Scholarly article on topic 'Warming decreases photosynthates and yield of soybean [Glycine max (L.) Merrill] in the North China Plain'

Warming decreases photosynthates and yield of soybean [Glycine max (L.) Merrill] in the North China Plain Academic research paper on "Agriculture, forestry, and fisheries"

CC BY-NC-ND
0
0
Share paper
Academic journal
The Crop Journal
OECD Field of science
Keywords
{"Global warming" / Phenology / "Soluble sugar" / "Soybean production" / Starch}

Abstract of research paper on Agriculture, forestry, and fisheries, author of scientific article — Lixia Zhang, Lili Zhu, Mengyang Yu, Mingxing Zhong

Abstract Understanding the responses of field crops such as soybean to climate warming is critical for economic development and adaptive management of food security. A field warming experiment was conducted using infrared heaters to investigate the responses of soybean phenology, photosynthetic characteristics, and yield to climate warming in the North China Plain. The results showed that 0.4°C and 0.7°C increases in soybean canopy air and soil temperature advanced anthesis stage by 3.8days and shortened the length of entire growth stage by 4.5days. Warming also decreased the leaf photosynthetic rate by 6.6% and 10.3% at the anthesis and seed filling stages, respectively, but increased the leaf vapor pressure deficit by 9.4%, 15.7%, and 14.1% at the anthesis, pod setting, and seed filling stages, respectively. However, leaf soluble sugar and starch were decreased by 25.6% and 20.5%, respectively, whereas stem soluble sugar was reduced by 12.2% at the anthesis stage under experimental warming. The transportation amount of leaf soluble sugar and contribution rate of transportation amount to seed weight were reduced by 58.2% and 7.7%, respectively, under warming. As a result, warming significantly decreased 100-seed weight and soybean yield by 20.8% and 45.0%, respectively. Our findings provide better mechanistic understanding of soybean yield response to climate warming and could be helpful for forecasting soybean yield under future climate warming conditions.

Academic research paper on topic "Warming decreases photosynthates and yield of soybean [Glycine max (L.) Merrill] in the North China Plain"

CJ-00145; No of Pages 8

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX

HOSTED BY

ELSEVIER

Available online at www.sciencedirect.com

ScienceDirect

Warming decreases photosynthates and yield of soybean [Glycine max (L.) Merrill] in the North China Plain

Lixia Zhang*, Lili Zhu, Mengyang Yu, Mingxing Zhong

State Key Laboratory of Cotton Biology, Key Laboratory of Plant Stress Biology, College of Life Sciences, Henan Uniuersity, Kaifeng 475004,

ARTICLE INFO

Article history:

Received 27 September 2015 Received in revised form 20 December 2015 Accepted 2 February 2016 Available online 10 February 2016

Keywords: Global warming Phenology Soluble sugar Soybean production Starch

ABSTRACT

Understanding the responses of field crops such as soybean to climate warming is critical for economic development and adaptive management of food security. A field warming experiment was conducted using infrared heaters to investigate the responses of soybean phenology, photosynthetic characteristics, and yield to climate warming in the North China Plain. The results showed that 0.4 °C and 0.7 °C increases in soybean canopy air and soil temperature advanced anthesis stage by 3.8 days and shortened the length of entire growth stage by 4.5 days. Warming also decreased the leaf photosynthetic rate by 6.6% and 10.3% at the anthesis and seed filling stages, respectively, but increased the leaf vapor pressure deficit by 9.4%, 15.7%, and 14.1% at the anthesis, pod setting, and seed filling stages, respectively. However, leaf soluble sugar and starch were decreased by 25.6% and 20.5%, respectively, whereas stem soluble sugar was reduced by 12.2% at the anthesis stage under experimental warming. The transportation amount of leaf soluble sugar and contribution rate of transportation amount to seed weight were reduced by 58.2% and 7.7%, respectively, under warming. As a result, warming significantly decreased 100-seed weight and soybean yield by 20.8% and 45.0%, respectively. Our findings provide better mechanistic understanding of soybean yield response to climate warming and could be helpful for forecasting soybean yield under future climate warming conditions.

