Journal of Plant Growth Regulation

, Volume 33, Issue 2, pp 397–407

Nighttime Warming Will Increase Winter Wheat Yield Through Improving Plant Development and Grain Growth in North China

Authors

  • Jin Chen
    • Institute of Applied EcologyNanjing Agricultural University
  • Yunlu Tian
    • Institute of Applied EcologyNanjing Agricultural University
  • Xin Zhang
    • Institute of Applied EcologyNanjing Agricultural University
    • Institute of Crop ScienceChinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture
  • Chengyan Zheng
    • Institute of Crop ScienceChinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture
  • Zhenwei Song
    • Institute of Crop ScienceChinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture
  • Aixin Deng
    • Institute of Crop ScienceChinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture
    • Institute of Applied EcologyNanjing Agricultural University
    • Institute of Crop ScienceChinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology & Ecology, Ministry of Agriculture
Article

DOI: 10.1007/s00344-013-9390-0

Cite this article as:
Chen, J., Tian, Y., Zhang, X. et al. J Plant Growth Regul (2014) 33: 397. doi:10.1007/s00344-013-9390-0

Abstract

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.

Keywords

Global warmingWheat phenophaseCarbohydrate metabolismGrain weightPassive nighttime warmingNorth China

Introduction

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

Site Descriptions

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.

Crop Management

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.

One hundred spikes that headed on the same day were chosen and tagged for each treatment. The flowering date and the position of each spikelet on the tagged panicles were recorded. Ten tagged spikes from each treatment were sampled every 7 days from anthesis to maturity. The spikes were stripped to grains and further separated into superior, inferior, and other grains (Jiang and others 2003). From the basal 5–12 spikelets on the spikes, the first and second basal grains on each spikelet were detached as superior grains and the remaining distal grains on the same spikelet were detached as inferior grain. All grains were separately oven-dried at 70 °C for 48 h to a constant weight to investigate grain-filling rate. The grain-filling process was fitted by Richards’ (1959) growth equation as described by Zhu and others (1988):
$$ W = A/\frac{A}{{(1 + Be^{ - kt} )^{1/N} }}. $$
(1)
Grain-filling rate (G) was calculated as the derivative of Eq. 1:
$$ G = \frac{{AKBe^{ - kt} }}{{N(1 + Be^{ - kt} )^{(N + 1)/N} }}, $$
(2)
where W is the grain weight (mg), A is the final grain weight (mg), t is the time after anthesis (days), and B, k, and N are coefficients determined by regression. The active grain-filling period was defined as when W was 1 % (t1) to 99 % (t2) of A. The average grain-filling rate during this period was calculated from t1 to t2.

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.

Data Analysis

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

The novel PNW facility has been widely used to observe plant responses to an increase in daily minimum temperature at the ecosystem scale under field conditions (Zeiher and others 1994; Beier and others 2004). Although the warming level using the PNW facility cannot be very high, it is enough to simulate the temperature increase predicted to occur during the next decades (Fig. 1a). The PNW facility could increase nighttime mean temperature on the wheat canopy by an average of 1.1 °C during the growing season (Fig. 1a). The warming level is within the range of climatic warming predicted to occur by 2050 in North China. Meanwhile, the pattern of diurnal change (Fig. 1b) of nighttime air temperature on the wheat canopy was similar for the warmed and unwarmed plots. Because the curtains were not spread out to cover the field when it rained or snowed, the difference in the mean air temperature between the treatments was relative low on some days (Fig. 1a). Meanwhile, the difference in temperature between the treatments was not constant largely because of the daily radiation changes of the tested site. However, the actual extent of climate warming on different dates and seasons is also uneven (IPCC 2007). Thus, the variations in the warming effect of the PNW facility are acceptable for this field experiment.
https://static-content.springer.com/image/art%3A10.1007%2Fs00344-013-9390-0/MediaObjects/344_2013_9390_Fig1_HTML.gif
Fig. 1

Differences in nighttime mean temperature between the warmed and unwarmed plots over the 2009–2010 growing seasons (a) and diurnal changes of wheat canopy mean air temperatures on May 19, 2010 (b) under the passive nighttime warming facility

Nighttime warming decreased soil water content by 3.2, 5.8, and 1.2 % during the growing seasons of 2007–2008, 2008–2009, and 2009–2010, respectively (Fig. 2). However, the decreases of soil water content were not significant compared to those of the unwarmed control. During the wheat-growing seasons, there was no limitation on soil water for the warmed and unwarmed plots. Moreover, because this PNW facility can be manually controlled, it saves power and money and can be used in fields where power is not available. The effects on the wheat canopy’s air temperature and the soil moisture indicate that this facility is suitable for studying winter wheat responses to climatic warming under field conditions in North China.
https://static-content.springer.com/image/art%3A10.1007%2Fs00344-013-9390-0/MediaObjects/344_2013_9390_Fig2_HTML.gif
Fig. 2

