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Crop Science 42:797-803 (2002)
© 2002 Crop Science Society of America

CROP PHYSIOLOGY & METABOLISM

Heat Stress during Flowering in Summer Brassica

Malcolm J. Morrison* and Doug W. Stewart

Agric. and Agri-Food Canada, Eastern Cereal and Oilseed Res. Ctr., Central Exp. Farm, K.W. Neatby Bldg, Ottawa, ON, Canada K1A 0C6

* Corresponding author (morrisonmj{at}em.agr.ca)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
Temperatures greater than 27°C, in a growth cabinet, have resulted in floral sterility and yield loss in Brassica napus L. Maximum daily temperatures often exceed this in the major canola growing regions. Our objective was to examine the effects of heat stress during flowering on yield and yield components of B. napus, B. rapa L., and B. juncea (L.) Czernj. & Cosson. Cultivars of the three Brassica species were grown in a split-plot design in the field for 3 yr at Ottawa, Canada. Three seeding dates were used each year to obtain different levels of heat stress during flowering. The number of flowers on the main raceme and the first and second branch racemes were counted at anthesis, from 10 plants per plot. At maturity, pods from the sampled plants were counted and seed numbers and weight determined. Two rows of the remainder of each plot was harvested for seed yield. A heat stress index was developed on the basis of the accumulation of daily maximum temperatures greater than a threshold temperature. The threshold temperature during flowering, which resulted in seed yield losses, was 29.5°C for all Brassica species. High mean maximum temperature during vegetative development resulted in a reduction in flower number for all Brassica species. Seed yield decreased as heat stress during flowering increased. The reduction in seed yield was primarily due to a reduction in flower number and in the number and size of the seeds produced per flower. Plant breeders should actively select for heat stress tolerance in future canola cultivars.

Abbreviations: GDD, growing degree days with a 5°C baseline temperature • Hi, heat stress index • MR, main raceme yield contribution to total plant yield • SF, seed weight per flower established • SR, success ratio • TF, threshold heat stress temperature


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
H IGH AIR TEMPERATURES during reproduction cause a reduction in fertility and seed yield in wheat (Triticum aestivum L., Saini et al., 1983), corn (Zea mays L.; Schoper et al., 1987; Mitchell and Petolino, 1988), cotton (Gossypium spp.; Kittock et al., 1988), cowpea [Vigna unguiculata (L.) Walp.; Ahmed and Hall, 1993], and pea (Pisum sativum L.; Guilioni et al., 1997). Summer rape (B. napus and B. rapa) is best adapted to cool growing regions; however, its cultivation is expanding into areas that may be too warm for optimal seed production.

Olsson (1960) reported that yield in summer rape was determined by number of pods, seeds per pod, and weight per seed. Of these components, number of pods produced per plant was most affected by environmental stresses like drought. Tayo and Morgan (1975) reported that only 45% of summer rape (B. napus) flowers developed into pods that were retained until harvest. They also determined that 75% of the pods that were present at maturity developed from flowers that opened within 14 d from the beginning of flowering. While summer rape has a considerable capacity to produce flowers on branch racemes, the narrow window of 1 to 2 wk around first flower is critical for seed yield. High temperature stress during this period may reduce seed yield. Richards and Thurling (1978) reported that a delay in planting, resulting in higher temperatures during flowering, caused lower yields. McGregor (1981) determined that pod abortion increased when later seeding dates delayed anthesis to a warmer part of the growing season.

In a yield trial across several locations in western Canada, mustard (B. juncea) had significantly higher seed yield than either species of canola (B. napus or B. rapa) (Woods et al., 1991). They concluded that mustard had more heat tolerance than canola and proposed that mustard with oil quality characteristics of canola may be a suitable oil seed crop for the warmer and drier areas of western Canada.

Polowick and Sawhney (1987) found that the flowers of B. napus plants grown in growth cabinets were smaller at air temperatures of 28/23°C (day/night). In a later paper, Polowick and Sawhney (1988) reported that while the fertility of B. napus (cv. Westar) was not impaired at 28/23°C, growth cabinet temperatures of 32/26°C resulted in sterile flowers with smaller sepals, petals, and stamens.

In a previous study, one of us reported that the B. napus cultivars Westar and Delta were almost entirely sterile when grown in a growth cabinet set at 27/17°C (day/night) (Morrison, 1993). The stage most sensitive to heat stress in summer rape occurred from late bud development until early seed development.