© 2016 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Global mean air temperature has increased by about 0.74 °C over the last century and is predicted to increase by 1.1 to 6.4 °C by the end of this century [1]. Changes in temperature have profoundly affected crop growth, development, and yield. Most studies of crops (such as wheat, rice, and maize) have found that climate warming could affect crop phenology [2-4], spikelet sterility [5,6], photosynthesis and carbon metabolism [7-10], yield, and quality

[11-15]. As the most widely grown legume, soybean is a major source of plant protein and oil and has become an important commodity crop in the word. Future demand for soybean will continue to increase due to world population increase, dietary change, and edible oil demand [16]. Better understanding of responses of soybean growth and yield to climate warming will facilitate strategy development for future food security.

The effects of warming on soybean yield have been investigated mostly using crop models and historical data

* Corresponding author. Tel.: +86 371 23881006; fax: +86 371 23882029. E-mail address: zhanglixia_1010@163.com (L. Zhang).

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

http://dx.doi.org/10.1016/j.cj.2015.12.003

2214-5141/© 2016 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

ARTICLE IN PRESS

2 THE CROP JOURNAL XX (2016) XXX - XXX

analyses. For example, crop model studies have suggested that soybean yield is negatively correlated with growing season warming [12,17,18]. Empirical analysis has indicated that warming could decrease soybean yield and that there is an average of 17% reduction in soybean yield for every 1 °C rise in temperature [19]. However, most studies using controlled chambers and greenhouses have found that warming might stimulate soybean yield in a certain temperature range [20] but would reduce yield above the temperature threshold during the seed filling stage [21,22]. Thus, responses of soybean yield to warming remain elusive. Most studies have indicated warming-induced increase and/or decrease in crop yield due to changes in phenological stage [23,24] and leaf photosyn-thetic characteristics [25,26], improvement in sources (leaf area and photosynthesis), and changes in sinks size (number of flowers, pods, seeds, and seed weight) [27,28]. Warming during reproductive growth might also influence pollen or stigma viability, pollen tube growth, and flower fertilization, finally leading to changes in soybean yield [29]. These studies have shown that the underlying mechanisms of warming effects on soybean yield remain complex. It is thus imperative to characterize the actual response of soybean yield to climate warming.

Soybean is one of the major crops in the North China Plain. To date, no field warming experiment has been performed in this region. A warming experiment with infrared heaters was conducted to investigate the responses of soybean phenology, photosynthetic characteristics, and yield to climate warming. The main objectives of this study were 1) to determine the extent to which warming affects soybean photosynthates and yield and 2) to identify the mechanisms responsible for reduction in soybean yield under climate warming.

2. Materials and methods

2.1. Study site

The study was conducted on the on-campus Research and Educational Farm (34°49'N, 114°17'E, 73 m.a.s.l.) of Henan University, Kaifeng, Henan province, China, in 2013. The area has a typical temperate arid climate. Mean annual air temperature is 14.3 °C, with monthly mean temperature ranging from -0.16 °C in January to 27.2 °C in July in the past 60 years (1953-2013) (temperature data were obtained from the Chinese Meteorological Agency, http://cdc.cma.gov.cn/home.do). Mean annual precipitation is 627 mm, of which 87.8% are distributed from April to October. Soil parent material and type are Yellow River sediment and sandy loam, respectively, with 65.7 ± 0.15% sand, 14.1 ± 0.03% silt, and 20.30 ± 0.02% clay. The sandy loam soils contain 11.04 ± 0.16 g kg-1 soil organic carbon, 0.47 ± 0.01 g kg-1 total nitrogen, and 27.20 ± 1.21 mg kg-1 dissolved organic nitrogen. Soil bulk density is 1.31 g cm-3 and soil pH is 8.66.

2.2. Experimental design and agronomic management

The field experiment used a complete randomized block design with two treatments, including ambient temperature as a control (C) and a diurnal warming treatment (W), replicated 6

times per treatment. Twelve plots (3 x 4 m in each plot) were arranged into three rows and four columns. There was 1 m-wide buffer zone between any two plots. In each warming plot, an infrared radiator (165 x 15 cm, Kalglo Electronics, Bethlehem, PA, USA) was suspended 2.25 m above the ground. The heater for the warming treatment was set at a radiation output of approximately 1600 W. This heater can provide about 10 m2 warming area with uniform and reliable warming effects, as reported in the previous study [30]. A dummy heater of the same shape and size was used to mimic the shading effect of the infrared heater in each control plot. The warming treatment was begun on the sowing date and maintained until the harvest date for an entire growing season. All plant samples and field measurements were performed in the approximate 10 m2 area in each plot.

