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Crop Science 41:1006-1011 (2001)
© 2001 Crop Science Society of America

CROP BREEDING, GENETICS & CYTOLOGY

Influence of Vernalization and Photoperiod Responses on Cold Hardiness in Winter Cereals

S. Mahfoozi, A. E. Limin and D. B. Fowler*

Crop Development Centre, Univ. of Saskatchewan, Saskatoon, SK, S7N 5A8, Canada

* Corresponding author (Brian.Fowler{at}usask.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
An understanding of the genetic regulation of low-temperature (LT) tolerance is a prerequisite for the development of cold tolerant cultivars for high stress regions. Vernalization requirement in winter habit cereals and photoperiod responsiveness in spring habit cereals has been shown to influence expression of the LT tolerance genes. The objective of the present study was to determine the influence of photoperiod response on expression of LT tolerance genes in vernalization requiring winter habit cultivars Norstar and Warrior wheat (Triticum aestivum L. em. Thell) and Kold barley (Hordeum vulgare L.). These cultivars were subjected to 8-h-short day (SD) and 20-h-long day (LD) photoperiods at cold acclimating temperature (4°C) over a period of 0 to 98 d. Final leaf number (FLN) was determined at intervals throughout the acclimation period to measure vernalization status. Photoperiod sensitivity did not affect vernalization as both SD and LD plants reached vernalization saturation at the same time. However, a significant increase in leaf number and delayed double ridge formation between 49 and 98 d under 4°C SD non-inductive flowering condition relative to the LD treatments indicated that SD delayed phenological development. Low-temperature tolerance gene expression as measured by LT50 was influenced before the signal for floral transition as indicated by FLN measurements. Photoperiodic response of SD sensitive winter barley and wheat cultivars was reflected in the level of expression of LT tolerance beginning in the early stages of vernalization and plant development. Subsequent LT acclimation continued for a longer time and to colder temperatures under SD compared to LD. These results support the hypothesis that vernalization and photoperiod responses regulate the expression of LT tolerance genes through their influence on the rate of plant development.

Abbreviations: FLN, final leaf number • LD, long day • LT, low-temperature • PP, photoperiod • SD, short-day


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
LOW-TEMPERATURE stress is a major factor limiting plant survival. To properly time flowering and cope with LT stress, winter cereals regulate their development through adaptive mechanisms that are responsive to day length and temperature. Photoperiod and vernalization requirements are the two major mechanisms that control the transition from vegetative to the reproductive phase. Vernalization is defined as the acceleration of the ability to flower by a chilling treatment (Chouard, 1960). On LT exposure, vernalization-requiring plants continue to reduce their FLN up to the point of vernalization saturation (Wang et al., 1995; Berry et al., 1980). Vernalization requirement is critical to winter habit plants as it prevents transition to the reproductive phase in regions with cold winters.

Day length is one of the most important environmental variables that influences the flowering of plants. Length of day affects apical morphogenesis, leaf production, tillering and other developmental processes in cereals (Kirby and Appleyard, 1980). Cereals are generally long day plants (Thomas and Vince-Prue, 1997), although many cultivars have been selected for photoperiod insensitivity. Long day accelerates floral initiation and heading by reducing the number of leaves in vernalized or spring habit plants (Levy and Peterson, 1972; Pinthus and Nerson, 1984). Under SD regimes, double ridge formation is delayed (Lucas, 1972) in sensitive genotypes and the plants produce more leaves rather than a reproductive inflorescence (Levy and Peterson, 1972; Holmes, 1973) until a genetically determined maximum leaf number is attained (Pinthus, 1985).

Low-temperature acclimation in cereals is a cumulative process characterized by a rapid initial LT response followed by a gradual reduction in rate of change to the point of vernalization saturation (Fowler et al., 1996a). Once the vernalization requirement is met and the vegetative phase ends, winter cereal plants gradually lose their ability to tolerate below-freezing temperatures even when they are maintained at temperatures in the optimum range for LT acclimation. Similarly, short day (SD) conditions have been shown to delay development in SD sensitive spring habit genotypes by increasing their FLN, which in turn results in greater and/or longer retention of LT tolerance (Mahfoozi et al., 2000). Based on these observations, it is likely that any factor that influences the length the vegetative growth stage affects the expression of LT-tolerance genes in cereals exposed to acclimating temperatures (Fowler et al., 1996a). Consequently, timing of the transition from the vegetative to reproductive phase is of fundamental interest not only in terms of flowering time but also in the regulation of LT gene expression (Fowler et al., 1999).

