The Effects of Temperature, Photoperiod and Light Integral on the Time to Flowering of Pansy cv. Universal Violet (Viola wittrockiana Gams.
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1 Annals of Botany 80: , 1997 The Effects of Temperature, Photoperiod and Light Integral on the Time to Flowering of Pansy cv. Universal Violet (Viola wittrockiana Gams.) S. R. ADAMS, S. PEARSON and P. HADLEY The Department of Horticulture, School of Plant Sciences, The Uni ersity of Reading, Reading, RG6 6AS, UK Received: 11 October 1996 Accepted: 24 February 1997 The effects of temperature, photoperiod and light integral on the time to first flowering of pansy (Viola wittrockiana Gams) were investigated. Plants were grown at six temperatures (means between 14 8 and 26 1 C), combined with four photoperiods (8, 11, 14 and 17 h). The rate of progress to flowering increased linearly with temperature (up to an optimum of 21 7 C) and with increase in photoperiod (r 0 91, 19 d.f.), the latter indicating that pansies are quantitative long day plants (LDPs). In a second experiment, plants were sown on five dates between July and December 1992 and grown in glasshouse compartments under natural day lengths at six temperatures (means between 9 4 and 26 3 C). The optimum temperature for time to flowering decreased linearly (from 21 3 C) with declining light integral from 3 4 MJm d (total solar radiation). Data from both experiments were used to construct a photothermal model of flowering in pansy. This assumed that the rate of progress to flowering increased as an additive linear function of light integral, temperature and photoperiod. Independent data from plants sown on three dates, and grown at five temperatures (means between 9 8 and 23 6 C) were used to validate this model which gave a good fit to the data (r 0 88, 15 d.f.). Possible confounding of the effects of photoperiod and light integral are discussed Annals of Botany Company Key words: Pansy; Viola wittrockiana, flowering, photo-thermal model, temperature, photoperiod, light integral. INTRODUCTION Although pansies (Viola wittrockiana Gams.) are commercially-important bedding plants, little is known about their flowering responses to temperature, photoperiod and light integral. Considerable commercial benefits can be gained from techniques which permit accurate scheduling of sowing for predetermined dates of crop maturity. Previous studies on pansies have concentrated on the close relative Viola tricolor. Withrow and Benedict (1936) showed that a daylength extension with low irradiance light hastened the flowering of Viola tricolor, indicating a long day flowering response. Hughes and Cockshull (1966) also reported that flowering of pansy was earlier when night-break lighting was applied, but no quantitative data are available on the photoperiod response of Viola wittrockiana, currently the most commonly cultivated species. However, there is a widely-held view among growers that it is day neutral, since the plant commonly flowers during winter. Similarly, very little is known about the flowering response of pansy to temperature. Merritt and Kohl (1991) showed that plants of cv. Universal Mix, grown at a mean diurnal temperature of 21 C, flowered earlier than those grown under cooler conditions. Pearson et al. (1995a) showed that time from visible bud to flowering in pansy cv. Universal Violet decreased linearly with increasing temperature from 10 to 25 C, but the optimum temperature for time to flowering has not been determined. Analytical approach: flowering responses to temperature, photoperiod and irradiance It has been shown for numerous plant species with both short and long day responses to photoperiod that, under inductive conditions, the rate of progress to first flowering (i.e. the opening of the first bud) can be described as a simple linear function of photoperiod and temperature: 1 f a bt cp, (1) where f is the number of days to first flowering, T is the mean daily temperature ( C), P is the mean photoperiod (hd ), and a, b and c are genotype-specific constants. For long day plants (LDPs), lengthening of photoperiod causes an increase in the rate of progress to flowering, so that c is positive, and ice ersa for short day plants (SDPs) (Hadley et al., 1983, 1984; Roberts, Hadley and Summerfield, 1985; Ellis et al., 1990). The temperature limits of the general thermal response can be described by three cardinal temperatures: the base (T b ), optimum (T o ) and ceiling (T c ) temperatures. At the base and ceiling temperatures the rate of progress to flowering is zero, whereas the highest rate of progress to flowering occurs at the optimum temperature. The optimum temperature can be estimated using the concept of effective temperature (Pearson, Hadley and Wheldon, 1993). This technique assumes that the response of the rate of development to temperature is similar, but opposite, above and below T o ; if this assumption is not correct in practice, the errors incurred will be small. Supra-optimal temperatures, for any estimated value of T o, can then be converted into effective temperatures (T e ) which represent the sub $ bo Annals of Botany Company
