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Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species
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Scientia Horticulturae 115 (2008) 309–314 www.elsevier.com/locate/scihorti
Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species Ola M. Heide * Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 A˚s, Norway Received 14 February 2007; received in revised form 27 August 2007; accepted 1 October 2007
Abstract Growth and dormancy induction of seedlings or micropropagated plants of three Prunus species were studied under controlled environment conditions. All the species tested, P. cerasus L. and P. insititia L. (two cultivars each), and P. avium L. were insensitive to photoperiod at high temperature and maintained continuous growth in both 10 and 24-h photoperiods at 21 8C. At lower temperatures, however, growth was controlled by the interaction of photoperiod and temperature, the species and cultivars varying somewhat in their responses. At 9 8C growth cessation was induced regardless of day-length conditions in the plum rootstocks ‘St. Julien A’ and ‘Weito’ as well as in the sour cherry rootstock ‘Weiroot’, whereas in the sour cherry rootstock ‘Gisela 5’ growth cessation took place in short day (SD) only. At intermediate temperatures (12 and 15 8C) growth cessation occurred in SD only in both sour cherry cultivars. In P. avium seedlings on the other hand, growth cessation in SD was only induced at 9 8C, continuous but reduced growth taking place also in SD at all higher temperatures. Growth rates increased progressively with increasing temperature under long day (LD) conditions in all species, and this was associated with increased internode length in LD compared with SD conditions. Production of new leaves was unaffected by photoperiod at high temperature, but was higher in LD than in SD at lower temperatures. After growth cessation at low temperature the plants developed winter buds and became dormant also in LD conditions. These results demonstrate that, like several species of the Pomoidae subfamily of the Rosaceae, these Prunus species are insensitive to short photoperiods at relatively high temperatures. However, the photoperiodic response of the Prunus species is highly temperature dependent, and the transition temperatures for shifts in the photoperiodic response mode vary among the species. # 2007 Elsevier B.V. All rights reserved. Keywords: Cherry; Growth cessation; Internode length; Leaf production; Plum; Rootstocks; Rosaceae
1. Introduction Seasonal regulation of growth and dormancy is crucial for plant survival in temperate and cold climates. This requires the timely sensing and processing of a regular and reliable environmental signal. The role of short photoperiods in the autumn as the dormancy-inducing signal in woody plants was first demonstrated by Garner and Allard (1923) and has later been amply documented for a wide variety of trees and shrubs (e.g. Kramer, 1936; Downs and Borthwick, 1956; Wareing, 1956; Nitsch, 1957; Heide, 1974; Ha˚bjørg, 1978; Bo¨hlenius et al., 2006). Temperatures within the normal growth range do not change the critical photoperiods for dormancy induction significantly, although warm conditions usually advance the progress to dormancy (Heide, 1974; Junttila et al., 2003).
* Tel.: +47 64965386; fax: +47 64965801. E-mail address: [email protected]. 0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.10.005
However, near-freezing night-time conditions (21/4 8C, 14/ 10 h) may induce growth cessation even in continuous light, at least in some species (Heide, 1974). An important exception to the short day (SD) control of dormancy in woody plants was already noticed by Garner and Allard (1923) for apple (Malus pumila Mill.), which was not affected by photoperiod. This exception was confirmed and extended to several other genera of the Rosaceae family by Nitsch (1957). As no other environmental signal was known to induce dormancy induction in these plants, their dormancy was considered to be under entirely endogenous control (Wareing, 1956; Battey, 2000). However, in a recent paper by Heide and Prestrud (2005), it was demonstrated that low temperature (<12 8C) consistently induces growth cessation and dormancy in apple and pear rootstocks under both SD and long day (LD) conditions. Chilling at 6 or 9 8C for about 1000 h was required for dormancy release and growth resumption. The investigation also confirmed that at higher temperatures (15–21 8C) short photoperiods have no dormancy-inducing effect in these plants.