Initiation of floral primordia, which is determined by the interplay of the response of the genotype to day length and temperature, determines the final number of leaves produced by the main shoot (Hay and Kirby, 1991). Transition from the vegetative to the reproductive phase can be determined by recording FLN or by dissection of the plant crown to expose the shoot apex. If transition from the vegetative to the reproductive growth stage is the critical developmental switch that initiates the down-regulation of LT-induced genes, photoperiod and vernalization responses should interact to determine the level of LT tolerance gene expression (Fowler et al., 1999). Consequently, the objective of the present study was to determine if LT tolerance genes are developmentally regulated by both photoperiod and vernalization responses in winter wheat and barley.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
The phenological development and LT tolerance of ‘Norstar’ and ‘Warrior’ winter wheat and ‘Kold’ winter barley were investigated in this study. The three cultivars were subjected to two photoperiod treatments (8 and 20 h day lengths) and 12 4°C acclimation periods (0, 7, 14, 21, 28, 35, 42, 49, 56, 70, 84, and 98 d). Final leaf number and LT50 (temperature at which 50% of the plants are killed by LT stress) of each cultivar was determined for each treatment combination.

The experimental design for the LT tolerance study was a 3 (cultivar) by 2 (photoperiod) by 12 (acclimation period) factorial in a four replicate randomized complete block design. The plants for LT50 determinations were grown hydroponically in continuously aerated half-strength modified Hoagland's solution as outlined by Brule-Babel and Fowler (1988). Germinated seeds were grown at 20°C in 8 h (SD) or 20 h (LD) days at a light intensity of 320 µmol m-2 s-1 for 14 d in hydroponic tanks before being acclimated under LD or SD conditions at 4°C and a light intensity of 220 µmol m-2 s-1. The procedure outlined by Limin and Fowler (1988) was used to determine the LT50 (temperature at which 50% of the plants are killed by LT stress) of each hydroponically grown genotype at the end of each LT acclimation period in SD and LD treatments. Plant crowns were covered in moist sand in aluminum-weighing cans and placed in a programmable freezer and held at -3°C for 12 h. After 12 h they were cooled at a rate of 2°C h-1 down to -17°C, then cooled at a rate of 8°C h-1. Five crowns were removed at 2°C intervals for each of five test temperatures selected for each cultivar in each treatment. Samples were thawed overnight at 4°C. Thawed crowns were planted into flats containing "Redi-earth" (W.R. Grace and Co. of Canada Ltd., Ajax, ON, Canada) that was kept moist. The flats were placed in a growth room maintained at 20°C with a 20 h-day/4 h night. Plant recovery was rated (alive vs. dead) after 21 d and LT50 was calculated for each treatment.

Two methods were used to determine the stage of phenological development: (i) dissection of the plant crown to reveal the shoot apex development and (ii) the FLN procedure described by Wang et al. (1995). The reproductive phase of the plant becomes visible as "double ridges" (see Fig. 3 and 4) in the shoot apex (Lucas, 1972; Pinthus, 1985; McMaster, 1997). Therefore, shoot apices of the hydroponically grown plants from the LT tolerance study were dissected and photographed for each acclimation period including a 112-d dissection (not shown) to determine when the double ridge stage occurred. The growth conditions and acclimation times for the FLN study were the same as those described for LT acclimation. The experimental design for the FLN study was a 3 (cultivar) by 2 (photoperiod) by 12 (acclimation period) factorial in a three replicate randomized complete block design. Plants for FLN determination were grown in 15 cm pots (two plants/pot) filled with "Redi-earth" along with the hydroponically grown material used for LT tolerance evaluation. The pots were wrapped in aluminum foil to help prevent radiant heat absorption from the lights and the plants were uniformly fertilized with "Osmocote" (Chisso-Asahi Fertilizer Co., Tokyo, Japan) sustained release fertilizer and a nutrient complete ("Tune-up" TM, Plant Products Ltd., Brampton, ON, Canada) water-soluble solution as required. Potted plants were transferred to 20°C chambers with 20 h (LD) photoperiods and a light intensity of 320 µmol m-2 s-1 at the end of each LT acclimation period to determine the stage of phenological development. Leaves were numbered sequentially and the plants were grown until the flag leaf emerged and the FLN on the main shoot could be determined. Transition from the vegetative to the reproductive phase was considered complete when the FLN became constant (Delecolle et al., 1989).



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  		Fig. 3. Apical development of Norstar winter wheat grown at 4°C under SD (8 h) and LD (20 h) photoperiods for 0, 49, and 98 d. Comparative phenological advancement to double ridge formation (LD98) is illustrated.