Variations of soil moisture at 0–20-cm layer during the growing seasons of 2007–2008 (a), 2008–2009 (b), and 2009–2010 (c) under the passive nighttime warming facility. Values are mean ± 1 SE

Impact of Warming on Wheat Phenophases

Temperature is a critical factor affecting wheat plant development and growth. In this experiment, an increase of 1.1 °C in nighttime air temperature greatly advanced wheat anthesis, resulting in an average reduction in the length of the preanthesis period of 6 days (p < 0.05) for the duration of the experiment (Table 1). Instead of accelerating wheat maturity, this warming caused an average extension in the length of the postanthesis period of 5 days (p < 0.05) compared to the unwarmed plots. Consequently, the length of the entire wheat growth period remained almost unchanged for the warmed plots compared to the unwarmed plots. Our results were different from previous model predictions (Liu and others 2010; Lobell and others 2012). Liu and others (2010) reported that global warming significantly shortened the entire wheat growth period in North China on average by 4 days decade−1, and Lobell and others (2012) found that even a 2 °C increase of mean air temperature could advance wheat maturity by 9 days in northern India.
Table 1

Responses of wheat phenophase date and period length to nighttime warming

Year

Treatment

Phenophase date (dd/mm/yy)

Length of phenophase period (days)

Sowing

Anthesis

Maturity

Pre-anthesis

Post-anthesis

Entire growth period

2007–2008

Unwarmed

4/Oct/07

28/Apr/08

04/Jun/08

207 ± 0.3a

37 ± 0.6b

244 ± 0.3a

Warmed

21/Apr-08

03/Jun/08

200 ± 0.3b

43 ± 0.6a

243 ± 0.3a

2008-2009

Unwarmed

5/Oct/08

29/Apr/09

03/Jun/09

206 ± 0.3a

35 ± 0.3b

241 ± 0.6a

Warmed

22/Apr/09

02/Jun/09

199 ± 0.3b

41 ± 0.3a

240 ± 0.3a

2009-2010

Unwarmed

10/Oct/09

06/May/10

11/Jun/10

208 ± 0.6a

36 ± 0.3b

244 ± 0.3a

Warmed

01/May/10

09/Jun/10

203 ± 0.3b

39 ± 0.0a

242 ± 0.3b

Average

Unwarmed

 

207a

36b

243a

Warmed

201b

41a

242b

Values are mean ± 1 SE. Values followed by a different letter are significantly different between treatments in each year (p < 0.05)

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

Low temperature, especially the daily minimum temperature, is the key limiting factor to leaf development and expansion of winter wheat in North China (Xiao and others 2013). Thus, even moderate warming at nighttime could enlarge the flag leaf area and the postanthesis green leaves’ area significantly (Fig. 3a). The flag leaf area per plant and postanthesis green leaves’ area were 38.3 and 13.8 % higher (p < 0.05) in the warmed plots than in the unwarmed plots, respectively. The flag leaf and postanthesis green leaves are the main sources of carbohydrates for grain filling, and more than half of accumulation of carbohydrates in grain is from postanthesis photosynthesis (Tahir and Nakata 2005; Yang and others 2008). The enlargement of postanthesis source size (that is, leaf area) suggests that moderate nighttime warming may benefit grain yield formation through improvement of the sink-source balance of the winter wheat plant (Zhang and others 2010).
https://static-content.springer.com/image/art%3A10.1007%2Fs00344-013-9390-0/MediaObjects/344_2013_9390_Fig3_HTML.gif
Fig. 3

The areas of flag leaf and total green leaves (a) and the rates of flag leaf respiration (b) and net photosynthesis (c) under the warmed and unwarmed plots at the flowing stage (May 2, 2010) and the early grain filling stage (19 May 2010). Values are mean ± 1 SE

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.