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Since several genera of the Pomoidae subfamily within the Rosaceae are known to be insensitive to photoperiod (Wareing, 1956; Nitsch, 1957; Heide and Prestrud, 2005), it is of interest to know how growth and dormancy are controlled in other subfamilies of the Rosaceae such as the Prunoidae. In an early investigations with embryo-cultured peach seedlings (Prunus persica) Lammerts (1943) demonstrated that seedlings kept in 16 or 24-h daylength at high temperature (above 21 8C) grew continuously, while their growth was arrested or strongly reduced in 8-h or natural winter SD at both low and intermediate temperatures. Similarly, Went (1957) reported that peach seedlings grew continuously in 16-h SD at a 23/ 17 8C day/night temperature while at day lengths of 13 h or less at the same temperature conditions, they ceased growing and became dormant. However, since temperature and photoperiod were not varied systematically in a factorial design, limited conclusion can be drawn from these experiments. In the present paper I present the results of experiments with three Prunus species (cherry and plum) which have been grown at a range of temperatures under both SD and LD conditions. A pronounced interaction of photoperiod and temperature is demonstrated. 2. Materials and methods 2.1. Plant material and cultivation ˚ s phytotron The experiments were performed in the A (608N, 118E) in daylight compartments combined with adjacent growth rooms for photoperiodic manipulation as explained below. The species and cultivars used for the experiments are listed in Table 1. Young seedlings of P. avium and in vitro micropropagated plants of P. cerasus and P. insititia were obtained from two commercial nurseries. The plants had been transferred to soil and grown in 4 cm plug trays for about 4 weeks to a height of 4–5 cm before delivery. When received, the plants were transplanted into 10 cm plastic pots containing a peat-based potting compost (84% peat, 10% fine sand and 6% clay), and grown at 21 8C in 24-h photoperiod for 1 week before the experimental treatments began. The plants were fertilized twice weekly with a complete fertilizer solution and otherwise watered with tap water as required. All plants received natural spring and summer daylight for 10 h per day (08:00–18:00 h). Whenever the photosynthetic photon flux (PPF) in the daylight compartments fell below about 150 mmol m2 s1 on cloudy days, an additional 125 mmol m2 s1 quanta was automati-
cally added. Daylength extension to 24-h photoperiod was provided by low-intensity light from 75-W incandescent lamps (about 6 mmol m2 s1 PPF). Plants receiving SD treatments were kept in darkness from 18:00 to 08:00 h. The additional light from the daylength extension treatment amounted to only 2% of the total daily radiation, the plants thus received nearly the same daily light integral in both daylengths. Temperatures were controlled to 1.0 8C and a water vapour pressure deficit of 530 Pa was maintained at all temperatures. Three experiments were carried out during the years 2004– 2006. Experiment 1 examined the elongation growth of ‘Gisela 5’ sour cherry and ‘Weito’ plum rootstocks at constant 9, 12, 15 and 21 8C and photoperiods of 10 and 24 h. The experiment was started on April 24, 2003 and lasted for 8 weeks. Plants whose growth had ceased at 9 8C were then transferred to 21 8C and 24-h LD for another 4 weeks in order to establish whether they were truly dormant. Experiment 2 was designed to test the effect of transferring actively growing plants of ‘Weiroot’ sour cherry and ‘St. Julien A’ plum rootstocks from 21 8C (10 h SD and 24 h LD) to 9 8C without change of photoperiod. The experiment was started on May 30, 2005 and lasted for 6 weeks. Experiment 3 examined the elongation growth of wild-growing sweet cherry seedlings at constant 9, 12, 15 and 21 8C and photoperiods of 10 and 24 h. An extra set of plants was transferred from 21 to 9 8C after 3 weeks of active growth. The experiment was started on May 4, 2006 and lasted for 8 weeks. 2.2. Experimental design and measurements The experiments were factorial with a split plot design with temperatures as main plots and with photoperiods and species/ cultivars as sub-plots. Each treatment included ten plants of each species/cultivar. Elongation growth was monitored by weekly measurements of plant heights. These observations provided accurate information of growth rates and the time of growth cessation. Production of new leaves (nodes) was determined by marking the last developed leaf (>2 cm) of each plant at start of the experiments and counting additional leaves at various times during the experiments. Analysis of variance (ANOVA) of the data obtained after 6–8 weeks of cultivation was performed using the Systat Version 5.0 program package. Since the experiments were not replicated in time, the main effects of treatments and species, and their interactions, were tested against their respective two- and three-factor interactions.
Table 1 Identity and origin of the Prunus species and cultivars used for the experiments Species
Cultivar
Origin
Characterization
P. P. P. P. P.
‘Gisela 5’ ‘Weiroot’ ‘St. Julien A’ ‘Weito’
Giessen, Germany Weihenstephan, Germany East Malling, UK Weihenstephan, Germany Vestby, Norway (598300 N)
Commersial rootstock Commersial rootstock Commersial rootstock Commersial rootstock Wild-growing trees
cerasus (Sour cherry) cerasus (Sour cherry) insititia (Plum) insititia (Plum) avium (Sweet cherry)
For further information on the plum and cherry rootstocks, see Rom and Carlson (1987).
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3. Results 3.1. Experiment 1 Both temperature and daylength had a highly significant effect (P < 0.001) on elongation growth of both the plum and the sour cherry cultivars (Fig. 1). However, the daylength effect varied with the temperature, yielding a highly significant interaction between the two environmental factors. Thus, in ‘Weito’ plum plants growth cessation occurred in both SD and LD at 9 8C, at 12 8C in SD only, while at 15 and 21 8C growth continued in both daylengths although at a lower rate in SD, especially at 15 8C. The more vigorous-growing ‘Gisela 5’sour cherry was less sensitive to low temperature and more sensitive to short photoperiods than was ‘Weito’. Thus, no growth cessation took place under LD conditions in ‘Gisela 5’ plants even at 9 8C. While continuous growth was maintained in both daylengths at 21 8C, growth cessation occurred in SD conditions at all lower temperatures in this cultivar, the rate of response increasing with decreasing temperature (Fig. 1). Thus, at 9 8C growth cessation took place after 3 weeks in SD, at 12 and 15 8C not until 7 weeks of cultivation. These results yielded a highly significant three-factor interaction on elongation growth of temperature, daylength and cultivar (P < 0.001). Leaf formation increased more or less linearily with increasing temperature in both species. The main effect of photoperiod was also significant (P < 0.05), and again with a highly significant interaction with temperature (P < 0.01). Thus, in both cultivars there was no significant effect of photoperiod on leaf formation at 21 8C, whereas growth cessation in SD at lower temperatures was accompanied by markedly reduced leaf numbers (Fig. 2). The photoperiodic effect on elongation growth at high temperature (21 8C) was thus an effect of internode length only, as the initiation of new nodes was unaffected by daylength at this temperature.
