Nighttime Warming Will Increase Winter Wheat Yield Through Improving Plant Development and Grain Growth in North China
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- Chen, J., Tian, Y., Zhang, X. et al. J Plant Growth Regul (2014) 33: 397. doi:10.1007/s00344-013-9390-0
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A better understanding of the actual impacts of nighttime warming on winter wheat growth will assist in breeding new varieties and agronomic innovation for food security under future climates. A 3-year experiment was conducted over an entire growth period of winter wheat using a passive warming facility in North China. An increase of 1.1 °C in mean nighttime temperature promoted wheat development, causing a 6-day reduction of the preanthesis period but a 5-day extension of the postanthesis period. This warming significantly stimulated the rate of leaf respiration at nighttime, resulting in higher carbohydrate depletion compared to that of the unwarmed control. However, stimulation of nighttime respiration and carbohydrate depletion could be compensated for by warming-led promotion of daytime photosynthesis and carbohydrate assimilation. Meanwhile, the flag leaf area per plant and the total green leaves area were significantly higher in the warmed plots than in the unwarmed plots. Besides extending the duration of grain filling, nighttime warming significantly promoted the filling rates of the superior and inferior grains, resulting in a significant increase in the 1,000-grain weight by 6.3 %. Consequently, this moderate increase in nighttime air temperature significantly increased wheat aboveground biomass and grain yield by 12.3 and 12.0 % (p < 0.05), respectively. A moderate warming at nighttime can improve the sink-source balance of winter wheat for higher yield. Our results suggest that climatic warming may benefit winter wheat production through improvement of plant development and grain growth in North China.
KeywordsGlobal warmingWheat phenophaseCarbohydrate metabolismGrain weightPassive nighttime warmingNorth China
The Earth has experienced significant increases in air temperature over the last decades, and the daily mean air temperature is predicted to rise by as much as 2.0–5.4 °C in this century (National Research Council 2010). Many observations have demonstrated that air temperature increases are due mainly to nighttime warming during the winter-spring seasons (Easterling and others 1997). Winter wheat (Triticum aestivum L.), the most important staple crop, is planted mainly in winter-spring seasons when warming is most likely anticipated (IPCC 2007). Because temperature is a major environmental factor that affects plant development and growth, even a moderate increase in air temperature is likely to have a significant impact on winter wheat production. Moreover, a daily minimum temperature increase will also decrease the diurnal temperature range, suggesting greater impact on crop growth compared to all-day warming (Peng and others 2004; Lobell 2007; Welch and others 2010). Thus, learning about the impact of nighttime warming on winter wheat production may facilitate the development of strategies for food security and agricultural adaptation for future climates.
The impact of air temperature increases on wheat growth has been extensively observed over the past decades (Bidinger and others 1977; Bhullar and Jenner 1985; Porter and Gawith 1999; Larmure and others 2005; Lobell and others 2011). These observations have greatly enhanced our understanding of the effects of high temperature on wheat development and growth and the underlying mechanisms of wheat’s response to high temperature. However, most of the existing experiments were conducted in controlled conditions such as growth chambers and greenhouses, which are different from the field conditions (Nijs and others 1996; Aronson and McNulty 2009). Although some experiments were conducted under field conditions, they were executed mostly for a short period, such as the postanthesis period (Slafer and Rawson 1995; Larmure and others 2005; Gregersen and others 2008), or even only for several days postanthesis (Savin and Nicolas 1996). Recently, a few experiments were conducted over an entire growth period under field conditions with an all-day warming regime (Aronson and McNulty 2009; Tian and others 2012). The warming levels were the same during the daytime and the nighttime, which may not completely present the actual effect of predicted warming on wheat growth because of the difference in the extent of warming between daytime and nighttime (Lobell 2007). Moreover, because the increase in air temperature set in most experiments was often higher than the warming rate predicted by climate models (Savin and Nicolas 1996; Aronson and McNulty 2009), the impact of global warming on winter wheat growth might be overestimated by existing observations and projections. To observe the impact of a moderate increase in daily minimum temperature on winter wheat over an entire growth period under field conditions may further increase our understanding of the impact of global warming on food production.
