Planta

Planta (1990)182:455~460

9 Springer-Verlag 1990

Relationships between circadian rhythm of chilling resistance and acclimation to chilling in cotton seedlings Kelcey D. McMillan and Arnon Rikin* Department of Botanyand Microbiology,Oklahoma State University, Stillwater,OK 74078, USA Received 20 February; accepted 30 May 1990

Abstract. Cotton (Gossypium hirsutum L. cv. Deltapine 50) seedlings grown under light-dark cycles of 12:12 h at 35 ~ C showed rhythmic daily changes in chilling resistance. Chilling treatment (5~ C, 48 h) started at the beginning or middle of the daily light period resulted in a substantial growth inhibition of the seedlings upon return to 35~ whereas when chilling was started at the beginning or middle of the dark period the subsequent growth of the seedlings was much less inhibited. This rhythm in chilling resistance persisted under continuous light for three 24-h periods, indicating that it is of an endogenous nature. Seedlings grown under continuous light from germination showed no daily changes in resistance, but a rhythm was initiated by introduction of a dark period of 6 h or longer. In 24-h cycles with different light and dark periods, maximal resistance was reached just before the start of dark period. Seedlings grown at 35~ C could be acclimated to chilling by exposure to low, non-damaging temperatures (25-15 ~ C). A short-term (6 h) exposure to 25~ C started at the resistant phase resulted in a large increase in resistance during the following otherwise sensitive phase. The resistance induced by the low temperature matched or slightly exceeded the maximal resistance reached during the resistant phase of the daily rhythm of chilling. The low-temperature-induced resistance and the daily rhythmic increase in resistance were not additive, indicating a common mechanism for the two kinds of resistances. An adaptive advantage of a combination of a rapid temperature-induced acclimation and the daily rhythmic increase in resistance is suggested. Key words: Acclimation (chilling) - Chilling (acclimation, resistance) - Gossypium (chilling) - Light-dark cycle (chilling resistance) Rhythm (chilling resistance)

Introduction Many plant species possess the ability to acquire resistance to low, non-freezing (chilling) and freezing temper* To whom correspondenceshould be addressed

Abbreviations: D = dark; L = light; LDC = light-dark cycleof 24 h

atures. Acclimation to low temperatures is induced by environmental factors, especially low, non-damaging temperatures (Graham and Patterson 1982; Levitt 1980). Various species widely differ in the degree of resistance that they can develop, and in the time needed to achieve this resistance. For instance, species such as Gossypium hirsutum and Phaseolus vulgaris are able to achieve a substantial level of chilling resistance (Guinn 1971; Wilson and Crawford 1974a, b) while Episcia reptans has very low or no ability to develop resistance (Wilson and Crawford 1974a, b). The length of time required for acclimation depends on the species, the physiological state of the plant, and the temperature to which the plant is chilled. In many chilling-sensitive species several hours of acclimation are sufficient to achieve a high level of resistance. For instance, in Lycopersicon esculentum cv. Rutgers grown at 25 ~ C, acclimation at 12.5~ C for 3 6 h increases resistance to chilling at 1~ for 48 h (Wheaton and Morris 1967). In Arabidopsis thaliana L. the acclimation to freezing temperatures requires one day of exposure to a temperature of 4 ~ C to increase freeezing resistance (Gilmour et al. 1988; Kurkela et al. 1988; Lang et al. 1989). On the other hand, acclimation of woody species to freezing temperatures usually requires several weeks (Levitt 1980). Light can also determine the degree of resistance in chilling-sensitive plants. In cotton seedlings grown under continuous light, chilling resistance increases with increased irradiance and decreases upon transfer to darkness. Addition of sucrose to the seedlings in the dark period prevents the effect of darkness, while application of the photosynthetic inhibitor DCMU (3-(3,4-dichlorophenyl)-l,l-dimethylurea) in light has the same effect as darkness (Rikin et al. 1981). These results indicate that a light-dependent photosynthetic product is essential for development and maintenance of chilling resistance. The chilling resistance of tomato and several other chilling-sensitive species is regulated by the daily lightdark cycles (LDCs). Seedlings grown under LDCs of 9 h L: 15 h D acquire resistance during the light period, remain resistant during the first part of the dark period, and are least resistant at the end of the latter (King et al. 1982). The development of resistance during the