Fig. 2. Effects of temperature and photoperiod on the formation of new leaves in the plum cultivar ‘Weito’ and the sour cherry cultivar ‘Gisela 5’. Filled columns represent 10-h SD and open columns 24-h LD conditions. Values are means standard errors for 10 plants in each treatment as recorded after 7 weeks of growth at the respective conditions.
‘Weito’ plants held at 9 8C formed winter buds and gradually developed autumn colours under both SD and LD conditions. In ‘Gisela 5’ this happened under SD conditions only. When these plants were transferred to high temperature (21 8C) and LD after 8 weeks of treatment, the plants remained dormant with no resumption of growth within 4 weeks, after which time the experiment was terminated. This test was performed on plants gown at 9 8C only. 3.2. Experiment 2 The interaction of temperature and daylength was confirmed in another pair of plum and sour cherry cultivars (Fig. 3). Both cultivars grew at constant rate at 21 8C in both SD and LD,
Fig. 1. Time course of elongation growth of the plum cultivar ‘Weito’ and the sour cherry cultivar ‘Gisela 5’ grown under different temperature and photoperiod regimes as indicated. Values are means standard errors for 10 plants in each treatment group.
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Fig. 3. Time course of elongation growth of the sour cherry cultivar ‘Weiroot’ and the plum cultivar ‘St. Julien A’ grown continuously at 21 8C in 10-h SD (filled symbols) and 24-h LD (open symbols), and after transfer to 9 8C under the same daylength conditions at the time indicated by arrows. Values are means standard errors for 10 plants in each treatment.
although at a slower rate in SD conditions. This effect of daylength was solely due to increased internode length in LD, as the average number of new leaves produced was the same in both daylengths (20.3 and 20.1 for ‘St. Julien A’; 18.2 and 18.4 for ‘Weiroot’ in LD and SD, respectively after 6 weeks of growth). When plants were transferred from 21 to 9 8C after 3 weeks of active growth, they immediately ceased growing in both daylengths, so that after 1 week no further growth took place in either cultivar (Fig. 3).
Fig. 4. Time course of elongation growth of seedlings of wild-growing sweet cherry grown under different temperature and photoperiod regimes as indicated. Arrows indicate time of transfer to 9 8C. Values are means standard errors for 10 plants in each treatment group.
3.3. Experiment 3 The sweet cherry seedlings grew vigorously and reached a height of nearly 1 m after 8 weeks at 21 8C and LD (Fig. 4). They also showed a somewhat different response to temperature and photoperiod than did the plum and sour cherry plants in the previous experiments. Thus, although SD reduced growth by reducing internode length at all temperatures also in this species, growth cessation in SD took place at 9 8C only. Like the ‘Gisela 5’ sour cherry, this species did not cease growing in LD at such low temperature, but continued a slow growth after a pause in growth during weeks 3 and 4. Such slow growth in LD was also maintained in about 50% of the plants after transfer from 21 to 9 8C after 3 weeks, whereas all plants in SD ceased growing within 1 week from transfer (Fig. 4), and subsequently formed winter buds. Although no growth cessation took place in SD at temperatures above 9 8C, stem elongation was strongly reduced in SD at these higher temperatures in this species in comparison to growth under LD conditions. The reduced elongation in SD was associated with a significant reduction in leaf numbers (Fig. 5). Therefore, reduced growth in SD in this species was
Fig. 5. Effects of temperature and photoperiod on the formation of new leaves of sweet cherry seedlings. Filled columns represent 10-h SD and open columns 24-h LD conditions. Values are means standard errors for 10 plants in each treatment group as recorded after 7 weeks of growth at the respective conditions.
O.M. Heide / Scientia Horticulturae 115 (2008) 309–314
due to the combined effect of reduction in both internode length and numbers. 4. Discussion The results of these experiments demonstrate a pronounced interaction of photoperiod and temperature in the regulation of growth and growth cessation in all the tested Prunus species. At high temperature (21 8C) they responded with continuous growth regardless of photoperiodic conditions in much the same way as Malus and Pyrus (Nitsch, 1957; Heide and Prestrud, 2005). However, unlike these genera, most of the Prunus species were clearly sensitive to daylength at intermediate temperatures (12 and 15 8C), and ceased growing after a few weeks in SD conditions (Figs. 1 and 3). At low temperature (9 8C) on the other hand, the Prunus species varied in their response to photoperiod. While the wild sweet cherry and the sour cherry ‘Gisela 5’ required the combination of low temperature and SD for growth cessation and formation of winter buds, the other Prunus cultivars ceased growing and formed winter buds at 9 8C in both SD and LD conditions in much the same way as Malus and Pyrus (Figs. 1 and 3). Such photoperiod temperature interactions are well known in the control of flowering (Thomas and Vince-Prue, 1997), and the molecular mechanisms controlling such interactions are now beginning to be understood (Halliday et al., 2003; Benedict et al., 2006). It has also recently been demonstrated that, in aspen trees, the same molecular mechanisms control SD induction of both flowering and growth cessation (Bo¨hlenius et al., 2006). Although the present investigation was not intended to study such molecular transduction processes, the results provide circumstantial evidence for temperature ‘‘gating’’ of phytochrome controlled photoperiodic processes