2 108 Adams et al. Time to Flowering in Pansy optimal temperature equivalents of supra-optimal temperatures in relation to developmental rate: T e T o T o T a and T b T a T c, (2) where T a is the actual temperature. To select the optimum temperature, T e is calculated for a range of optima. The optimized value for T o is the one which minimizes the residual sum of squares of the regression between reciprocal of days (rate of progress) to flowering and effective temperature. By considering effective temperatures, eqn (1) can be adapted to quantify the effects of both supra- and sub-optimal temperatures on the rate of progress to flowering: 1 f a bt e cp. (3) However, the general photo-thermal equation [eqn (3)] does not take into account the influence of light integral per se on the rate of progress to flowering. To date, little quantitative information is available to describe the effect of light integral on time to flowering. There is evidence to suggest that, at least for chrysanthemum, the rate of progress to flowering (Cockshull, 1972; Pearson et al., 1993) and flower initiation (Langton, 1992) decrease rapidly at light integrals below approx. 3MJm d (total solar radiation). Increasing irradiance above this threshold appears to have little additional affect on the time to flowering. The aims of this study were, therefore, to investigate the flowering responses of Viola wittrockiana to temperature, photoperiod and light integral, for plants grown under both natural and controlled daylengths, and to investigate how light integral can be accommodated within the general photo-thermal flowering model. MATERIALS AND METHODS Experiment 1. The effect of temperature and photoperiod on time to flowering: constant photoperiods The objective of this experiment was to determine the flowering response of pansy cv. Universal Violet to photoperiod and temperature. Seeds were sown on 14 Feb in a seed tray containing a peat-based seed and modular compost (SHL; William Sinclair Horticulture Ltd, Lincoln, UK), germinated and grown on for 15 d at 20 1 C in a growth room providing 90 µmol m s (PAR) at plant height from a mixture of white fluorescent and tungsten bulbs (6 3% tungsten calculated by nominal wattage), with a 16 h photoperiod. In accordance with commercial practice, these were then pricked out into plug-trays (Plantpak P84, Plantpak Ltd, Maldon, UK; volume of each cell, 40 ml) containing the same peat-based compost. The plants were placed on movable trolleys in the inner six, of a linear array of eight temperature-controlled glasshouse compartments (3 7 m 7 m) set to provide minimum temperatures of 6, 10, 14, 18, 22 and 26 C, with ventilation at temperatures 4 C above these set-points. Mean diurnal temperatures within each compartment were calculated from temperatures recorded on a data-logger (Datataker, DT500, Data Electronics, Letchworth Garden City, UK), linked to aspirated PT temperature sensors (15 sec scans, logged hourly). Each compartment was equipped with four photoperiodcontrolled chambers, sealed from exterior light sources. Plants remained in the glasshouse for 8 h. At 1600h each day, they were wheeled into the photoperiod chambers where they remained until 0800h the following morning. Daylengths were extended inside each of the chambers by low irradiance lighting (11µmol m s, PAR) provided by a 40W tungsten and a 15W compact fluorescent light bulb. In all treatments, the lamps were switched on automatically at 1600h for a duration dependent on the daylength length required (8, 11, 14 and 17 h). The chambers were continuously ventilated, with an average air speed of 0 2 ms over the plants when inside the chambers, to minimize any temperature increase. This experimental design provided a combination of six temperatures and four photoperiods. When plants reached the five leaf stage, they were potted on into 9 cm pots (volume 370 ml) containing a peat-based potting compost (SHL) into which 25% perlite had been incorporated. An irrigation system provided Sangral 111 liquid feed (SHL, William Sinclair Horticulture Ltd, Lincoln, UK) at each watering, at a conductivity of 1500 µs (182 ppm N; 78 ppm P; 150 ppm K), acidified to ph 5 8. Six replicate plants were grown in each treatment and the number of days to flowering (i.e. when the corolla had fully opened) were recorded for each plant. Experiment 2. The effect of temperature and sowing date on time to flowering: natural photoperiods This experiment was carried out to establish the flowering response of pansy to a wide range of temperatures, natural photoperiods and light integrals. Seeds of cv. Universal Violet were sown in a seed tray containing a peat-based compost (Shamrock Special; Shamrock Horticulture Ltd, Bristol, UK) on five occasions; 10 Jul. 1992, 4 Sep. 1992, 21 Oct. 1992, 11 Nov and 2 Dec These were germinated and grown for 25 d in a growth cabinet (Conviron S10H) at a temperature of C and an irradiance of 90 µmol m s (PAR), provided by a 2:1 mixture of warm white fluorescent and tungsten bulbs (determined on the basis of nominal wattage), with a 12 h daylength. Plants were then pricked out into plug-trays, and