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K.D. McMillan and A. Rikin: Rhythmic chilling resistance and chill-acclimation in cotton

light period is accompanied by carbohydrate accumulation, and its decrease at the end of the dark period by carbohydrate depletion (King et al. 1988). The regulation of chilling resistance by L D C s is probably modulated by photosynthetic production of carbohydrates (King et al. 1988). Water stress contributes to the relative severity of the injury during different phases of the L D C , but water deficiency during or following chilling is not the primary cause for the daily differences in chilling resistance (King and Reid 1987). The goal of the present study was to characterize the rhythmic chilling resistance further, especially its possible endogenous nature and the light conditions for its entrainment. We also examined the relationships between short-term acclimation by low temperatures and the daily changes in chilling resistance.

Material

and methods

Plant material and growth conditions. Cotton seeds (Gossyphtm hirsuture L. cv. Deltapine 50, obtained from Delta and Pine Land Co., Scott, Miss., USA; harvested in 1987) were sown in plastic pots (10 cm diameter, 8.5 cm high) filled with a mixture of peat and vermiculite (Terra-Lite, Redi-Earth; W.R. Grace & Co., Cambridge, Mass., USA). Four days from sowing, seedlings were thinned to three per pot. They were grown in growth chambers at 35~ for 9 LDCs of 12:12 h. The light (250 gmol-m-2.s -1) source was a combination of fluorescent (F48T18-CW-VHO; Sylvania, Danvers, Mass., USA) and incandescent lamps. The seedlings were fertilized 4 d after germination with 60 ml of i g/1 20N20P-20K soluble fertilizer (Peters; W.R. Grace & Co.) and irrigated as needed with water. Chilling conditions, evaluation of chilling resistance and chill-acclimation. All experiments, both on variations in chilling resistance and on chilling acclimation, were done with seedlings grown at 35~ for 9 LDCs of 12:12 h. Chilling treatment was given by exposing the seedlings for 48 h to 5~ at 85% RH under the same light conditions as in their previous growth. After chilling, the seedlings were returned to 35~ C for 7 LDCs of 12:12 h and at the end of this period chilling resistance was evaluated by measuring the fresh weight of the shoot above the cotyledons. Deviations from this schedule will be specified in the particular experiments. For inducing acclimation, seedlings were transferred to lower temperatures, as specified for each experiment. In most experiments an acclimating temperature of 25~ was used; it was chosen because it was the highest one still effective in inducing substantial acclimation. In all experiments, each treatment was conducted with at least nine seedlings in three pots. The results shown are the mean _+ SE. Each experiment was repeated at least three times.

Results

Daily rhythmic changes in chilling resistance Characteristics of the chilling resistance rhythm in seedlings grown at 35 ~ C. Cotton seedlings grown in L D C s of 12:12 h underwent rhythmic changes in their chilling resistance when exposed to 48 h o f chilling (5 ~ C under the regular 12:12 h LDCs) at 6-h intervals during the LDCs, and then returned to the standard temperature