Air temperatures greater than 27°C are often reached in the field at flowering time in the major summer rape growing regions. It is important to determine what effect heat stress has on summer rape fertility and to determine if observations made in the growth cabinet are repeated in the field. The objective of this experiment was to examine the effects of high temperature stress during flowering on the fertility and yield of Brassica species grown in the field. A heat stress index during flowering was developed for summer Brassica on the basis of the accumulation of daily maximum temperature above a threshold temperature.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
The experiment was done at the Central Experimental Farm, Ottawa (Lat. 45° 23' N) from 1989 to 1991. Three seeding dates, spaced approximately 2 wk apart, were used to obtain different temperature regimes during flowering. Brassica napus, cvs. Westar and Delta, B. juncea, cv. Cutlass, and B. rapa, cv. Tobin, were planted in a split-plot design with seeding date as the main effect and cultivar the subeffect. Individual plots were replicated four times and consisted of 8 rows, 6 m long, spaced 18 cm apart. Seeds were planted 1 to 1.5 cm deep at a rate of 150 seeds m-2 into a Lyons loam (fine loamy, mixed, mesic Typic Endoaquoll; Canadian classification: Orthic Humic Gleysol). In the spring, 34 kg ha-1 of N as NH4NO3 was applied preplant and incorporated. The fields were treated with preplant incorporated granular trifluralin ({alpha},{alpha},{alpha}-trifluoro-2,6-dinitro-N,N-dipropyl-p-toluidine) at 1.25 L ha-1 a.i. to control weeds. The plots were also hand weeded during the season. Carbofuran (2,3-dihydro-2,2-dimethylbenzofuran-7-yl methylcarbamate) insecticide was applied with the seed at 5 kg ha-1 to prevent damage from flea beetles (Phyllotera spp and Psylliodes spp). Natural precipitation was augmented with irrigation to ensure that each seeding date received a minimum of 2 cm of water per week until physiological maturity when irrigation was stopped.

Phenological observations were made on a regular basis with the Harper and Berkenkamp (1975) growth stage key. A particular growth stage was reached when 50% of the plants within the plot had achieved that stage. Maximum and minimum daily temperatures and precipitation, measured at a near-by weather station, were used to calculate growing degree days (GDD) with a 5°C baseline temperature (Morrison et al., 1989).

At the beginning of flowering, all of the buds and open flowers on the main raceme and the subsequent two primary branch racemes were counted and recorded from 10 plants selected at random from within each plot. For the remainder of the paper, the main raceme and the two primary branch racemes together will be referred to as the main racemes, while all other racemes originating from the main stem will be designated as branch racemes. The plants were tagged and numbered, and at harvest the tagged plants were removed from the field and the number of pods on the main racemes counted. The number of branch racemes and their pods were counted. Pods from the main racemes and the branch racemes were kept separate for further processing. Pods from the main racemes and the branch racemes were threshed and seed weight and the number of seeds determined. The number of seeds per pod were determined by dividing the number of seeds per plant by the number of pods per plant. A 10-plant mean for each trait was calculated and used in data analyses.

Three parameters were developed to examine the effect of heat stress on seed yield. The success ratio (SR,%) represented a ratio of the number of pods developed on the main racemes to the number of flowers initially established, and provided an indication of the effect of heat stress on fertilization, because pods without seeds usually abort. The main raceme yield (MR,%) represented the seed yield contribution from the main racemes to total seed yield per plant and was calculated by dividing the seed yield (g) from the main racemes by total seed yield (g) per plant. The seed yield per flower (SF, g) was calculated by dividing the seed yield (g) per main racemes by the number of flowers per main racemes. The SF provided an indication of the effect of heat stress on both fertility and seed development.

When ripe, plants in the two center rows per plot (2.16 m2) were cut by hand, placed in large bags, and air dried. The plants were threshed with a stationary combine. Seed from the bulk harvest was cleaned, dried to approximately 30 g kg-1 moisture, and weighed.

The data were analyzed initially by year as a split-plot with seeding date as the main effect and cultivar as the split effect. Both error A (for testing seeding date) and error B (for testing cultivar effect) from each year were tested for homogeneity before the data were pooled and an ANOVA done by cultivar on the combined data across the 3 yr of the test. The combined ANOVA was used to separate year x date effects for each cultivar.