transferred to the same six temperature-controlled glasshouse compartments as used in expt 1 (set to provide minimum temperatures of 4, 10, 14, 18, 22 and 26 C). These were grown under natural daylengths and potted up at the five leaf stage as in expt 1, using the same peat-based compost (Shamrock Special). Plants were irrigated by hand and provided twice weekly with a solution of Sangral 101 soluble fertilizer (260 ppm N; 0 ppm P; 223 ppm K). The pots were gradually re-spaced to avoid mutual shading, until they reached a final plant density of 40 pots m. Twenty replicate plants were used in each treatment and the number of days for 50% of the population to reach flowering (corolla fully opened) were recorded. Mean diurnal temperatures were calculated from temperatures recorded on a data-logger (Combine; Murdoch, 1985) linked to aspirated thermistors (5 min intervals). Mean daily light integrals were obtained from a meterological site located 300 m from the glasshouses. The
3 glasshouse light transmission measured at the site (70%) was used to estimate the light integral transmitted into the glasshouse. Daily photoperiods during the course of the experiment were computed using the method of Sellers (1965). Experiment 3. Model alidation In order to validate the model independently, a further three crops were sown on 18 Oct. 1995, 29 Nov and 10 Jan Plants were raised as in expt 1 and grown on to flowering in the same temperature-controlled glasshouse compartments, set to provide minimum temperatures of 6, 10, 14, 18 and 22 C. Plants were again potted on at the five leaf stage and supplied with nutrients and water as described for expt 2. For each sowing date, 20 replicate plants were grown in each temperature compartment and the number of plants flowering was recorded daily. Temperature data were recorded using a DT500 data logger as in expt 1, light data were measured as in expt 2, and photoperiods during the course of the experiment were estimated using the method of Sellers (1965). RESULTS Experiment 1. The effect of temperature and photoperiod on time to flowering: constant photoperiods By the end of the experiment, 143 d after sowing, all plants had flowered except those grown at 26 C and photoperiods of 8 and 17 h. Rate of progress to flowering, estimated as the reciprocal of time to flowering, increased linearly with increasing photoperiod (Fig. 1), indicating a quantitative Adams et al. Time to Flowering in Pansy 109 Days to flower Temperature ( C) FIG. 2. Relationships between time to flowering and mean temperature from sowing for pansy cv. Universal Violet sown on 10 Jul ( ), 4 Sep ( ), 21 Oct ( ), 11 Nov ( ) and 2 Dec ( ). Each point is the time at which 50% of the 20 replicate plants had flowered. long day response. There was no evidence of either a ceiling or a critical photoperiod. In addition, flowering appeared to be sensitive to photoperiod in all temperature photoperiod combinations. Rate of progress to flowering increased linearly with temperature up to an optimum of 21 7 C [estimated using eqn (2)] and declined thereafter. Thus, for example, plants grown at a mean temperature of 15 C and a 17 h photoperiod flowered after 99 d compared with 124 d at 15 C and a 8 h photoperiod. Multiple linear regression showed that photoperiod and temperature affected the rate of progress to flowering independently (r 0 91, 19 d.f.), indicating that the general photo-thermal model [eqn (3)] was appropriate in describing the flowering response of pansy to temperature and photoperiod. 30 1/Days to flower Photoperiod (h d 1 ) Temperature ( C) FIG. 1. The effects of mean temperature and photoperiod on the reciprocal of days to flowering (1 f) of pansy cv. Universal Violet. Each point is the mean of six replicate plants. The mesh was fitted by regression analysis; 1 f ( ) ( )T e ( )P, r 0 91, 19 d.f., where T e and P represent effective temperature and photoperiod, respectively, with an optimum temperature (T o )of21 7 C. Experiment 2. The effect of temperature and sowing date on time to flowering: natural photoperiods All crops flowered within the experimental period, except those grown at the two highest temperatures in the 4 September sowing, and plants grown at the highest temperature in the 21 October and 11 November sowings. The effect of temperature on time to flowering was relatively small compared with the effect of sowing date (Fig. 2). The earliest flowering occurred in crops sown during July, whereas the slowest flowering occurred in crops sown during September. Figure 2 also indicates that the optimum temperature for earliest flowering decreased between the July and September sowings. Thus, for plants sown in July, which flowered rapidly, the optimum temperature appeared to be in the region C, but for plants sown in September, whose flowering was the slowest, the optimum temperature appeared to be approx. 16 C. The optimum temperature for plants grown at each sowing date was estimated using eqn (2) using the FITNONLINEAR subroutine of GENSTAT 5 (GENSTAT 5, Release 3 1, 1993) and then plotted against the mean daily light integral received for that particular sowing date (Fig.