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Fig. IA-C. Rhythmic resistance of cotton seedlings to chilling. Seedlings were grown at 35~ C for 9 LDCs of 12 h D:12 h L from sowing (A). At the end of the 9th LDC one group of seedlings was transferred to continuous light (B) and one group was transferred to continuous darkness (C). Then, for 72 h at 6-h intervals seedlings were exposed to chilling, e, Non-chilled; A, chilled; n, light period; m, dark period (35 ~ C) for 7 LDCs. The seedlings were most sensitive when chilling had started 6 h after the beginning of the light period. They acquired resistance at the end of the light period, stayed resistant during the first half of the dark period, and showed declining resistance during the rest of the latter (Fig. 1 A). When exposed to chilling the seedlings had only two developed cotyledons and just initiations of true leaves. The degree of resistance was evaluated by measuring the growth o f the true leaves after 7 d at the standard temperature (35 ~ C) following the chilling treatment (5 ~ C/48 h). At the end of the chilling treatment, no visual s y m p t o m s were observed on the true leaves initiated at any treatment but cotyledons of seedling exposed to chilling starting at the sensitive phase looked more wilted than those exposed to chilling starting at the resistant phase. When chilling was started at the resistant phase of the L D C the seedlings resumed vigorous growth when returned to 35 ~ C and completed their life cycle. In contrast, when chilling was started at the sensitive phase the seedlings grew only slightly when returned to 3 5 ~ and most o f them ultimately wilted and died. In order to find out whether the daily changes o f chilling resistance were determined by the immediate

K.D. McMillan and A. Rikin: Rhythmic chilling resistance and chill-acclimationin cotton light conditions or involved an endogenous control, seedlings grown under LDCs of 12:12 h were transferred for 72 h to continuous light and exposed to chilling (5 ~ C under continuous light) at 6-h intervals. The changes in resistance persisted under continuous light for the 3-d period during which the plants were observed (Fig. 1 B). The maximal and minimal phases of resistance under the first 48 h of continuous light corresponded to those under the regular 12:12-h LDCs, but after 48 h, the period of the rhythm is probably longer than 24 h, as indicated by the 30-h interval between the beginning of the resistant phase on the second day and its beginning on the third day (Fig. 1 B). Transfer of seedlings grown under 12:12-h LDCs to continuous darkness resulted in a general decrease in chilling resistance (Fig. 1 C). Because of the decreased resistance, with only low peaks apparent, it was not possible to determine the period of the rhythm under continuous darkness precisely. During the first 24 h of darkness the resistant phase corresponded to that which occurred under the regular LCDs of 12" 12 h, but the degree of resistance was much lower. After longer periods in darkness the rhythm seemed to decrease from 24 to 12 h. On the third day in darkness no resistant phase could be observed and the seedlings remained uniformly sensitive. However, continuous darkness also caused pronounced growth inhibition in control seedlings not exposed to chilling (Fig. 1 C).

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Entrainment of the chilling-resistance rhythm by different LD Cs. Seedlings grown under continuous light from germination onwards showed no daily changes of chilling resistance (Fig. 2A), but transfer to three LDCs with various combination of light and dark periods established a daily rhythmicity of chilling resistance (Fig. 2 B, C, D). An LDC of 18 h L:6 h D caused a small degree of resistance (Fig. 2B) while LDCs with longer dark periods of 12 h (Fig. 2C) or 18 h (Fig. 2D) resulted in larger degree. Under all LDCs tried, the resistant phase began at the end of the light period, while minimal resistance occurred 18 h after the beginning of the dark period. Therefore, in LDCs of 18 h L:6 h D minimal resistance occurred 12 h after the beginning of the light period (Fig. 2B), under LDCs of 12:12 h 6 h after the beginning of the light period (Fig. 2C) and under LDCs of 6 h L: 18 h D it occurred just at the beginning of the light period (Fig. 2D). Chili-acclimation in relation to the daily changes in chilling resistance Chill-acclimation by temperature. It has been known that cotton seedlings acquire chilling resistance when transferred from the standard growth temperature to a lower acclimating temperature (Guinn 1971; Wilson and Crawford 1974b). To analyze this response further seedlings grown at 35~ were given 48-h periods at 30 ~ 25 ~ 20 ~ 15 ~ and 10~ for 48 h before exposure to a chilling treatment (5 ~ C/48 h); the transfer was made 6 h after the beginning of the light period, i.e., at the sensitive phase of the LDC (Fig. 3 A). Transfer to 30 ~ 25 ~