Soybean seed (cv. Zhonghuang13) was obtained from a local seed company and sown on June 1. After seedlings emerged in 5 days, plants were thinned to a density of 24 plants per m2. Herbicides and pesticides were applied as necessary, following local agronomic management practices. Irrigation was generally performed at the anthesis and seed filling stages according to soybean growth demand. Soybeans were harvested on October 6.

2.3. Field measurements

2.3.1. Temperature and moisture

Plant canopy air temperature (Tc) and soil temperature (Ts) were measured with a thermocouple and recorded with automatic data loggers, respectively (Ibutton, DS1922L-F50). Two temperature sensors were placed at the center of each plot. One sensor was positioned in the soybean canopy for air temperature measurement and was gradually raised with the soybean growth. The other sensor was buried 10 cm below the soil surface for soil temperature measurement. The temperature data were stored at 1 h intervals for the entire growing stage. Soil moisture at the depth of 0-10 cm was measured using TDR (this instrument was produced by Sentek Pty Ltd., Balmain, Australia), recorded 6 times per month from June to October in each plot.

2.3.2. Soybean phenophase, biomass growth, and grain yield The phenological stages of soybean include both vegetative (V1-Vn) and reproductive (R1-R8) development stages. The dates of the developmental stages were recorded for each plot, based on the method of a previous study [31]. The entire growing stages of soybean were divided into pre-anthesis and post-anthesis stages. Anthesis, pod setting, seed filling, and maturity stages were defined, respectively, as the times when 50% of plants flowered, pods set, seeds filled, and pods and leaves showed yellow color in each plot.

At the harvest stage, five plant samples were taken from each plot to measure aboveground biomass (AGB). Soybean yield was determined by harvesting a 1 m2 area from each plot by hand. The pod tissues were passed through a thresher to separate the seeds, which were weighed to obtain seed yield (SY). All plant samples were oven-dried at 65 °C for 24 h and weighed. The harvest index (HI) was calculated as HI = SY/AGB.

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX 3

2.3.3. Leaf area, chlorophyll content, uapor pressure deficit, and photosynthetic characteristics

At the anthesis, pod setting, and seed filling stages, the top three unfolded leaves from three plants in each plot were selected to measure leaf length and leaf width using a flexible ruler. Leaf areas were evaluated using the equation (leaf length x leaf width x 0.75) [32]. Estimates of the chlorophyll content of the same leaves were determined with a chlorophyll meter (SPAD-502, Minolta, Osaka, Japan). Leaf vapor pressure deficit (VPD), net photosynthetic rate (Pn), transpiration rate (Tr), and stomatal conductance (Cond) of the same leaves were measured with a Portable Photosynthesis System (Li-Cor 6400, Li-Cor Inc., USA), and the photosynthetic measurements were conducted at 1200 |imol m-2 s-1 radiation intensity on clear mornings (at 09:00-11:00, 3-4 h after sunrise). The mean of three measurements was used to represent the corresponding parameter for each plot.

2.3.4. Accumulation and translocation of leaf and stem soluble sugar and starch

The top three leaves and main stems of soybean were taken from each plot by hand during anthesis and physiological maturity (the end of seed filling) stages, respectively. Plant samples were oven-dried at 65 °C for 24 h to measure photosynthate concentration. Photosynthates including soluble sugar and starch were measured by the anthrone method using sucrose as the standard [10,33].

Based on these measurements, three parameters were used to compare the translocation of photosynthates from leaf and stem to seed between treatment and control plots, defined as follows:

Photosynthate translocation amount (g per plant) = photo-synthate amount at anthesis stage - photosynthate amount at maturity stage.

Photosynthate translocation rate (%) = (photosynthate translocation amount/photosynthate amount at anthesis stage) x 100.

Contribution of photosynthate translocation amount to grain weight (%) = (photosynthate translocation amount/ grain weight at maturity stage) x 100 [8,32,34].

2.4. Statistical analysis

All statistical analyses were performed with SAS software (Version 8.01; SAS Institute Inc., Cary, NC, USA). One-way ANOVA was used to evaluate the effects of the experimental treatment on measured variables. Differences were considered significant at the level of P < 0.05.