To examine heat stress during flowering, we created an index based upon the maximum (Tmax) daily temperature, received from the beginning of bolting through to the end of flowering, that was greater than a threshold temperature (TF). The heat stress index (Hi) during flowering was defined as:

[1]
where (Tmax-TF) >= 0, {Delta}t is a time (day) step and n is the number of days during flowering.

To calculate Hi, we needed an estimate of the threshold temperature (TF). We assumed that cultivar yield (Y) was reduced by Hi, accumulated from the beginning of bolting to the end of flowering, according the following equation:

[2]
where Ymax was the Y axis intercept and represented yield unaffected by heat stress and b was a regression coefficient. We used seed yield data from the three seeding dates across 3 yr and a least squares optimization procedure (Marquardt, 1963) to determine the best values of Ymax, b, and Hi, for each cultivar. This value of Hi was used with locally collected weather data to obtain TF using Eq. [1]. The process was iterative and stopped when an estimate of TF was resolved that resulted in the lowest sums of squares of the deviation between calculated and observed yields. The best estimate of TF was used to calculate Hi units for each cultivar from locally collected weather data for each seeding date x year combination.

For each cultivar and seeding date x year combination, GDD, calendar days, and Hi , were accumulated for the growth phases from seeding to bolting (vegetative), bolting to end of flowering (flowering), and end of flowering to physiological maturity (seed development). Mean Tmax was calculated for the same growth phases as the sum of the daily maximum temperature divided by the number of days during a growth phase. Simple linear correlation (r, with n - 2 df) was used to define the relationship between calendar days, mean Tmax, or Hi and flower number, pod number, and seed yield.

To observe the effect of heat stress during flowering on specific traits, the data from each year x date combination were plotted against their respective Hi during flowering for each cultivar. A straight line was fitted through the points by simple linear regression. The degree of association between the trait and Hi was examined by calculating the simple linear correlation coefficient (r, with n - 2 df).


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
SUMMARY
 REFERENCES
 
Growing degree days were calculated from seeding to physiological maturity (Table 1). When averaged across years, the first date of seeding of Westar required 606 GDD to reach first flower (data not shown) and 1103 GGD to reach physiological maturity. In an earlier study, conducted at Winnipeg, Canada (49°N latitude), Westar rapeseed required 576 and 1157 GDD to reach the same stages (Morrison et al., 1989). The warmer climate of Ottawa resulted in slightly greater accumulation of GDD to first flower and fewer GDD to physiological maturity. Differences in time to first flower between latitudes indicates that the GDD model may require a photoperiod factor to improve its accuracy.


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  		Table 1. Growing degree days (GDD) from seeding to physiological maturity.

 
The threshold temperature (TF) during flowering was not significantly different among species, with the combined value being 29.5°C (Table 2). To test the accuracy of TF, the model predicting yield (Eq. [2]) was calculated from different values of TF. The mean SEE of predicted yield when compared with observed yield decreased to a minimum at a TF of 29.5°C, followed by a rapid increase (Fig. 1) .


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  		Table 2. Critical Heat Stress Temperatures (TF °C) and their standard errors for four Brassica cultivars and all cultivars combined.

 


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  		Fig. 1. Mean standard error of estimate (SEE g m-2) of the model predicted yield with varying threshold temperatures (TF) compared to the observed yield.

 
Flower number, pod number, and seed yield were tested for correlation with calendar days, mean Tmax, and Hi for three phases of crop development (Table 3). The number of calendar days were not correlated with flower or pod number for any growth phase. Calendar days during flowering were correlated with seed yield in Cutlass, but there were no other significant correlations among the other cultivars or growth phases. Thurling (1974) proposed that a delay in seeding resulted in a shorter number of days from seeding to first flower and lower yields because of a reduced capacity to produce and fill seeds. Thurling (1974) used three seeding dates separated by 30 d each, during a period of decreasing photoperiod, while in our experiment the intervals between seeding dates were only 15 d apart during a period of increasing photoperiod. Perhaps if the seeding dates in our experiment were further apart, the relationship between the vegetative development time and yield might have been stronger. Seed yield was not correlated with the number of calendar days during seed development, indicating that a longer seed filling period did not result in higher seed yield.


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  		Table 3. Linear correlation coefficients (r) of flower number, pod number, and seed yield with calendar days (days), mean maximum temperature (Tmax), and the heat stress index (Hi) for four Brassica cultivars during three growth phases.