as suggested by Halliday et al. (2003). Dormancy is a quantitative condition that is gradually attained and overcome. It has been demonstrated in both conifers (Heide, 1974) and deciduous trees (Junttila, 1976) that during early stages of SD-induced growth cessation, a shift back to LD is all that is needed for growth resumption. Even with as many as 32 SD cycles, growth resumption took place in subsequent LD in Salix (Junttila, 1976). Furthermore, buds at different positions on the annual shoot often exhibit different dormancy states. For these reasons a precise time of dormancy attainment cannot be determined. However, after growth cessation, the Prunus species formed terminal winter buds, and a relatively deep state of dormancy was demonstrated after 8 weeks of low temperature treatment in Exp. 1, in much the same way as previously demonstrated for Malus, which under the same conditions required about 1000 h of chilling for growth resumption (Heide and Prestrud, 2005). There is thus little doubt that the described growth cessation in the Prunus species also led to bud dormancy. The pronounced interaction of photoperiod and temperature that was demonstrated in the Prunus species, suggests that these species actually have a dual dormancy induction control system, securing timely growth cessation and
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dormancy induction in response to the progressive lowering of daylength and temperature in the autumn. Thus, under unusually mild autumn conditions the Prunus species will still be induced to growth cessation by the rapidly decreasing photoperiod around fall equinox. Such a dual control mechanism would make these species especially well adapted to avoiding the possible negative effects on winter bud preparations by the predicted and ongoing global warming (Serreze et al., 2000). An exception to this behaviour was seen in P. avium, which maintained an active (but reduced) growth in SD at intermediate temperatures and ceased growth in SD at low (9 8C) temperature only. A similar temperature photoperiod interaction was reported for raspberry (Rubus idaeus), another member of the Rosaceae (Williams, 1959). Thus, raspberry plants grew continuously in both 9 and 14-h photoperiod at 21 8C, at 10 8C they ceased growing in both daylengths, whereas at 15 8C growth cessation took place in SD only. Nestby (1986) demonstrated that even under natural continuous light conditions at high latitudes, raspberry plants ceased growing and became dormant at low summer temperatures of about 10 8C. Growth cessation and dormancy induction by low temperature thus seems to be rather widespread within the Rosaceae. However, in Prunus species the photoperiodic response is highly temperature dependent, and the transition temperatures for shifts in the photoperiodic response mode vary among species and cultivars. Acknowledgement I am grateful to Gartnerhallen’s Elite Plant Station, Sauherad, Norway and Bla˚dike Tree Nurseries, Vestby, Norway for the gift of the micropropagated plants and the Prunus avium seedlings, respectively. References Battey, N.H., 2000. Aspects of seasonality. J. Exp. Bot. 51, 1769–1780. Benedict, C., Geisler, M., Trygg, J., Huner, N., Hurry, V., 2006. Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol. 141, 1219–1232. Bo¨hlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H., Nilsson, O., 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040– 1043. Downs, R.J., Borthwick, H.A., 1956. Effect of photoperiod on growth of trees. Bot. Gaz. 117, 310–326. Garner, W.W., Allard, H.A., 1923. Further studies in photoperiodism, the response of the plant to relative length of day and night. J. Agric. Res. 23, 871–920. Ha˚bjørg, A., 1978. Photoperiodic ecotypes in Scandinavian trees and shrubs. Meld. Nor. Landbrukshøgsk. 57 (33), 1–20. Halliday, K.J., Salter, M.G., Thingnaes, E., Whitelam, C.G., 2003. Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J. 33, 875–885. Heide, O.M., 1974. Growth and dormancy in Norway spruce (Picea abies). I. Interaction of photoperiod and temperature. Physiol. Plant 30, 1–12. Heide, O.M., Prestrud, A.K., 2005. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol. 25, 109–114.
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Junttila, O., 1976. Apical growth cessation and shoot tip abortion in Salix. Physiol. Plant 38, 278–286. Junttila, O., Nilsen, J., Igeland, B., 2003. Effect of temperature on the induction of bud dormancy in ecotypes of Betula pubescens and Betula pendula. Scand. J. For. Res. 18, 208–217. Kramer, P.J., 1936. Effect of variation in length of day on growth and dormancy of trees. Plant Physiol. 11, 127–137. Lammerts, W.E., 1943. Effect of photoperiod and temperature on growth of embryo-cultured peach seedlings. Am. J. Bot. 30, 707–711. Nestby, R., 1986. Red raspberry growth variation of selections and cultivars, at different northern latitudes in the year of planting. Acta Hort. 183, 191–198. Nitsch, J.P., 1957. Photoperiodism in woody plants. Proc. Am. Soc. Hort. Sci. 70, 526–544.
Rom, R.C., Carlson, R.F., 1987. Rootstocks for Fruit Crops. John Wiley and Sons, New York, 494 pp. Serreze, M.C., Walsch, J.E., Chapin III, F.C., et al., 2000. Observational evidence of recent change in the northern high-latitude environment. Clim. Change 46, 159–207. Thomas, B., Vince-Prue, D., 1997. Photoperiodism in Plants, second ed. Academic Press, London, 428 pp. Wareing, P.J., 1956. Photoperiodism in woody plants. Annu. Rev. Plant Physiol. 7, 191–214. Went, F.W., 1957. The Experimental Control of Plant Growth. Chapter 12. The Ronald Press Company, New York. Williams, I.H., 1959. Effects of environment on Rubus idaeus L. III. Growth and dormancy of young shoots. J. Hort. Sci. 34, 210–218.