 


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  		Fig. 4. Apical development of Kold winter barley grown at 4°C under SD (8 h) and LD (20 h) photoperiods for 0 to 98 d. Comparative phenological advancement to double ridge formation (LD42, SD70) is illustrated.

 
Analyses of variance were conducted to determine the level of significance of differences due to main effects and their interactions in each experiment. Where significant differences were identified, regression analyses of treatment means were used to plot curves that best described the shape and behavior of the responses. The exponential decay linear combination equation was employed to describe the relationship between FLN (y) and days of acclimation (x) at 4°C for the 7 to 98 d periods (Table 1).


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  		Table 1. Estimated regression coefficients (exponential decay linear combination equation for 7 to 98 d) for final leaf number of Kold barley and Warrior and Norstar wheat{dagger} (see Fig. 1) acclimated at 4°C under both long day (LD = 20 h) and short day (SD = 8 h){ddagger} for 0 to 98 d and then moved to 20°C LD (see Fig. 2).

 


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  		Fig. 1. Final leaf number (FLN) of Norstar and Warrior winter wheat and Kold winter barley acclimated at 4°C for 0 to 98 d (average of LD (20 h) and SD (8 h) treatments) and then moved to 20°C LD conditions (SE of data points = 0.45). See Table 1 for regression coefficients.

 


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  		Fig. 2. Average final leaf number (FLN) of Norstar and Warrior winter wheat and Kold winter barley acclimated at 4°C for 0 to 98 d under long (LD = 20 h) and short days (SD = 8 h) and then moved to 20°C LD conditions (SE of data points = 0.35). See Table 1 for regression coefficients.

 
The peak four parameter Weibull equation was used to describe the relationship between LT50 (y) and days of acclimation (x) at 4°C (Table 2).


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  		Table 2. Estimated regression coefficients (peak four parameter Weibull equation) for LT50 of Kold barley (7 to 98 d) and Warrior and Norstar wheat (0 to 98 d) acclimated at 4°C under both long day (LD = 20 h) and short day (SD = 8 h) for 0 to 98 d (see Fig. 5).

 


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  		Fig. 5. Low-temperature tolerance of Norstar and Warrior winter wheat and Kold winter barley acclimated under both long (LD = 20 h) and short (SD = 8 h) d at 4°C for 0 to 98 days (SE of data points = 0.48). See Table 2 for regression coefficients.

 
Nonlinear regression procedures outlined by SigmaPlot (2000) were used to provide least squares estimates of the regression coefficients in these equations.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Phenological Development
When grown under LD at continuous 20°C compared to a 49 d pretreatment at 4°C for 49 d, Norstar and Warrior wheat and Kold barley reduced their leaf number from 22.5 to 12.0, 19.0 to 11.0, 22.0 to 18.2, respectively (Fig. 1), indicating that these are winter habit cultivars with a vernalization requirement (Wang et al., 1995). Analysis of variance for FLN of plants acclimated at 4°C for 0 to 98 d and then moved from SD or LD to 20°C LD indicated that differences due to cultivars, photoperiod (PP), and acclimation period were significant (P < 0.05). The cultivar x PP interaction was not significant indicating Norstar, Warrior, and Kold have similar responses to PP in the range between 0 and 98 d. However, the acclimation period x cultivar interaction was highly significant (P < 0.01), probably due to differences between wheat and barley in the time to vernalization saturation (Fig. 1, Table 1). The acclimation period x photoperiod interaction was also significant (P < 0.05) indicating that the effect of photoperiod was dependent upon the stage of vernalization (Fig. 2, Table 1).

Initiation of floral primordia is determined by genotype and environment interactions, which in turn determines the FLN produced by the main stem (Hay and Ellis, 1998). When the last leaf (flag leaf primordia) is formed the plant begins the reproductive phase (Robertson et al., 1996). Fulfillment of the LT requirement (vernalization saturation), which is also an indication of the point of transition from the vegetative to the reproductive phase (Robertson et al., 1996), is considered complete once the cold treatment no longer reduces FLN (Wang et al., 1995). Final leaf number measurements indicated that vernalization saturation was achieved between 42 and 49 d for Norstar and Warrior winter wheat and 28 to 35 d for Kold winter barley (Fig. 1). Double ridge formation, when leaf and spikelet initials are both apparent on the shoot apex, is another clear indication that transition to the reproductive phase has begun (McMaster, 1997). However, double ridge formation was not observed until 98 d for LD (Fig. 3) and 112 d for SD (not shown) treatments in Norstar and Warrior winter wheat and 42 d for LD and 70 d for SD treatments in Kold winter barley (Fig. 4). Thus, under the LT growth conditions of this experiment, the signal for transition to the reproductive stage occurred long before the physical manifestation of double ridge formation. These observations show conclusively that floral initiation occurs before double ridge formation as suggested by Gott et al. (1955) and Delecolle et al. (1989) using aposteriori analysis of leaf and shoot apex primordia numbers. Yan and Wallace (1996) suggested that photoperiod genes are less active at lower temperature, but the delay in double ridge formation under SD compared to LD indicates that these winter habit cultivars were sensitive to SD treatments even at 4°C.