4 110 Adams et al. Time to Flowering in Pansy Optimum temperature ( C) Actual days to flower Light integral (MJ m 2 d 1 ) FIG. 3. The relationship between estimated optimum temperature [as described in eqn (2)] and light integral (MJ m d ; total solar radiation) for crops sown on 10 Jul ( ), 4 Sep ( ), 21 Oct ( ), 11 Nov ( ), 2 Dec ( ) and 16 Feb ( ), (r 0 96, 4 d.f.). Vertical bars indicate s.e. of the estimates of optimum temperature. Predicted days to flower Actual days to flower FIG. 4. The actual time to 50% flowering of pansy plants grown at a range of mean temperatures between 9 4 and 26 3 C and sown on five dates between 10 Jul and 2 Dec. 1992, compared with those predicted from the relationship between photoperiod and temperature on the reciprocal of time to flowering [eqn (3); see legend to Fig. 1] from expt 1 ( ). ( ), Predicted times to flowering, using the temperature, light integral and photoperiod model [eqn (5)] compared with the actual values of all the crops grown during expts 1 and 2. The solid line is the line of identity (r 0 94, 44 d.f.). 3). This shows that the optimum temperature decreased linearly with decrease in light integral below 3 4 MJm d (total solar radiation). Above this value there was no evidence of a change in optimum temperature, where T o 21 3 C. A broken stick relationship fitted to the data accounted for 96% of the variance in the change in optimum temperature with light integral: T o 6 93 ( 0 61) 4 25 ( 0 72) M (r 0 96, 4 d.f.), (4) where M 3 38 MJ m d (total solar radiation), if M 3 38 MJ m d then T 21 3 C. o Predicted days to flower 180 FIG. 5. Validation of the flowering model, comparing the time to flowering of plants sown on three occasions; 18 Oct ( ), 29 Nov ( ) and 10 Jan ( ), and grown at one of five different temperatures between 9 8 and 23 6 C, with those predicted by the flowering model [eqn (5)]. The vertical bars indicate 95% confidence intervals for the mean flowering date of the 20 replicate plants (r 0 88, 15 d.f.). The combined effects of temperature, photoperiod and light integral on time to flowering The application of the general photo-thermal flowering model, using parameters derived from expt 1 [eqn (3)] was then examined using data from expt 2. Figure 4 (open symbols) shows the predicted times to flowering compared with the observed flowering dates for all plants in expt 2. This demonstrates that the model, taking into account only temperature and photoperiod, did not predict time to flowering accurately. However, the error was systematic, such that the flowering times of the fastest-maturing plants were overestimated, whereas those of the late-maturing plants were underestimated. Mean light integral was then incorporated into the flowering model as a linear term, and the model fitted using all the data from both experiments. The analysis, which assumed that the optimum temperature for flowering varied with light integral according to the relationship shown in Fig. 3 [eqn (4)], described the data accurately: 1 f T e P M ( ) ( ) ( ) ( ) (r 0 94, 44 d.f.), (5) where the optimum temperature to determine T was derived e from eqn (4). Therefore, all three environmental factors examined had significant and independent linear effects on the reciprocal of time to flowering. Further analysis revealed that there were no interactions between any of the variables. Figure 4 shows the predicted s. actual flowering dates of the data used to construct the relationship; this indicates that there was little evidence for any systematic deviation in predicted compared with actual times to flowering. Experiment 3. Model alidation Independent data from the three crops sown on 18 Oct. 1995, 29 Nov and 10 Jan. 1996, and grown at one of
5 five temperature regimes (minimum temperatures of 6, 10, 14, 18 and 22 C) were used to test the validity of the flowering model [eqn (5)]. For each data set, the model was solved using an iterative procedure against running means of average daily temperature, photoperiod and light integral, up to the day on which the product of the average daily contributions to flowering equalled one (determined as the days from sowing multiplied by the average daily progress to flowering, derived from eqn. (5) solved with running means on each day). The accuracy of the predictions is illustrated in Fig. 5, which indicates that the model gave a good fit to the data (r 0 88, 15 d.f.). DISCUSSION This study has shown that Viola wittrockiana is a quantitative LDP, contradicting the widely-held view amongst commercial producers that modern pansy varieties are day neutral. The response to photoperiod was, however, quite weak compared with that of the closely-related species Viola tricolor; Withrow and Benedict (1936) showed that plants of the latter species grown in glasshouses with the daylength extended to 21 h, flowered up to 72 d earlier than control plants grown under natural short days. Here, the difference between the 17 and 8 h treatments, at 15 C, was only 25 d. This weak response to photoperiod is