Scientia Horticulturae 115 (2008) 309–314 www.elsevier.com/locate/scihorti
Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species Ola M. Heide * Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 A˚s, Norway Received 14 February 2007; received in revised form 27 August 2007; accepted 1 October 2007
Abstract Growth and dormancy induction of seedlings or micropropagated plants of three Prunus species were studied under controlled environment conditions. All the species tested, P. cerasus L. and P. insititia L. (two cultivars each), and P. avium L. were insensitive to photoperiod at high temperature and maintained continuous growth in both 10 and 24-h photoperiods at 21 8C. At lower temperatures, however, growth was controlled by the interaction of photoperiod and temperature, the species and cultivars varying somewhat in their responses. At 9 8C growth cessation was induced regardless of day-length conditions in the plum rootstocks ‘St. Julien A’ and ‘Weito’ as well as in the sour cherry rootstock ‘Weiroot’, whereas in the sour cherry rootstock ‘Gisela 5’ growth cessation took place in short day (SD) only. At intermediate temperatures (12 and 15 8C) growth cessation occurred in SD only in both sour cherry cultivars. In P. avium seedlings on the other hand, growth cessation in SD was only induced at 9 8C, continuous but reduced growth taking place also in SD at all higher temperatures. Growth rates increased progressively with increasing temperature under long day (LD) conditions in all species, and this was associated with increased internode length in LD compared with SD conditions. Production of new leaves was unaffected by photoperiod at high temperature, but was higher in LD than in SD at lower temperatures. After growth cessation at low temperature the plants developed winter buds and became dormant also in LD conditions. These results demonstrate that, like several species of the Pomoidae subfamily of the Rosaceae, these Prunus species are insensitive to short photoperiods at relatively high temperatures. However, the photoperiodic response of the Prunus species is highly temperature dependent, and the transition temperatures for shifts in the photoperiodic response mode vary among the species. # 2007 Elsevier B.V. All rights reserved. Keywords: Cherry; Growth cessation; Internode length; Leaf production; Plum; Rootstocks; Rosaceae
1. Introduction Seasonal regulation of growth and dormancy is crucial for plant survival in temperate and cold climates. This requires the timely sensing and processing of a regular and reliable environmental signal. The role of short photoperiods in the autumn as the dormancy-inducing signal in woody plants was first demonstrated by Garner and Allard (1923) and has later been amply documented for a wide variety of trees and shrubs (e.g. Kramer, 1936; Downs and Borthwick, 1956; Wareing, 1956; Nitsch, 1957; Heide, 1974; Ha˚bjørg, 1978; Bo¨hlenius et al., 2006). Temperatures within the normal growth range do not change the critical photoperiods for dormancy induction significantly, although warm conditions usually advance the progress to dormancy (Heide, 1974; Junttila et al., 2003).
* Tel.: +47 64965386; fax: +47 64965801. E-mail address: [email protected]. 0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.10.005
However, near-freezing night-time conditions (21/4 8C, 14/ 10 h) may induce growth cessation even in continuous light, at least in some species (Heide, 1974). An important exception to the short day (SD) control of dormancy in woody plants was already noticed by Garner and Allard (1923) for apple (Malus pumila Mill.), which was not affected by photoperiod. This exception was confirmed and extended to several other genera of the Rosaceae family by Nitsch (1957). As no other environmental signal was known to induce dormancy induction in these plants, their dormancy was considered to be under entirely endogenous control (Wareing, 1956; Battey, 2000). However, in a recent paper by Heide and Prestrud (2005), it was demonstrated that low temperature (<12 8C) consistently induces growth cessation and dormancy in apple and pear rootstocks under both SD and long day (LD) conditions. Chilling at 6 or 9 8C for about 1000 h was required for dormancy release and growth resumption. The investigation also confirmed that at higher temperatures (15–21 8C) short photoperiods have no dormancy-inducing effect in these plants.