More than 70 % of Chinese winter wheat is sown in the north plain, where the mean air temperature is predicted to increase approximately 1.5 °C by 2050, mainly due to the increases in daily minimum temperature during winter-spring seasons (Chavas and others 2009). To our knowledge, there have been no studies on the impact of an increase in the daily minimum temperature on winter wheat growth for an entire growing cycle under field conditions in North China. Therefore, we conducted a 3-year experiment using a passive nighttime warming facility (Zeiher and others 1994; Beier and others 2004) to mimic the predicted increase in daily minimum temperature in North China. Our objective was to observe the responses of wheat phenology, biomass production, leaf carbon metabolism, and grain filling to a moderate increase in the daily minimum temperature.
Materials and Methods
The experiment was conducted from the fall of 2007 to the summer of 2010 in Fengxian county, Jiangsu province, China (34°50′07′′N, 116°39′34′′E, 33 above sea level), which is the central zone of the main winter wheat growing region in North China. Wheat is commonly sown in October and harvested in early June of the next year. The mean annual precipitation and air temperature is 630 mm and 14.6 °C, respectively. The soil is a cumulated irrigated fluvo-aquic soil (Typic fluvisols in the soil taxonomy classification system of the US) (Soil Survey Staff 2010). Relevant soil properties were as follows: pH 7.3, total N, 2.2 g kg−1; available P, 42.9 mg kg−1; available K, 55.4 mg kg−1; and soil organic matter, 20.0 g kg−1.
Experiment Design and Warming Facility
The experiment was a completely random design with three replicates and included two treatments: warming at nighttime (warmed) and unwarmed control (unwarmed). The warmed plot was covered with a curtain from sunset to sunrise (around 19:00–06:00) every night from sowing to harvest time, except for days when it rained or snowed (Zeiher and others 1994). Each replicate plot was 4 m × 5 m, and the distance between the adjacent plots was 10 m to avoid heating contamination.
Based on the technique of passive nighttime warming (PNW) (Zeiher and others 1994; Beier and others 2004), a novel PNW facility under manual control was constructed for this experiment. This PNW facility is energy-saving and cost-saving and can be widely used in the field where power is not available. The warmed plot was covered by a reflective curtain fixed on galvanized steel tubes at both ends. The curtain material consisted of 0.25-mm-wide aluminum foil knitted into a fiberglass cloth (Jiangyin Zhongchang Fiberglass Composite Material Co., Ltd., China). The curtain can reflect 97 % of direct and 96 % of diffuse radiation and allow transfer of water vapor; it is opaque to visible radiation. Thus, this curtain can reduce the loss of infrared radiation from the field surface and increase the air temperature on the wheat canopy during the night. The unwarmed control was not covered with a curtain. To alleviate the impact of the curtain on air exchange in the field, the spacing between the curtain and wheat canopy was kept within 25–30 cm by a weekly adjustment of the height of the curtain over the wheat according to plant height. Two men were responsible for running this PNW facility. During the growing cycle, the reflective curtains were spread out to cover the field at sunset (around 19:00 pm) and rolled up at sunrise (around 06:00 am) by hand every day. To keep the same precipitation background between the treatments, the curtain was kept rolled up at night when it rained or snowed. The length of the entire growing period was more than 240 days for each experimental year, and the warmed plots were kept uncovered due to rain and snow for fewer than 20 days for each growing season.
Two winter wheat cultivars (Yangfu 188 in 2007–2008 and Aikang 58 in 2008–2010), which are widely grown in North China, were used in this experiment. The seeds were manually sown in October at a density of 225 plants m−2 and 20 cm between rows. Crops were harvested in early June on a plot-by-plot basis depending on the maturity dates of each treatment. The fertilizer applications of N, P, and K in each plot were 22.5, 7.5, and 7.5 g m−2, respectively. The total P and K and half of the N were applied as basal dressing 2 days prior to sowing. The other half of the N was applied as side dressing at early tilling in the beginning of March. To keep the same regimen of agronomic management between the treatments, all fertilizers were applied on each plot on the same date according to the unwarmed control. The same irrigation regimen was used for the warmed and unwarmed plots if irrigation was necessary according to soil moisture, and there was no water limitation on wheat growth during the experimental period for all plots.
Canopy Temperature and Soil Moisture Monitoring
The temperatures were manually measured with a thermometer at some key stages during the 2007–2008 and 2008–2009 growing seasons. Because these measurements were not continuous, that temperature data are not presented here. To get continuous temperature data during the 2009–2010 growing season, the air temperature over the wheat canopy was monitored automatically every 20 min for each treatment for an entire growth period using a digital temperature monitor (ZDR241, Hangzhou Zheda Electronic Instrument Co., Ltd., China). The monitor incorporated a MF52A502J3950 NTC thermistor (Nanjing Shiheng Electronic Technology Co., Ltd.), with a resolution of 0.1 °C, accuracy of ±0.5 °C, and a range of −40 to 100 °C. Because this experiment warmed the wheat only at night and we focused on nighttime temperature, no sun shield was used during the growing period.