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Fig. 2 A-D. Entrainment of daily changes in the resistance of cotton seedlings to chilling by LDCs with different light and dark periods. Seedlings were grown at 35~ C for 6 d under continuous light from sowing (A). Then, seedlingswere transferred to 3 LDCs with different light and dark periods: 18 h L:6h D (B), 12:12h (C) and 6 h L:I8 h D (D). At the end of the third LDC, for 24 h, at 6-h intervals seedlingswere exposed to chilling. Symbols as in Fig. 1

20 ~ and 15~ C by itself, i.e. with no subsequent chilling treatment, slightly reduced the subsequent growth the seedlings when these were returned to 35 ~ C, while transfer to 10~ C was more damaging and inhibited subsequent growth by 60%. When, following the low-temperature treatments, the seedlings were given 48 h at 5~ C their resistance to this chilling treatment was found to be increased, i.e. they had become acclimated to chilling. Transfer to 20 ~ C was the most effective in inducing chilling resistance relative to seedlings maintained at 35~ throughout, as evaluated by subsequent shoot growth after returning to 35 ~ C. Chilling resistance was also increased by 48 h at 25 ~ and 15~ C but only slightly by transfer to 30 ~ and 10 ~ C (Fig. 3A). When the 48-h low-temperature treatments at 30 ~ 25 ~ 20 ~ 15~ and 10~ were started not 6 h after the beginning but at the end of the light period, i.e. in the resistant phase of the LDC, the seedling response was different (Fig. 3B). Firstly, transfer from 35 ~ to 10~ C

458

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Fig. 4. Long-term acclimation of cotton seedlings to chilling by low temperature. Chill-acclimation began by transfer to 25~ C and at 12-h intervals seedlings were exposed to chilling, e, Non-chilled; zx, chilled, acclimated; n, light period; B, dark period

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Fig. 3A, B. Acclimation of cotton seedlings to chilling by various low temperatures and as affected by the time in the LDC when acclimation began. Six h after the beginning of the light period (A), and at the end of the light period, seedlings were transferred and kept at 10~ 15~ 20~ 25~ and 30~ C for 48 h. Then, seedlings were exposed to chilling starting 6 h after the beginning of (A) and at the end (B) of the light period. Open bars = after acclimation before chilling; hatched bars = non-chilled; solid bars = chilled

did not result in substantial subsequent growth inhibition after the seedlings were returned to 35 ~ C. Secondly, the beginning of the chilling exposure coincided with the resistant phase. Under such conditions the potential acclimating effects of the low temperatures cannot be detected since the chilling resistance was initially high in seedlings maintained at 35 ~ C (Fig. 3 B).

Time course o f chill-acclimation. Seedlings grown at 3 5 ~ and transferred to 2 5 ~ had acquired maximal resistance to 48 h chilling at 5 ~ already after 12 h (Fig. 4). Maintaining them at 2 5 ~ for an additional 60 h did not result in a further increase of resistance (Fig. 4). Determining the exact length of time required for chill-acclimation by low temperature is complicated by the fact that the daily changes in the resistance m a y interfere with the resistance induced by the acclimating temperature. Transfer of seedlings to 25 ~ C at the beginning o f the light period for 6 h did not result in increased chilling resistance. A longer time at 25 ~ C coincided with the daily resistant phase which continued up to the middle of the dark period. When, towards the end of the dark period, the resistant phase came to its end, the resistance of the seedlings acclimated by low temperature remained high (Fig. 5). Thus, under such conditions 6 h at 25 ~ C are not sufficient to induce resistance whereas 18 h and longer are, but under these conditions it cannot be determined which period between 6 and 18 h at 25 ~ C

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Fig. 5. Acclimation of cotton seedlings to chilling by low temperature as affected by the time in the LDC when acclimation began. Chill-acclimation was started by transfer of seedlings to 25~ C either at the beginning of the light period or 6 h after the beginning of the dark period. At 6-h intervals from the beginning of the respective acclimation treatment and for a total of 24 h, seedlings were exposed to chilling. Arrows indicate the time when seedlings were transferred to 25~ C. e, Non-chilled; A, chilled; zx, chilled, acclimated; [], light period; B, dark period

is enough to induce resistance. However, this can be done by transfer of seedlings to 25 ~ C starting at the middle of the dark period since after 6-12 h at 2 5 ~ the seedlings have reached the sensitive phase. U n d e r these conditions, a period o f 6 h at 25 ~ C was actually found to be sufficient to induce resistance (Fig. 5).

