae
63 (1995) 143-154
153
The combination of shorter days and higher temperatures will prevent bolting and enhance the proportion of plants in which the primary umbel develops directly from the bulb. Zwart-Roodzant (1990) showed that within a crop, plants with elongated flower stalks are first to become obvious and later in the season plants without elongation of the flowering stalk. In practice, only elongated flower stalks are a problem, because only then is yield and quality reduced.
Acknowledgements We thank Dr. A. J. Haverkort for his comments on the manuscript.
References Bemier, G., Kinet, J.M. and Sachs, R.M., 1981. The Physiology of Flowering, Vol. I. The Initiation of Flowers. CRC Press, Boca Raton, FL, 568 pp. Booij, R. and Meurs, E.J.J., 1993. Flower induction and initiation in celeriac (Apium graveolens L. var. rapaceum (Mill.) DC): effects of temperature and plant age, Sci. Hortic., 55: 227-238. Booij, R. and Meurs, E.J.J., 1994. Flowering in celeriac (Apium graveolens 1. var rapaceum (Mill.) DC.): effects of photoperiod. Sci. Hortic., 58: 271-284. Booij, R., Meurs, E.J.J., Thiel, F. and Boekestein, A., 1992. Cryo-scanning electron microscopy of the apex of celeriac (Apium graveolens L. var. rapaceum (Mill.) DC) during initiation of the inflorescence. Sci. Hortic., 51: 309-320. Dragland, S., 1972. Effects of temperature and day-length on growth, bulb formation and bolting in leeks (Allium porrum L.). Meld. Norg. Landbrukshogsk., 51(46): 1-14. Elers, B. and Wiebe, H.J., 1984. Flower formation of Chinese cabbage. I. Response to vernalization and photoperiods. Sci. Ho&., 22: 219-131. Hanisova, A. and Krekule, J., 1975. Treatments to shorten the development period of celery (Apium graveolens L.). J. Hortic. Sci., 50: 97-104. Heide, O.M., 1970. Seed-stalk formation and flowering in cabbage. I. Day-length, temperature and time relationships. Meld. Norg. Landbrukshogsk., 49(27): 1-21. Heide, O.M., 1973. Environmental control of bolting and flowering in red garden beets. Meld. Norg. Landbrukshogsk., 52 (15): 1-15. Heide, O.M., 1986. Primary and secondary induction requirements for flowering in Alopecwus pratensis. Physiol. Plant., 66: 251-256. Heide, O.M., Bush,’ M.G. and Evans, L.T., 1987. Inhibitory and promotive effects of gibberellic acid on floral initiation and development in Poa pratensis and Bromus inermis. Physiol. Plant., 69: 342-350. Hiller, L.K. and Kelly, W.C., 1979. The effect of post-vernalization temperature on seedstalk elongation and flowering in carrots. J. Am. Sot. Hortic. Sci., 104: 253-257. Hiller, L.K., Kelly, WC. and Powell, L.E., 1979. Temperature interactions with growth regulators and endogenous gibberellin-like activity during seedstalk elongation. Plant Physiol., 63: 1055-1061. Lane, P., Galwey, N. and Alvey, N., 1987. GENSTAT5. An Introduction. Oxford University Press, Oxford, 163 pp. Pressman, E. and Negbi, M., 1980. The effect of day length on the response of celery to vernalization. J. Exp. Bot., 31: 1291-1296. Pressman, E., Shaked, R. and Aracan, L., 1993. The effect of flower-inducing factors on leaf tipbum formation in Chinese cabbage. J. Plant Physiol., 141: 210-214. Roberts, E.H. and Summerfield, R.J., 1987. Measurement and prediction of flowering in annual crops. In: J.G. Atherton (Editor), Manipulation of Flowering. Butterworths, London, pp. 17-50.
154
R. Booij, EJJ. Meurs/Scientia Horticulturae 63 (1995) 143-1.54
Roelofse, E.W., Hand, D.W. and Hall, R.L., 1989. The effect of daylength on the development of glasshouse celery. J. Hortic. Sci., 64: 283-292. Suge, H. and Takahashi, H., 1982. The role of gibberellins in the stem elongation and flowering of Chinese cabbage, Brassica campestris var. pekinensis in their relation to vernalization and photoperiod. Rep. Inst. Agric. Res. Tohoku Univ., 33: 15-34. Vince-Pure, D., 1975. Photoperiodism in Plants. McGraw-Hill, London, 444 pp. Vince-Prue, D., 1985. Photoperiod and hormones. In: R.P. Pharis and D.M. Reid (Editors), Hormonal Regulation of Development, III. Role of Environmental Factors. Springer, Berlin, pp. 308-364. Zwart-Roodzant, M.H., 1990. Bolting in celeriac. Verslag proefstation voor de akkerbouw en de groenteteelt in de vollegrond no. 12, PAGV, Lelystad, 47 pp. (In Dutch.)