The temperature monitors were positioned in the center of the plot under the curtain at the height of the wheat canopy. Because the temperature monitor system was very expensive, only one replicate’s temperature was monitored for each treatment and the other two replicates were manually measured using a thermometer in some key stages. Therefore, we just present the temperature data monitored by the digital temperature monitor system during the 2009–2010 growing season. Meanwhile, soil moisture was tested at key stages of wheat growth (that is, jointing, anthesis, and maturity stages) using the direct weighing method presented by Bremner (1965).
Plant Growth and Grain Yield Determination
The sowing, heading, and maturity dates were recorded for every year. Anthesis was recorded when anthers in the central spikelets of 50 % of the ears in a plot had extruded and maturity was recorded when most of the ears in a plot were no longer green. Fifteen culms of plant samples were taken from each plot at maturity phases. Dry weights were determined separately for each plant part after oven drying at 70 °C for at least 48 h. Spike and grain yields in each plot were determined by harvesting 1 m2 of plants after maturity.
Fifteen plants were sampled from each plot and the flag leaf area and total green leaf area were measured using a Li-3000 Portable Area Meter (Li-3000, Li-Cor, Inc., Lincoln, NE, USA) on 19 May 2010.
Leaf Photosynthesis and Respiration Properties
Leaf net photosynthetic rates and respiration rates (expressed as loss of carbon) were measured at the early grain-filling stage (19 May) in daytime (between 09:00 and 11:00) and nighttime (between 23:00 and 01:00) by a portable photosynthesis system (Li-6400, Li-Cor, Inc.), respectively, in 2010. When measuring net photosynthetic rates and respiration rates, the photosynthetic photon flux density, provided by a 6400-02 LED light source, was set to 1,200 and 0 μmol m−2, respectively. The temperature and CO2 concentration in the leaf cuvette were set to 25 °C and 370 ppm (ambient CO2 concentration in the field), respectively. The humidity was kept similar to natural field conditions of each plot (Turnbull and others 2002; Whitehead and others 2004). Five flag leaves of the main stem were selected in each plot for both rate determinations.
Determination of Soluble Sugar and Starch Concentrations
Fifteen culms of plant samples were sampled from each plot after sunset (18:00) on 18 May and 19 May and before sunrise (06:00) on 19 May 2010, and the top three leaves were taken from the plant to measure soluble sugar and starch concentrations. Soluble sugar was determined by the anthrone method (Li 2000) using sucrose as the standard. Dry samples (0.1 g) were placed in a 25-mL cuvette containing 10 mL distilled water, allowed to stand at 100 °C for 1 h, and filtered into 50-mL volumetric flasks. The reaction mixture of 7.5 mL contained 0.5 mL extract, 0.5 mL mixed reagent (1 g anthrone + 50 mL ethyl acetate), 5 mL H2SO4 (98 %), and 1.5 mL distilled water. The mixture was heated at 100 °C for 1 min and the absorbance was read at 630 nm using a UV-1800 spectrophotometer (Shimadzu Corporation, Kyoto, Japan). Starch was determined by the anthrone method (Li 2000) with sucrose as the standard. The remainder of measured soluble sugar was transferred to a 25-mL cuvette containing 10 mL distilled water and 1.0 mL HClO4 (9.2 mol L−1). The cuvette was placed in a boiling water bath for 30 min, cooled to 30 °C, and filtered into 50-mL volumetric flasks. The reaction mixture of 7.5 mL contained 2 mL extract, 0.5 mL mixed reagent (1 g anthrone + 50 mL ethyl acetate), 5 mL H2SO4 (98 %), and 1.5 mL distilled water. The mixture was heated at 100 °C for 1 min and absorbance was read at 630 nm.
All data were analyzed using Excel 2003 and the statistical package SPSS 11.5 to test the significance of the experiments. The means were separated using Tukey’s least significant difference at an alpha level of 0.05. If there was no significant difference between the treatments for a parameter, then the values from all the experiments for that parameter were used to obtain the mean and error.