 
Mean Tmax during vegetative development was correlated negatively with flower number for all cultivars, while Hi during the same period was correlated negatively with flower number for Delta (Table 3). Mean Tmax and Hi during vegetative development were correlated negatively with pod number for Delta and Cutlass. During flowering, only Hi was correlated significantly with a reduction in flower number in Cutlass and Tobin, while both mean Tmax and Hi were correlated negatively with pod number in Cutlass.

For all cultivars, mean Tmax was correlated negatively with seed yield during vegetative development and, with the exception of Delta, during flowering (Table 3). The Hi was correlated negatively with seed yield for all cultivars during vegetative development and flowering. There were no significant correlations of mean Tmax or Hi with seed yield during seed development, indicating that seed yield reduction from heat stress temperatures occurred prior to seed development.

The correlation between mean Tmax and Hi during vegetative development and flowering was significant for all cultivars (data not shown). This was not unexpected since, Tmax was used to calculate Hi. It is difficult to determine what aspect of mean Tmax was responsible for plant damage since the upper and lower limits have not been established. It is likely that high mean Tmax during vegetative development was responsible for reducing the number of flowers on the plants. This condition was exacerbated during flowering by further high temperatures. The response of Brassica to mean Tmax during vegetative development requires further research. The fact that Hi during vegetative development was correlated significantly to reductions in seed yield is evidence that a lower TF would improve the heat stress equation during this growth phase. Future experiments will be designed to focus on improving the heat stress equation during vegetative development in conjunction with heat stress during flowering.

We have concentrated the remainder of our study on Hi calculated during flowering. In the growth cabinet experiment, temperatures greater than 27°C during flowering caused sterility in Westar and Delta (Morrison, 1993). The threshold temperature determined in the current field experiment was 29.5°C and there was no evidence of complete raceme sterility as encountered previously. In the growth cabinet, flowers were exposed to a constant high temperature for the entire daylight period, whereas in the field, the critical temperature was determined from the maximum daily temperature, which may have only lasted for a short duration. The cabinet plants were exposed to heat stress during a similar developmental period, while in the field not all flowers were exposed to the same heat stress intensity, resulting in greater reserves of unstressed flowers. Furthermore, field grown plants had wind and insects to vector pollen and enhance pollination.

As Hi increased, the number of flowers per main racemes decreased in Cutlass and Tobin (Fig. 2A) . The number of pods per main racemes decreased significantly as Hi increased in Cutlass (Fig. 2B). The ratio of the number of pods produced per flower set (success ratio, SR) was not associated significantly with Hi in any cultivar (Fig. 2C) indicating that some successful pollination occurred on the flowers that were established.



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  		Fig. 2. Relationship between heat stress during flowering and (a) number of flowers on the main racemes; (b) number of pods on the main racemes; (c) success ratio (%, ratio of pods produced per flowers produced). The LSD error bar represents differences among year by date samples and r = linear correlation coefficient (n - 2df).

 
When averaged across seeding dates and years, the number of flowers, on the main racemes, that produced pods was 59, 69, and 55% for B. napus, B. juncea, and B. rapa, respectively. Tayo and Morgan (1975) and McGregor (1981) observed that less than 45% of the flowers formed on B. napus cultivars produced pods. It seems that the rapeseed plant produces nearly twice as many flowers as it fills. Williams and Free (1979) have suggested that the over production of flowers is a survival mechanism in anticipation of insect and disease loss. The reduction in flower number with higher mean Tmax during vegetative development is evidence that Brassica plants can adjust to environmental conditions by altering the number of potential resource demanding sinks.

The number of seeds from the main racemes decreased with increasing Hi in Delta and Tobin (Fig. 3A) . As Hi increased, the 1000-seed weight decreased significantly in all cultivars except Delta (Fig. 3B). As Hi increased, seeds per pod on the main racemes decreased significantly in Westar and Cutlass (Fig. 3C).



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  		Fig. 3. Relationship between heat stress during flowering and (a) number of seeds on the main racemes; (b) seed weight per 1000 seeds (g); (c) number of seeds per pod on the main racemes. The LSD error bar represents differences among year by date samples and r = linear correlation coefficient (n - 2df).

 
The contribution of the main racemes to total plant yield (MR%) increased as Hi increased in Cutlass and Tobin (Fig. 4A) . As Hi increased, the seed yield per flower set (SF, g) on the main raceme decreased significantly in all cultivars (Fig. 4B). Total seed yield decreased significantly with increasing Hi in all cultivars (Fig. 4C).