Warming-led net enhancement in source activity can also be partly confirmed by the diurnal characteristics of postanthesis leaf carbon metabolism (Fig. 4). At the early stage of grain filling, the concentrations of soluble sugar and starch in the top three leaves at 18:00 were higher in the warmed plots than in the unwarmed plots (Fig. 4a). After one night, the corresponding concentrations decreased greatly and were lower at 06:00 in the warmed plots than in the unwarmed plots. During the second daytime, interestingly, the corresponding concentrations increased greatly and were significantly higher at 18:00 again in the warmed plots than in the unwarmed plots (Fig. 4a). Warming-led enhancement in daytime production was significantly higher than the stimulation of nighttime depletion (Fig. 4b). The differences in the diurnal changes of leaf carbohydrates between the treatments indicate that warming-led stimulation of nighttime depletion can be compensated for by warming-led enhancement of daytime production.
https://static-content.springer.com/image/art%3A10.1007%2Fs00344-013-9390-0/MediaObjects/344_2013_9390_Fig4_HTML.gif
Fig. 4

The diurnal changes of leaf soluble carbohydrates (a) and the amounts of nighttime depletion and daytime accumulation of leaf carbohydrates (b) under the warmed and unwarmed plots at the early stage of grain filling (19 May 2010). Data are expressed on a dry-weight basis (DW). Values are mean ± 1 SE

The differences in the diurnal changes in the amounts of leaf carbohydrates between the treatments may also be partly due to the differences in grain-filling rate (that is, sink activity), because nighttime warming caused great differences in grain weight at the early filling stage (Fig. 5). Warming-led stimulation in sink activity can accelerate carbohydrate depletion in the source, thus consequently promoting source activity (Fig. 3c) and daytime carbohydrate production (Fig. 4). The source-sink relationship, which is affected by both genotype and environmental factors, plays an important role in the difference in photosynthesis and photosynthate partitioning of wheat (Herzog 1982; Calderini and others 2006; Zhang and others 2010). A large and strong source contributes greatly to sink formation and growth (that is, grain number and weight), and a strong sink (that is, high grain-filling rate) can also promote source productivity. Our results demonstrate that the negative effects of moderate warming on the source at nighttime can be compensated for by the warming-led positive effects on source size (that is, leaf area) and activity (that is, photosynthesis). Meanwhile, warming-led stimulation of sink activity (that is, grain-filling rate) may also increase carbohydrate consumption in the source, consequently promoting source activity (that is, photosynthesis and respiration rates). This suggests that predicted nighttime warming may not cause tremendous losses in the production of winter wheat in North China.
https://static-content.springer.com/image/art%3A10.1007%2Fs00344-013-9390-0/MediaObjects/344_2013_9390_Fig5_HTML.gif
Fig. 5

Changes in dry weight of the superior grain (a, c) and the inferior grain (b, d) during the growing seasons of 2007–2008 and 2008–2009 under the warmed and unwarmed plots. Values are mean ± 1 SE. DPA, days post anthesis. The tested cultivars were Yangfu 188 during 2007–2008 and Aikang 58 during 2008–2009

Impact of Warming on Grain Filling and Grain Weight

Similar positive effects of nighttime warming on grain weight were found over the study years (Fig. 5; Table 2). The increases in both superior and inferior grain weight were significantly greater in the warmed plots than in the unwarmed plots (Fig. 5). The average filling rates of superior grains and inferior grains were 1.8 and 13.8 % higher on average, respectively, during the growing seasons of 2007–2008 and 2008–2009 in the warmed plots than in the unwarmed plots (Table 2), but the differences were not significant. Meanwhile, the average value of the 1,000-grain weight was 6.3 % higher (p < 0.05) in the warmed plots than in the unwarmed plots, though there were no significant differences in the numbers of productive spikes and filled grains between the treatments (Table 2). Consequently, nighttime warming significantly increased wheat aboveground biomass and grain yield by 12.3 and 12.0 % on average, respectively, across the study years (Table 2).
Table 2

Wheat aboveground biomass, grain yield, yield components, and grain filling rate under the warmed and unwarmed plots

Year

Treatment

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)

Superior

Inferior

2007–2008

Unwarmed

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

Warmed

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

2008–2009

Unwarmed

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

Warmed

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

2009–2010

Unwarmed

1664.1 ± 38.93a

610.0 ± 5.71b

450.0 ± 7.37a

24.9 ± 0.28a

47.8 ± 0.26a

Warmed

1856.0 ± 75.99a

653.7 ± 9.54a

464.5 ± 12.21a

26.4 ± 0.12a

48.5 ± 0.29a

Average

Unwarmed

1445.8b

597.6b

441.8a

31.5a

44.6b

1.30a

1.11a

Warmed

1623.2a

669.1a

439.5a

33.9a

47.4a

1.32a

1.25a

Values are mean ± 1 SE. Values followed by a different letter are significantly different between treatments in each year (p < 0.05). “–” means data are not available because the grain-filling rate was not determined in 2009–2010 growing season

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.

Conclusions

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.

Acknowledgments

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).

Copyright information

© Springer Science+Business Media New York 2013