probably one of the reasons why Viola wittrockiana, often referred to as winter flowering pansy can flower and be produced over the winter months. This study has also indicated an important effect of light integral on flowering, presumably as a consequence of increased assimilate availability and growth. Previous analyses using the general photo-thermal model have not shown a significant effect of light integral on time to flowering, with the exception of Pearson et al. (1993) in their reanalysis of the effects of temperature and irradiance on the time to flowering in chrysanthemum. However, the present study indicates that such responses can be missed particularly when daylengths are extended with lighting at photosynthetic irradiances i.e. when light integral and photoperiod are confounded. To accommodate an influence of light integral, the general photo-thermal equation was modified [eqn (5)] by assuming that the rate of progress to flowering was a positive linear function of light integral. This implies that the relationship between days to flowering and light integral is hyperbolic such that, at low light integral, small increases in light will produce a substantial reduction in time to flowering. Conversely, at high light integral, further increases in light will produce little additional effect on time to flowering. A similar response has been reported for flower commitment of chrysanthemum (Langton, 1992). Information on the effects of light integral on the time to flowering is of considerable value, since growers could control flowering, and therefore grow to defined schedules, by manipulating the light environment, either by shading or through the use of supplementary lighting. Temperature significantly affected the time to flowering, Adams et al. Time to Flowering in Pansy 111 as reported for many other species (see, for example, Ellis et al., 1990). Other studies have shown that optimum temperature for certain species varies with ontogeny; for example, in Primula malacoides (Ru nger and Wehr, 1971), and in Osteospermum jucundum (Pearson et al., 1995b) the optimum temperature for flower induction was lower than for flower development following induction. However, the present study has shown that, at low light integrals the optimum temperature for flowering decreased. A similar shift in optimum temperature was also suggested by an analysis of the effects of light, photoperiod and temperature on flowering of Senecio hybridus (Larsen, 1988). The reason for this shift in optimum temperature with light integral has not been established. It may be that the optimum temperature declines as the assimilate availability decreases as a result of low light integrals, but further work is needed to establish the physiological basis of this response. The response to temperature was weak relative to the effect of light integral such that the potential for manipulating maturity dates by adjusting the temperature is relatively small. Furthermore, increases in temperature during the later stages of plant development would have deleterious effects on plant quality, since this would reduce flower size (Pearson et al., 1995a). In addition to using the model to predict flowering date, the model [eqn (5)] could also be used for the rapid screening of new pansy germplasm, as has been proposed with other species (Ellis et al., 1990). Cultivars with a low value of b, the constant for the temperature response, would flower adequately at a range of temperatures. Varieties with a low value of c, the photoperiod response constant, and the constant for the light integral response, would have a greater propensity for flowering in the winter months, where scheduling pansy production is difficult at present. The general photo-thermal model can be used to develop improved sowing date schedules. The value of improved scheduling techniques should not be underestimated, since, in the UK alone, it has been estimated that up to 10% of bedding production is wasted as a result of inadequate scheduling (S. Coutts, pers. com.). Conventionally, crop schedules are developed by sowing a series of crops over a range of dates and measuring their flowering dates, but such schedules are notoriously inaccurate. The results achieved are highly dependent not only on the environmental conditions experienced during the development of the programme, but also, as shown here, latitude, since photoperiod and light integrals change with latitude. However, by using the photo-thermal model, schedules can be tailored for individual growers, since the model considers environmental factors which vary between different locations; i.e. photoperiod, irradiance and temperature. Furthermore the flowering model could be used on-line by growers to advise how maturity dates can be manipulated to meet defined targets. Such an approach would be most powerful if combined with models, such as those proposed by Pearson et al. (1995a) and Adams, Pearson and Hadley (1997), for predicting the effects of environment on plant quality.