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  		Fig. 4. Relationship between heat stress during flowering and (a) main raceme yield as a proportion of total yield (b)main racemes seed yield (g) per flower; (c) seed yield g m-2. The LSD error bar represents differences among year by date samples and r = linear correlation coefficient (n - 2df).

 
Seed yield per plant is the product of the number of seeds per plant and the weight of those seeds. In turn, the number of seeds per plant is the product of the number of pods per plant and the number of seeds per pod. Heat stress during flowering can influence seed yield through a reduction in one or more of these components. In Cutlass, as Hi increased, there were fewer pods per plant with fewer seeds per pod of lower 1000-seed weight. In Tobin, as Hi increased, there were fewer seeds per plant with lower 1000-seed weight. In Westar, heat stress resulted in fewer seeds per pod with a lower 1000-seed weight, while Delta had lower number of seeds per plant. The two B. napus cultivars responded to heat stress in similar fashion with the notable exception of 1000-seed weight. In Westar, 1000-seed weight was reduced by Hi, while in Delta, it was not. Differences in yield component sensitivity to heat stress within species indicates that there is genetic variability for this trait and new cultivars may be developed with improved heat stress tolerance.

The effects of heat stress during reproduction on temperate crops can be grouped into three areas: reduced flower number prior to anthesis, reduced flower fertility because of pollen sterility or ovary damage, and a reduced capacity of the plant to support pods and seeds after fertilization. High mean Tmax prior to anthesis reduced the number of flowers on the main racemes. Heat stress during flowering caused a significant reduction in the number of flowers and pods on the main racemes in Cutlass and Tobin. Future experiments should examine heat stress prior to bolting, when flowers are being formed, because of the significant correlation between seed yield and Tmax and Hi (Table 3). The cabinet experiment (Morrison 1993) showed that high temperature resulted in lower fertility because of reduced pollen viability and female fertility, resulting in pollination with no fertilization. It was unlikely that the reduction in yield experienced in the field was the result of pollen sterility because SR was not significantly reduced by Hi. Brassica produces an abundance of pollen and not all of it would have been exposed to the same TF because of diurnal and seasonal fluctuations in Tmax. Brassica juncea pollen has the capability to withstand temperatures as high as 60°C without effect to pollen viability (Rao et al., 1992). Heat stress temperatures may have damaged the ovary, reducing the number of ovules fertilized. Pechan (1988) suggested that barriers may exist between the pollen tube and the ovule in B. napus, and that enzymes are required to dissolve these barriers, facilitating fertilization. High temperatures may have inhibited the production or action of these enzymes, resulting in a reduced number of seeds per pod. Tayo and Morgan (1979) demonstrated that the numbers of pods and seeds per pod was regulated by the capability of B. napus to supply carbon to the inflorescence for the period from 3 wk following anthesis. In our experiment, heat stress during flowering may have limited photoassimilate production and translocation to developing seeds, resulting in pods with fewer seeds of lesser weight.

From a multi-location trial across the northern Great Plains, Woods et al. (1991) concluded that because B. juncea had higher yield than B. napus or B. rapa in drier regions, it was more drought and heat tolerant than canola. Our study showed that B. juncea was as susceptible to heat stress during flowering as either B. napus or B. rapa.


   SUMMARY
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
REFERENCES
 
The accumulation of daily air temperatures greater than 29.5°C during the period from bolting to the end of flowering significantly reduced yield all Brassica species tested. Flower number per plant decreased with increasing mean maximum daily temperature during vegetative development. The number of flowers and pods produced on the main racemes decreased with increasing heat stress in B. juncea and B. rapa. Heat stress during flowering primarily caused a reduction in seed weight per flower developed, with some decrease in seed number per pod evident. The actual physiological mechanisms resulting in reduced seed size or number per pod should be determined. Kittock et al. (1988) found that nearly half of the 30% yield improvement in lint yield of new Pima cotton cultivars was the result of increased tolerance to high temperatures, indicating that heat stress is a trait that can be selected for in a plant breeding program. With global warming, heat stress may become more of a problem in the major Brassica growing regions of Canada and to safeguard future yield, plant breeders should be selecting for increased heat stress tolerance.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 
ECORC contribution no. 02-41.

Received for publication September 29, 2000.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY
 REFERENCES
 




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