Time-course of chilling damage. When acclimated and non-acclimated seedlings were exposed to increasing lengths of chilling temperature (5 ~ C) starting 6 h after the beginning of the light period, i.e. in the sensitive phase of the L D C , it became evident that after 2 or 3 d of chilling that the acclimated seedlings were much more resistant than the non-acclimated ones, although after 4 d o f chilling growth in both kinds of seedlings was severely inhibited (Fig. 6A). When the exposure to chilling was started during the end of the light period, i.e. in the resistant phase of the L D C , the resistance of the acclimated seedlings was only slightly higher than that of the non-acclimated ones. Increasing the time o f chilling from 2 to 4 d resulted in increased growth inhibi-

K.D. McMillanand A. Rikin: Rhythmicchillingresistanceand chill-acclimationin cotton

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I ! 3 4 Chilling exposure (d) Fig. 6A, B. Response of non-acclimated and acclimated cotton seedlings to chilling started at the phase of minimal or maximal resistance. Chill-acclimationwas achieved by transfer of seedlings to 25~ C for 24 h. Then, seedlingswere exposed to chillingstarting 6 h after the beginningof (A) and at the end of (B) the light period. A, Chilled;zx, chilled,acclimated

tion in both non-acclimated and acclimated seedlings, and after 5 d of chilling the growth of both kinds of seedlings was greatly inhibited (Fig. 6 B).

Discussion

Daily changes of chilling resistance have been demonstrated in several plant species such as tomato, mung bean, bell pepper, corn and eggplant (King et al. /982). We now show that in cotton seedlings these daily resistance changes are at least partially controlled by an endogenous rhythm since in seedlings grown under LDCs of 12:12 h it persists in continuous light for at least three cycles. After two cycles in darkness the rhythm disappears and the seedlings are chilling-sensitive all the time. This disappearance of the resistant phase under continuous darkness is probably a consequence of the known need for light energy and photosynthetic products in order to develop chilling resistance (King et al. 1988; Rikin etal. /981). Under a 12:12h LDC the rhythm is characterized by a period of 24 h; the sensitive phase occurs in the light period and the resistant phase in the dark period. The degree of chilling damage depends on the time in the LDC when the treatment begins, although chilling exposure longer than one LDC is required to inflict substantial growth inhibition. Since the sensitive or resistant phase of the LDC is shorter than the time needed to achieve chilling damage, seedlings exposed to chilling at the sensitive phase would pass through the resistant phase before chilling damage is observed, and seedlings exposed to chilling at the resistant phase would pass through the sensitive phase. Such a situation is expected to eliminate any observed daily changes in chilling resis-