6 112 Adams et al. Time to Flowering in Pansy ACKNOWLEDGEMENTS We thank the Horticultural Development Council and The Ministry of Agriculture, Fisheries and Food who funded this work. We would also like to thank Stuart Coutts and Brian Crosby for their useful comments and encouragement. LITERATURE CITED Adams SR, Pearson S, Hadley P An analysis of the effects of temperature and light integral on the vegetative growth of Pansy cv. Universal Violet (Viola wittrockiana Gams.). Annals of Botany. 79: Cockshull KE Photoperiodic control of flowering in the chrysanthemum. In: Rees AR, Cockshull KE, Hand DW, Hurd RG, eds. Crop processes in controlled en ironments. London: Academic Press, Ellis RH, Hadley P, Roberts EH, Summerfield RJ Quantitative relations between temperature and crop development and growth. In: Jackson MT, Ford-Lloyd BV, Parry ML, eds. Climatic change and plant genetic resources. London: Belhaven Press, Hadley P, Roberts EH, Summerfield RJ, Minchin FR A quantitative model of reproductive development in cowpea (Vigna unguiculata (L.) Walp.) in relation to temperature and photoperiod, and implications for screening germplasm. Annals of Botany 51: Hadley P, Roberts EH, Summerfield RJ, Minchin FR Effects of temperature and photoperiod on flowering in soyabean (Glycine max (L.) Merrill): a quantitative model. Annals of Botany 53: Hughes AP, Cockshull KE Effects of night-break lighting on bedding plants. Experimental Horticulture 16: Langton FA Interrupted lighting of chrysanthemums: monitoring of average daily light integral as an aid to timing. Scientia Horticulturae 49: Larsen R A prediction model for floral development of Senecio hybridus Hyl. Moll s Stam. Swedish Journal of Agricultural Research 18: Merritt RH, Kohl HC Morphology of bedding plants in response to low night temperature and energy use implications. Scientia Horticulturae 45: Murdoch AJ Low cost, computer based data handling of soil temperature data in field experiments. Aspects of Applied Biology 10: Pearson S, Hadley P, Wheldon AE A reanalysis of the effects of temperature and irradiance on the time to flowering in chrysanthemum (Dendranthema grandiflora). Journal of Horticultural Science 68: Pearson S, Parker A, Adams SR, Hadley P, May DR. 1995a. The effects of temperature on the flower size of pansy (Viola wittrockiana Gams). Journal of Horticultural Science 70: Pearson S, Parker A, Hadley P, Kitchener HM. 1995b. The effect of photoperiod and temperature on reproductive development of Cape Daisy (Osteospermum jucundum cv. Pink Whirls ). Scientia Horticulturae 62: Roberts EH, Hadley P, Summerfield RJ Effects of temperature and photoperiod on flowering in chickpeas (Cicer arietinum L.). Annals of Botany 55: Ru nger W, Wehr B Einfluß von Tagesla nge und Temperatur auf die Blu tenbildung und -entwicklung von Primula malacoides. Gartenbauwissenschaft 36: Sellers WD Physical climatology. Chicago: University of Chicago Press. Withrow RB, Benedict HM Photoperiodic responses of certain greenhouse annuals as influenced by intensity and wavelength of artificial light used to lengthen the daylength. Plant Physiology 11:
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