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Since several genera of the Pomoidae subfamily within the Rosaceae are known to be insensitive to photoperiod (Wareing, 1956; Nitsch, 1957; Heide and Prestrud, 2005), it is of interest to know how growth and dormancy are controlled in other subfamilies of the Rosaceae such as the Prunoidae. In an early investigations with embryo-cultured peach seedlings (Prunus persica) Lammerts (1943) demonstrated that seedlings kept in 16 or 24-h daylength at high temperature (above 21 8C) grew continuously, while their growth was arrested or strongly reduced in 8-h or natural winter SD at both low and intermediate temperatures. Similarly, Went (1957) reported that peach seedlings grew continuously in 16-h SD at a 23/ 17 8C day/night temperature while at day lengths of 13 h or less at the same temperature conditions, they ceased growing and became dormant. However, since temperature and photoperiod were not varied systematically in a factorial design, limited conclusion can be drawn from these experiments. In the present paper I present the results of experiments with three Prunus species (cherry and plum) which have been grown at a range of temperatures under both SD and LD conditions. A pronounced interaction of photoperiod and temperature is demonstrated. 2. Materials and methods 2.1. Plant material and cultivation ˚ s phytotron The experiments were performed in the A (608N, 118E) in daylight compartments combined with adjacent growth rooms for photoperiodic manipulation as explained below. The species and cultivars used for the experiments are listed in Table 1. Young seedlings of P. avium and in vitro micropropagated plants of P. cerasus and P. insititia were obtained from two commercial nurseries. The plants had been transferred to soil and grown in 4 cm plug trays for about 4 weeks to a height of 4–5 cm before delivery. When received, the plants were transplanted into 10 cm plastic pots containing a peat-based potting compost (84% peat, 10% fine sand and 6% clay), and grown at 21 8C in 24-h photoperiod for 1 week before the experimental treatments began. The plants were fertilized twice weekly with a complete fertilizer solution and otherwise watered with tap water as required. All plants received natural spring and summer daylight for 10 h per day (08:00–18:00 h). Whenever the photosynthetic photon flux (PPF) in the daylight compartments fell below about 150 mmol m2 s1 on cloudy days, an additional 125 mmol m2 s1 quanta was automati-
cally added. Daylength extension to 24-h photoperiod was provided by low-intensity light from 75-W incandescent lamps (about 6 mmol m2 s1 PPF). Plants receiving SD treatments were kept in darkness from 18:00 to 08:00 h. The additional light from the daylength extension treatment amounted to only 2% of the total daily radiation, the plants thus received nearly the same daily light integral in both daylengths. Temperatures were controlled to 1.0 8C and a water vapour pressure deficit of 530 Pa was maintained at all temperatures. Three experiments were carried out during the years 2004– 2006. Experiment 1 examined the elongation growth of ‘Gisela 5’ sour cherry and ‘Weito’ plum rootstocks at constant 9, 12, 15 and 21 8C and photoperiods of 10 and 24 h. The experiment was started on April 24, 2003 and lasted for 8 weeks. Plants whose growth had ceased at 9 8C were then transferred to 21 8C and 24-h LD for another 4 weeks in order to establish whether they were truly dormant. Experiment 2 was designed to test the effect of transferring actively growing plants of ‘Weiroot’ sour cherry and ‘St. Julien A’ plum rootstocks from 21 8C (10 h SD and 24 h LD) to 9 8C without change of photoperiod. The experiment was started on May 30, 2005 and lasted for 6 weeks. Experiment 3 examined the elongation growth of wild-growing sweet cherry seedlings at constant 9, 12, 15 and 21 8C and photoperiods of 10 and 24 h. An extra set of plants was transferred from 21 to 9 8C after 3 weeks of active growth. The experiment was started on May 4, 2006 and lasted for 8 weeks. 2.2. Experimental design and measurements The experiments were factorial with a split plot design with temperatures as main plots and with photoperiods and species/ cultivars as sub-plots. Each treatment included ten plants of each species/cultivar. Elongation growth was monitored by weekly measurements of plant heights. These observations provided accurate information of growth rates and the time of growth cessation. Production of new leaves (nodes) was determined by marking the last developed leaf (>2 cm) of each plant at start of the experiments and counting additional leaves at various times during the experiments. Analysis of variance (ANOVA) of the data obtained after 6–8 weeks of cultivation was performed using the Systat Version 5.0 program package. Since the experiments were not replicated in time, the main effects of treatments and species, and their interactions, were tested against their respective two- and three-factor interactions.
Table 1 Identity and origin of the Prunus species and cultivars used for the experiments Species
Cultivar
Origin
Characterization
P. P. P. P. P.
‘Gisela 5’ ‘Weiroot’ ‘St. Julien A’ ‘Weito’
Giessen, Germany Weihenstephan, Germany East Malling, UK Weihenstephan, Germany Vestby, Norway (598300 N)
Commersial rootstock Commersial rootstock Commersial rootstock Commersial rootstock Wild-growing trees
cerasus (Sour cherry) cerasus (Sour cherry) insititia (Plum) insititia (Plum) avium (Sweet cherry)
For further information on the plum and cherry rootstocks, see Rom and Carlson (1987).
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3. Results 3.1. Experiment 1 Both temperature and daylength had a highly significant effect (P < 0.001) on elongation growth of both the plum and the sour cherry cultivars (Fig. 1). However, the daylength effect varied with the temperature, yielding a highly significant interaction between the two environmental factors. Thus, in ‘Weito’ plum plants growth cessation occurred in both SD and LD at 9 8C, at 12 8C in SD only, while at 15 and 21 8C growth continued in both daylengths although at a lower rate in SD, especially at 15 8C. The more vigorous-growing ‘Gisela 5’sour cherry was less sensitive to low temperature and more sensitive to short photoperiods than was ‘Weito’. Thus, no growth cessation took place under LD conditions in ‘Gisela 5’ plants even at 9 8C. While continuous growth was maintained in both daylengths at 21 8C, growth cessation occurred in SD conditions at all lower temperatures in this cultivar, the rate of response increasing with decreasing temperature (Fig. 1). Thus, at 9 8C growth cessation took place after 3 weeks in SD, at 12 and 15 8C not until 7 weeks of cultivation. These results yielded a highly significant three-factor interaction on elongation growth of temperature, daylength and cultivar (P < 0.001). Leaf formation increased more or less linearily with increasing temperature in both species. The main effect of photoperiod was also significant (P < 0.05), and again with a highly significant interaction with temperature (P < 0.01). Thus, in both cultivars there was no significant effect of photoperiod on leaf formation at 21 8C, whereas growth cessation in SD at lower temperatures was accompanied by markedly reduced leaf numbers (Fig. 2). The photoperiodic effect on elongation growth at high temperature (21 8C) was thus an effect of internode length only, as the initiation of new nodes was unaffected by daylength at this temperature.