Results and Discussion
Impact of Warming on Wheat Canopy Temperature and Soil Moisture
Impact of Warming on Wheat Phenophases
Responses of wheat phenophase date and period length to nighttime warming
Phenophase date (dd/mm/yy)
Length of phenophase period (days)
Entire growth period
207 ± 0.3a
37 ± 0.6b
244 ± 0.3a
200 ± 0.3b
43 ± 0.6a
243 ± 0.3a
206 ± 0.3a
35 ± 0.3b
241 ± 0.6a
199 ± 0.3b
41 ± 0.3a
240 ± 0.3a
208 ± 0.6a
36 ± 0.3b
244 ± 0.3a
203 ± 0.3b
39 ± 0.0a
242 ± 0.3b
The differences in the background air temperatures among the study sites may mainly contribute to the different responses of wheat phenophase to warming. In the region of North China, daily minimum temperatures are commonly lower than 10 °C during the preanthesis phase, and daily maximum temperature increases quickly to more than 25 °C during the postanthesis phase (Shah and Paulsen 2003; Liu and Kang 2006; Zhong and others 2008). It is well known that the wheat anthesis date is related more to daily minimum temperature and accumulated temperature and maturity date is related more to daily maximum temperature (Porter and Gawith 1999). At the experimental site, wheat anthesis is often delayed by a relatively low preanthesis temperature and the maturity date is advanced by a high postanthesis temperature, especially the dry-hot wind weather that occurs there. An increase of 1.1 °C in nighttime temperature can greatly enhance the preanthesis daily minimum temperature and accumulated temperature at the study site. Thus, the wheat development rate was accelerated (Table 1). Instead of increasing the daily maximum temperature, this nighttime warming can shift the postanthesis phase to more optimal temperature conditions due to earlier anthesis as compared with the unwarmed plots (Porter and Gawith 1999), consequently resulting in an extension of the postanthesis period. Based on historical data analysis, Xiao and others (2013) reported that the winter wheat preanthesis period had been shortened by 2.7 days and the length of the postanthesis period remained almost unchanged over the past decades in North China, and the historical changes of the length of the winter wheat phenophase period were mostly because of adaptations to global warming through breeding of new varieties of wheat. Recently, Tian and others (2012) also found that an increase of less than 1.5 °C in the daily mean temperature could significantly shorten the preanthesis phase but extend the postanthesis phase in East China. A warming-led extension of the post-anthesis period may benefit winter wheat yield because postanthesis carbon assimilation contributes to the main parts of grain weight (Yang and others 2008).
Impact of Warming on Leaf Area and Carbon Metabolism
Temperature is also the key factor in source activity (that is, leaf respiration and photosynthesis rates) (Fig 3b, c). The nighttime respiration rates were significantly higher in the warmed plots (2.92 and 1.29 μmol CO2 m−2 s−1) than in the unwarmed plots (2.54 and 0.67 μmol CO2 m−2 s−1) at the flowering and the grain-filling stages, respectively (Fig. 3b). However, warming-led stimulation of nighttime respiration may promote daytime photosynthesis (Kanno and others 2009). The net photosynthesis rates were also significantly higher in the warmed plots (27.4 and 20.8 μmol CO2 m−2 s−1) than in the unwarmed plots (20.8 and 18.0 μmol CO2 m−2 s−1) (Fig. 3c). Moreover, warming-led enhancement of the photosynthesis rate was significantly greater than the stimulation of nighttime respiration. Recently, Kanno and others (2009) also found that warming-led stimulation of nighttime respiration of rice leaves could be partially compensated for by warming-led promotion of daytime photosynthesis. It is likely that the negative impact of nighttime warming on source activity may be compensated for by the positive effects.