459

tance and to result in a uniform response to chilling started at any time during the LDC. One possible explanation for the daily changes in chilling resistance is that the sensitive or resistant phase may become unchangeable upon exposure to chilling. Accordingly, seedlings exposed to chilling starting at the sensitive phase would remain permanently sensitive and ultimately would be damaged while seedlings exposed to chilling starting at the resistant phase would remain permanently resistant. Another possible explanation is that upon chilling exposure started at the sensitive phase, a fast and irreversible change occurs in the cells. This initial and crucial change would develop into chilling damage only after an additional 1-2 d of chilling. There are other examples of plant responses to external factors that are longer than one LDC but are dependent on the time of the beginning of the exposure. Cotton seedlings show daily changes in their resistance to several herbicides although the differential injury symptoms do not appear until after more than one LDC from herbicide application (Rikin et al. 1984b), In bean seedlings, treatment with exogenous ethylene stimulates ethylene production, the degree of ethylene stimulation by ethylene treatment depending on the time in the LDC when treatment begins, and the differential ethylene production lasting more than one LDC (Rikin and Anderson 1990). The daily changes of chilling resistance are not expressed when seedlings are grown, from germination onwards, under continuous light. The rhythm is entrained by exposing them to LDCs. A dark period of 6 h is sufficient to establish a rhythm with a small degree of resistance; longer dark periods result in a higher degree of resistance. Under all LDCs with different lengths of the dark period which we tried the resistant phase was set to begin at the end of the light period. This timing of the resistant phase may be assumed to have an adaptive significance; it may protect chilling-sensitive plants from chilling that starts during the evening and first part of the night. Since the rhythm is endogenously controlled, the resistant phase will always occur at the end of the day, irrespective of day-to-day variations of irradiation caused by sunny or cloudy days. The protection is further enhanced by the chill-acclimation that is induced by the low temperatures of the night. By the end of the light period cotton seedlings grown under 35~ C can withstand temperatures down to 10~ These low temperatures in turn acclimate the seedlings to still lower temperatures which may occur later during the otherwise sensitive phase. The time required to achieve the temperature-induced resistance to 5~ C approximates the length of the resistant phase. Thus, the combination of an endogenously controlled resistant phase at the end of the day and a fast acclimation process induced by low temperatures provides the chilling-sensitive plant with means to cope with and survive chilling temperatures that begin at the end of the day or the beginning of the night and may reach their lowest level around morning. This would be another example where an endogenous rhythm ensures the initiation of preparation to survive an environmental stress. So far, this has been known for the acclimation of woody plants to freezing. This

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K.D. McMillan and A. Rikin: Rhythmic chilling resistance and chill-acclimation in cotton

acclimation, in several species, starts in the fall independently of temperature or photoperiod (Siminovitch 1982). Several daily rhythms have been found previously in cotton seedlings (Rikin et al. 1984a, b, 1985), including leaf movement from a horizontal position in the day to a vertical position at night, and resistance to the herbicide bentazon, which is high during the day and low during the night. The chilling-resistant and the chilling-sensitive phases coincide mainly with leaves in the vertical and horizontal positions, respectively. However, as the pattern of daily resistance to the herbicide bentazon shows an inverse correlation to the daily chilling resistance a c o m m o n resistance mechanism for the daily resistances to this herbicide and to chilling is unlikely. It has been proposed that a light-dependent photosynthetic product is needed to develop and maintain chilling resistance (King et al. 1988; Rikin et al. 1981). However, when grown under LDCs with dark periods of 12 h or shorter, cotton seedlings reach their lowest degree of resistance during the light period, when photosynthetic products should be most abundant. Only under LDCs with longer dark periods, namely, 18 h D in the present work and 15 h in the work of King et al. (1982), the beginning of the daily increase of chilling resistance coincides with the beginning of the light period. Under continuous light from germination on the seedlings showed no daily changes in chilling resistance and the degree of resistance was always high. Taken together these findings indicate that the observed degree of chilling resistance at a given time may be determined by the relative contributions of a photosynthetic material which is a product of the immediate light conditions, and by the phase of the endogenous rhythm. At certain times during the L D C the immediate light product and the endogenous rhythm may have opposite effects. Thus, under an LDC of 12:12 h, photosynthetic products are probably most abundant 6 h after the beginning o f the light period, but the seedlings are least resistant at this time. Acclimated cotton seedlings show no daily changes of chilling resistance because the sensitive phase is eliminated. Several observations indicate that acclimation to chilling by low temperatures and the daily development of chilling resistance are induced, at least in part, by a similar mechanism. Firstly, the magnitude of the resistance induced by low-temperature acclimation at the daily sensitive phase is only slightly higher than the maximal daily resistance of non-acclimated seedlings. Secondly, the resistance induced by low-temperature acclimation, and the resistance reached in the daily resistance rhythm are non additive, so that the resistance induced by low-temperature acclimation during the daily resistant phase is only slightly higher than the resistance in the daily high-resistance rhythm alone. Thirdly, the time required to induce resistance by low temperature is similar to the time o f transition from the daily sensitive to the daily resistant phase. Further work is directed at elucidating the possible c o m m o n mechanism of chill-

acclimation by temperature and the daily resistant phase. This work was supported by a U.S. Department of Agriculture Competitive Research Grant No. 89-37264-4814. K.D.M. was supported by an NSF grant for Summer Research Experience for Undergraduates. References