Fig. 2. Effects of temperature and photoperiod on the formation of new leaves in the plum cultivar ‘Weito’ and the sour cherry cultivar ‘Gisela 5’. Filled columns represent 10-h SD and open columns 24-h LD conditions. Values are means standard errors for 10 plants in each treatment as recorded after 7 weeks of growth at the respective conditions.
‘Weito’ plants held at 9 8C formed winter buds and gradually developed autumn colours under both SD and LD conditions. In ‘Gisela 5’ this happened under SD conditions only. When these plants were transferred to high temperature (21 8C) and LD after 8 weeks of treatment, the plants remained dormant with no resumption of growth within 4 weeks, after which time the experiment was terminated. This test was performed on plants gown at 9 8C only. 3.2. Experiment 2 The interaction of temperature and daylength was confirmed in another pair of plum and sour cherry cultivars (Fig. 3). Both cultivars grew at constant rate at 21 8C in both SD and LD,
Fig. 1. Time course of elongation growth of the plum cultivar ‘Weito’ and the sour cherry cultivar ‘Gisela 5’ grown under different temperature and photoperiod regimes as indicated. Values are means standard errors for 10 plants in each treatment group.
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Fig. 3. Time course of elongation growth of the sour cherry cultivar ‘Weiroot’ and the plum cultivar ‘St. Julien A’ grown continuously at 21 8C in 10-h SD (filled symbols) and 24-h LD (open symbols), and after transfer to 9 8C under the same daylength conditions at the time indicated by arrows. Values are means standard errors for 10 plants in each treatment.
although at a slower rate in SD conditions. This effect of daylength was solely due to increased internode length in LD, as the average number of new leaves produced was the same in both daylengths (20.3 and 20.1 for ‘St. Julien A’; 18.2 and 18.4 for ‘Weiroot’ in LD and SD, respectively after 6 weeks of growth). When plants were transferred from 21 to 9 8C after 3 weeks of active growth, they immediately ceased growing in both daylengths, so that after 1 week no further growth took place in either cultivar (Fig. 3).
Fig. 4. Time course of elongation growth of seedlings of wild-growing sweet cherry grown under different temperature and photoperiod regimes as indicated. Arrows indicate time of transfer to 9 8C. Values are means standard errors for 10 plants in each treatment group.
3.3. Experiment 3 The sweet cherry seedlings grew vigorously and reached a height of nearly 1 m after 8 weeks at 21 8C and LD (Fig. 4). They also showed a somewhat different response to temperature and photoperiod than did the plum and sour cherry plants in the previous experiments. Thus, although SD reduced growth by reducing internode length at all temperatures also in this species, growth cessation in SD took place at 9 8C only. Like the ‘Gisela 5’ sour cherry, this species did not cease growing in LD at such low temperature, but continued a slow growth after a pause in growth during weeks 3 and 4. Such slow growth in LD was also maintained in about 50% of the plants after transfer from 21 to 9 8C after 3 weeks, whereas all plants in SD ceased growing within 1 week from transfer (Fig. 4), and subsequently formed winter buds. Although no growth cessation took place in SD at temperatures above 9 8C, stem elongation was strongly reduced in SD at these higher temperatures in this species in comparison to growth under LD conditions. The reduced elongation in SD was associated with a significant reduction in leaf numbers (Fig. 5). Therefore, reduced growth in SD in this species was
Fig. 5. Effects of temperature and photoperiod on the formation of new leaves of sweet cherry seedlings. Filled columns represent 10-h SD and open columns 24-h LD conditions. Values are means standard errors for 10 plants in each treatment group as recorded after 7 weeks of growth at the respective conditions.
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due to the combined effect of reduction in both internode length and numbers. 4. Discussion The results of these experiments demonstrate a pronounced interaction of photoperiod and temperature in the regulation of growth and growth cessation in all the tested Prunus species. At high temperature (21 8C) they responded with continuous growth regardless of photoperiodic conditions in much the same way as Malus and Pyrus (Nitsch, 1957; Heide and Prestrud, 2005). However, unlike these genera, most of the Prunus species were clearly sensitive to daylength at intermediate temperatures (12 and 15 8C), and ceased growing after a few weeks in SD conditions (Figs. 1 and 3). At low temperature (9 8C) on the other hand, the Prunus species varied in their response to photoperiod. While the wild sweet cherry and the sour cherry ‘Gisela 5’ required the combination of low temperature and SD for growth cessation and formation of winter buds, the other Prunus cultivars ceased growing and formed winter buds at 9 8C in both SD and LD conditions in much the same way as Malus and Pyrus (Figs. 1 and 3). Such photoperiod temperature interactions are well known in the control of flowering (Thomas and Vince-Prue, 1997), and the molecular mechanisms controlling such interactions are now beginning to be understood (Halliday et al., 2003; Benedict et al., 2006). It has also recently been demonstrated that, in aspen trees, the same molecular mechanisms control SD induction of both flowering and growth cessation (Bo¨hlenius et al., 2006). Although the present investigation was not intended to study such molecular transduction processes, the results provide circumstantial evidence for temperature ‘‘gating’’ of phytochrome controlled photoperiodic processes