Impact of Warming on Grain Filling and Grain Weight
Wheat aboveground biomass, grain yield, yield components, and grain filling rate under the warmed and unwarmed plots
Aboveground biomass (103 kg ha−1)
Grain yield (103 kg ha−1)
Productive spike No. (plants m−2)
Filled grain (grains spike−1)
1,000-grain weight (g)
Grain filling rate (mg grain−1 day−1)
1329.9 ± 52.30b
649.6 ± 27.38b
462.9 ± 2.60a
37.4 ± 1.22a
38.2 ± 1.03b
1.27 ± 0.14a
1.30 ± 0.12a
1519.3 ± 41.20a
763.6 ± 67.94a
447.9 ± 3.82b
42.1 ± 3.83a
43.3 ± 0.72a
1.30 ± 0.07a
1.40 ± 0.01a
1343.5 ± 28.02b
533.2 ± 28.87a
412.5 ± 10.66a
32.3 ± 0.88a
47.8 ± 0.53b
1.33 ± 0.04a
0.90 ± 0.03a
1494.5 ± 46.03a
590.1 ± 16.39a
406.0 ± 6.83a
33.2 ± 0.32a
50.3 ± 0.08a
1.34 ± 0.03a
1.10 ± 0.12a
1664.1 ± 38.93a
610.0 ± 5.71b
450.0 ± 7.37a
24.9 ± 0.28a
47.8 ± 0.26a
1856.0 ± 75.99a
653.7 ± 9.54a
464.5 ± 12.21a
26.4 ± 0.12a
48.5 ± 0.29a
Many studies have reported that and increase in temperature can stimulate the grain-filling rate but with a large reduction in filling time (Bhullar and Jenner 1985; Savin and Nicolas 1996; Tahir and Nakata 2005; Gregersen and others 2008). The negative effects of high temperature on grain-filling duration could not be compensated for by its positive effects on grain-filling rate, consequently resulting in a large reduction in grain weight. In the present experiment, nighttime warming significantly prolonged grain-filling duration (that is, the length of the postanthesis period) (Table 1) with an increase in grain-filling rate (Table 2). Thus, nighttime warming led to a significant increase in the 1,000-grain weight and grain yield (Table 2). The differences in the responses of grain-filling duration between our observations and previous studies are likely the result of the different warming regimens. First, previous observations have focused mainly on the effect of high-temperature stress on wheat grain growth (Slafer and Rawson 1995; Savin and Nicolas 1996; Tahir and Nakata 2005). The experimental temperatures were often set higher than 35 °C, which might accelerate wheat maturity due to heat stress. In the present experiment, an increase of 1.1 °C in nighttime temperature did not lead to heat stress on grain filling because the background temperature is relative low at the study site. Second, most of previous observations were conducted for a short period, such as the postanthesis phase; thus, there were no changes in wheat phenophase caused by warming. Our experiment was conducted for an entire growth period, resulting in a large reduction in the preanthesis period (Table 1). Early anthesis can shift the wheat postanthesis phase to a more optimal temperature condition for leaf photosynthesis and grain filling. Thus, instead of shortening the duration of grain-filling, our nighttime warming prolonged grain-filling duration in North China (Table 1). Savin and Nicolas (1996) also found that an optimal air temperature during the post-anthesis phase could greatly benefit barley grain filling in Australia.
This study evaluated the actual responses of (1) winter wheat phenophases, (2) leaf carbon metabolism, and (3) grain filling to nighttime temperature increases to learn the impact of predicted climatic warming on wheat production in North China. We found a consistent impact of nighttime warming on winter wheat growth across the 3 years of the experiment, though the sizes of the impact were different. Even a moderate increase of 1.1 °C in nighttime air temperature could significantly advance wheat anthesis, resulting in a large decrease of the preanthesis period. The length of the postanthesis period, however, was prolonged by this warming due to the warming-led earlier anthesis. Consequently, the length of the entire growth period remained almost unchanged compared to that of the unwarmed control. Due to the enlargement of the postanthesis leaf area and the compensating effects of daytime photosynthesis on nighttime respiration, aboveground biomass production was significantly enhanced by nighttime warming. Warming-led earlier anthesis shifted the postanthesis phase to more optimal temperature conditions; thus, nighttime warming tended to stimulate the filling rate of wheat grain, especially the inferior grain. In addition to extending the duration of grain-filling, great increments of the 1,000-wheat grain weight and yield were found in this experiment. Nighttime warming cannot really mimic climatic warming with the great increase of daily minimum temperature, and the PNW facility cannot completely avoid light interception by the curtain covering. Thus, there may be some influences on our results. However, decrease in radiation due to the curtain covering and nighttime warming may theoretically be detrimental to wheat growth, so our results may underestimate the positive effects of a daily minimum temperature increase on wheat growth. According to the projections of climate models, the air temperature may increase less than 1.5 °C in North China by 2050. Our observations indicate that wheat production in North China may benefit from predicted climatic warming. This study will help to evaluate food production under future climates, and there needs to be more effort to use the positive effects of climatic warming on winter wheat growth through breeding new varieties and agronomic innovation.
This work was supported by the National Basic Research Program of China (2010CB951501), the National Key Technology Support Program of China (2011BAD16B14), and the Chinese Nature Science Foundation of (30771278, 31201179).