In contrast to the plateau observed for plants grown under LD, the point of minimum FLN under SD 4°C (non-inductive conditions) was followed by significant (P < 0.05) increase in FLN between 49 and 98 d (Fig. 2). It appears that temperature and photoperiod affect the fate of shoot primordia after they have developed a bias or partial commitment toward a certain fate as suggested by Hempel et al. (1998). For example, vernalization of wheat can increase the number of labile primordia with a developmental fate that is not fixed until double ridge formation (Griffiths et al., 1985). Levy and Peterson (1972) have reported similar increases in FLN of vernalized winter wheat under non-inductive SD conditions. Continuous vegetative growth of plants under non-inductive conditions has even been related to flower/inflorescence reversion to leaf primordia in some plant species (Battey and Lyndon, 1990). It therefore appears that non-inductive flowering conditions, even though vernalization saturation is complete, extend the vegetative phase and delay transition to the reproductive phase.

Low-Temperature Tolerance
Analysis of variance indicated that differences in LT50 due to cultivars, PP, acclimation period, and the acclimation period x PP interactions were highly significant (P < 0.001). The cultivar x PP interaction was not significant indicating that the cultivars responded similarly to PP over the 0 to 98-d period. In spite of a limited response to photoperiod at these low temperatures, significant (P < 0.001) differences in LT50 were associated with the delay in phenological development due to SD compared to LD treatments (Fig. 5, Table 2). Plants grown at 4°C started to acclimate at a rapid rate under both LD and SD. The rate of change in LT tolerance then gradually slowed until LT tolerance began to be lost. These changes were most apparent in the wheat cultivars, which possess a greater ability to acclimate to LT than barley. The wheat plants reached their maximum LT tolerance between 42 and 49 d, which is about the same time as vernalization saturation occurred (Fig. 1 and 5). This is in agreement with previous reports by Fowler et al. (1996a) and indicates that the signaled end of the vegetative phase, as indicated by FLN measurements (Fig. 1 and 2), corresponds to the start of LT tolerance loss. Acclimation rate was similar or faster under LD compared to SD for the first 14 to 21 d. However, greater LT tolerance was maintained under SD than LD for the period from 28 to 98 d (Fig. 5). This appears to be the result of an extended vegetative period that delayed the transition to the reproductive stage as illustrated in Fig. 3 and 4.

The photoperiodic response of SD sensitive winter barley and wheat cultivars was reflected in the level of expression of LT tolerance beginning in the early stages of vernalization and plant development (Fig. 5). The SD and LD LT response curves began to separate before the vernalization saturation point, as determined by FLN, indicating that plant development rate can be influenced by photoperiod during the vernalization process. Takahashi and Yasuda (1970) suggested that photoperiod response is concealed by winter growth habit in cereals and determination of a photoperiod response of a winter type must be preceded by vernalization saturation. More correctly, it would appear that some degree of vernalization may be required in winter cereals before photoperiod responsiveness can be revealed. Responsiveness to photoperiod, however, occurs long before vernalization is complete (Fig. 5). This implies that winter habit genotypes are not in the juvenile (nonresponsive to photoperiod) stage for the full duration of the vernalization requirement and only a short period of LT exposure is required before they are responsive to photoperiod.

The results of this study show that photoperiod response and vernalization requirements interact with temperature from early stages of plant growth to influence the rate of phenological development and the expression of LT tolerance genes. They also verify that vernalization requirement (Fowler et al., 1996a, 1996b) and SD photoperiod sensitivity (Mahfoozi et al., 2000) allow LT tolerance genes to be expressed for a longer period of time at temperatures in the LT acclimation range. As such, they support the developmental theory of LT tolerance gene expression (Fowler et al., 1999) which states that level and duration of gene expression determine the degree of LT tolerance and any factor that delays the transition from the vegetative to the reproductive stage increases the duration of expression of LT tolerance genes in cereals exposed to acclimating temperatures.


   ACKNOWLEDGMENTS
 
Financial support from the Agricultural Research, Education, and Extension Organization (AREEO) of the Agricultural Ministry of Iran is gratefully acknowledged. The excellent technical assistance of Garcia Schellhorn is greatly appreciated.

Received for publication August 24, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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