as suggested by Halliday et al. (2003). Dormancy is a quantitative condition that is gradually attained and overcome. It has been demonstrated in both conifers (Heide, 1974) and deciduous trees (Junttila, 1976) that during early stages of SD-induced growth cessation, a shift back to LD is all that is needed for growth resumption. Even with as many as 32 SD cycles, growth resumption took place in subsequent LD in Salix (Junttila, 1976). Furthermore, buds at different positions on the annual shoot often exhibit different dormancy states. For these reasons a precise time of dormancy attainment cannot be determined. However, after growth cessation, the Prunus species formed terminal winter buds, and a relatively deep state of dormancy was demonstrated after 8 weeks of low temperature treatment in Exp. 1, in much the same way as previously demonstrated for Malus, which under the same conditions required about 1000 h of chilling for growth resumption (Heide and Prestrud, 2005). There is thus little doubt that the described growth cessation in the Prunus species also led to bud dormancy. The pronounced interaction of photoperiod and temperature that was demonstrated in the Prunus species, suggests that these species actually have a dual dormancy induction control system, securing timely growth cessation and
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dormancy induction in response to the progressive lowering of daylength and temperature in the autumn. Thus, under unusually mild autumn conditions the Prunus species will still be induced to growth cessation by the rapidly decreasing photoperiod around fall equinox. Such a dual control mechanism would make these species especially well adapted to avoiding the possible negative effects on winter bud preparations by the predicted and ongoing global warming (Serreze et al., 2000). An exception to this behaviour was seen in P. avium, which maintained an active (but reduced) growth in SD at intermediate temperatures and ceased growth in SD at low (9 8C) temperature only. A similar temperature photoperiod interaction was reported for raspberry (Rubus idaeus), another member of the Rosaceae (Williams, 1959). Thus, raspberry plants grew continuously in both 9 and 14-h photoperiod at 21 8C, at 10 8C they ceased growing in both daylengths, whereas at 15 8C growth cessation took place in SD only. Nestby (1986) demonstrated that even under natural continuous light conditions at high latitudes, raspberry plants ceased growing and became dormant at low summer temperatures of about 10 8C. Growth cessation and dormancy induction by low temperature thus seems to be rather widespread within the Rosaceae. However, in Prunus species the photoperiodic response is highly temperature dependent, and the transition temperatures for shifts in the photoperiodic response mode vary among species and cultivars. Acknowledgement I am grateful to Gartnerhallen’s Elite Plant Station, Sauherad, Norway and Bla˚dike Tree Nurseries, Vestby, Norway for the gift of the micropropagated plants and the Prunus avium seedlings, respectively. References Battey, N.H., 2000. Aspects of seasonality. J. Exp. Bot. 51, 1769–1780. Benedict, C., Geisler, M., Trygg, J., Huner, N., Hurry, V., 2006. Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol. 141, 1219–1232. Bo¨hlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H., Nilsson, O., 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040– 1043. Downs, R.J., Borthwick, H.A., 1956. Effect of photoperiod on growth of trees. Bot. Gaz. 117, 310–326. Garner, W.W., Allard, H.A., 1923. Further studies in photoperiodism, the response of the plant to relative length of day and night. J. Agric. Res. 23, 871–920. Ha˚bjørg, A., 1978. Photoperiodic ecotypes in Scandinavian trees and shrubs. Meld. Nor. Landbrukshøgsk. 57 (33), 1–20. Halliday, K.J., Salter, M.G., Thingnaes, E., Whitelam, C.G., 2003. Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J. 33, 875–885. Heide, O.M., 1974. Growth and dormancy in Norway spruce (Picea abies). I. Interaction of photoperiod and temperature. Physiol. Plant 30, 1–12. Heide, O.M., Prestrud, A.K., 2005. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol. 25, 109–114.
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Junttila, O., 1976. Apical growth cessation and shoot tip abortion in Salix. Physiol. Plant 38, 278–286. Junttila, O., Nilsen, J., Igeland, B., 2003. Effect of temperature on the induction of bud dormancy in ecotypes of Betula pubescens and Betula pendula. Scand. J. For. Res. 18, 208–217. Kramer, P.J., 1936. Effect of variation in length of day on growth and dormancy of trees. Plant Physiol. 11, 127–137. Lammerts, W.E., 1943. Effect of photoperiod and temperature on growth of embryo-cultured peach seedlings. Am. J. Bot. 30, 707–711. Nestby, R., 1986. Red raspberry growth variation of selections and cultivars, at different northern latitudes in the year of planting. Acta Hort. 183, 191–198. Nitsch, J.P., 1957. Photoperiodism in woody plants. Proc. Am. Soc. Hort. Sci. 70, 526–544.
Rom, R.C., Carlson, R.F., 1987. Rootstocks for Fruit Crops. John Wiley and Sons, New York, 494 pp. Serreze, M.C., Walsch, J.E., Chapin III, F.C., et al., 2000. Observational evidence of recent change in the northern high-latitude environment. Clim. Change 46, 159–207. Thomas, B., Vince-Prue, D., 1997. Photoperiodism in Plants, second ed. Academic Press, London, 428 pp. Wareing, P.J., 1956. Photoperiodism in woody plants. Annu. Rev. Plant Physiol. 7, 191–214. Went, F.W., 1957. The Experimental Control of Plant Growth. Chapter 12. The Ronald Press Company, New York. Williams, I.H., 1959. Effects of environment on Rubus idaeus L. III. Growth and dormancy of young shoots. J. Hort. Sci. 34, 210–218.