Gilmour, S.J., Hajela, R.K., Thomashow, M.F. (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiol. 87, 740-750 Graham, D., Patterson, B.D. (1982) Responses of plants to low, nonfreezing temperatures: proteins, metabolism and acclimation. Annu. Rev. Plant Physiol. 33, 347-372 Guinn, G. (1971) Chilling injury in cotton seedlings: changes in permeability in cotyledons. Crop Sci. 11, 101-102 King, A.I., Reid, M.S. (1987) Diurnal chilling sensitivity and desiccation in seedlings of tomato. J. Am. Soc. Hortic. Sci. 112, 821 824 King, A.I., Reid, M.S., Patterson, B.D. (1982) Diurnal changes in the chilling sensitivity of seedlings. Plant Physiol. 70, 211 214 King, A.I., Joyce, D.C., Reid, M.S. (1988) Role of carbohydrates in diurnal chilling sensitivity of tomato seedlings. Plant Physiol. 86, 764-768 Kurkela, S., Frank, M., Heino, P., Lang, V., Palva, E.T. (1988) Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Rep. 7, 415-498 Lang, V., Heino, P., Palva, E.T. (1989) Low temperature acclimation and treatment with abscisic acid induce common polypeptides in Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 77, 729-734 Levitt, J. (1980) Responses of plants to environmental stresses. I. chilling, freezing and high temperature stresses. Academic Press, New York Rikin, A., Anderson, J.D. (1990) Rhythmic responses to hormones and herbicides in plants. In: Chronobiology: its role in clinical medicine, general biology, and agriculture, pt. B, pp. 895-903, Hayes, D.K., Pauly, J.E., Reiter, R.J., eds. Wiley-Liss, New York Rikin, A., Gitler, C., Atsmon, D. (1981) Chilling injury in cotton (Gossypium hirsutum L.): light requirement for reduction of injury and for the protective effect of abscisic acid. Plant Cell Physiol. 22, 453-460 Rikin, A., Chalutz, E., Anderson, J.D. (1984a) Rhythmicity in ethylene production in cotton seedlings. Plant Physiol. 75, 493 495 Rikin, A., St. John, J.B., Wergin, W.P., Anderson, J.D. (1984b) Rhythmical changes in the sensitivity of cotton seedlings to herbicides. Plant Physiol. 76, 297-300 Rikin, A., Chalutz, E., Anderson, J.D. (1985) Rhythmicity in cotton seedlings. Rhythmic ethylene production as affected by silver ions and as related to other rhythmic processes. Planta 163, 227-231 Siminovitch, D. (1982) Major acclimation in living bark of 16 September black locust tree trunk sections after five weeks at 10~ C in the dark - evidence for endogenous rhythm in winter hardening. In: Plant cold hardiness and freezing stress mechanisms and crop implications, vol. 2, pp. 117-128, Li, P.H., Sakai, A. eds. Academic Press, London Wheaton, T.A., Morris, L.L. (1967) Modification of chilling sensitivity by temperature conditioning. Proc. Am. Soc. Hortic. Sci. 41, 529-533 Wilson, J.M., Crawford, R.M.M. (1974a) The acclimatization of plants to chilling temperatures in relation to fatty-acid composition of leaf polar lipids. New Phytol. 73, 805-820 Wilson, J.M., Crawford, R.M.M. (1974b) Leaf fatty-acid content in relation to hardening and chilling injury. J. Exp. Bot. 25, 121-131

Relationships between circadian rhythm of chilling resistance and acclimation to chilling in cotton seedlings.

Cotton (Gossypium hirsutum L. cv. Deltapine 50) seedlings grown under light-dark cycles of 12:12h at 35°C showed rhythmic daily changes in chilling re...
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