3. Results

3.1. Temperature and moisture

During the entire growth season, mean plant Tc under warming was 29.5 °C, with a range from 17.9 to 37.3 °C, 0.4 °C (P < 0.05) higher than the control. Plant Tc tended to increase from anthesis to pod setting stages, and then decreased until the maturity stage (Fig. 1a). Mean Ts under warming was

27.5 °C, with a range from 20.6 to 34.2 °C, 0.7 °C (P < 0.05) higher than the control (Fig. 1b). Mean soil moisture under warming was 7.2% (v/v), with a range from 3.1 to 16.6% (v/v), and showed no significant difference from the control. Soil moisture tended to decline from anthesis to maturity stages (Fig. 1c). However, mean plant Tc and Ts were significantly elevated under warming, and the response trends of plant Tc and Ts were closely consistent with those in the control during the entire growth season. Thus, the infrared radiator was an effective warming heater in the field experiment.

Warming increased the mean cumulative temperature by 38.8 and 44.2 °C (both P < 0.05) at the anthesis and pod setting stages, respectively (Fig. 2a). However, daily mean maximum temperature under warming was 1.8 and 1.6 °C (both P < 0.05) higher than control at the seed filling and maturity stages, respectively (Fig. 2b), and daily mean minimum temperature under warming was 1.7 °C (P < 0.05) higher than control at the anthesis stage (Fig. 2c).

3.2. Soybean phenophase, biomass, and grain yield

Warming advanced anthesis stage of soybean by 3.8 days (P < 0.05) and shortened the length of whole growth stage by 4.5 days (P < 0.05). No marked change in the length of the post-anthesis stage was observed (Table 1). Warming also decreased seed yield by 45.0% (P < 0.05) and reduced the harvest index by 41.0% (P < 0.05). Although warming decreased the 100-seed weight by 20.8% (P < 0.05), there were no significant differences in other yield components (plants per m2, pod number per plant, seed number per plant, and seed weight per plant) between the warming and the control treatments (Table 1).

3.3. Leaf area, chlorophyll content, VPD, and photosynthetic rate

Warming decreased the flag leaf area of soybean by 8.4% (P < 0.05) at the anthesis stage but did not affect flag leaf area at the pod setting and seed filling stages (Fig. 3a). Warming also reduced leaf chlorophyll content by 5.8% and 7.8% (both P < 0.05) at the anthesis and seed filling stages, respectively (Fig. 3b), but increased the leaf VPD by 9.4%, 15.7%, and 14.1% (all P < 0.05) at the anthesis, pod setting, and seed filling stages, respectively (Fig. 3c). However, leaf Pn was 6.6% and 10.3% (both P < 0.05) lower under warming than the control at the anthesis and seed filling stages, respectively (Fig. 3d), but leaf Tr was 7.3% (P < 0.05) higher under warming than the control at the anthesis stage (Fig. 3e). In addition, warming reduced leaf Cond by 18.8% and 18.4% (both P < 0.05) at the anthesis and seed filling stages, respectively (Fig. 3f).

3.4. Accumulation and translocation of soluble sugar and starch

At the anthesis stage, leaf soluble sugar and starch were reduced by 25.6% and 20.5% (both P < 0.05), respectively, under warming (Fig. 4a, b). Stem soluble sugar was decreased by 12.2% (P < 0.05) under warming (Fig. 4c). In addition to reducing soluble sugar and starch, warming decreased the transportation amount of leaf soluble sugar and contribution

ARTICLE IN PRESS

4 THE CROP JOURNAL XX (2016) XXX - XXX

Month/day

Fig. 1 - Effects of warming on plant canopy air temperature (Tc), soil temperature (Ts), and soil moisture. Data are mean ± 1 SE. C, control; W, warming. Dotted lines indicate the main phenological dates under warming and control treatments.

rate of transportation amount to seed weight by 58.2% and 7.7% (both P < 0.05), respectively (Fig. 5a, c). No significant changes in transportation of stem soluble sugar to seed were observed (Fig. 5d, e, f).

4. Discussion

4.1. Effects of warming on soybean photosynthates

Better understanding of source-sink relationship and photo-synthates allocation could be very helpful for studying response mechanisms of crop yield. The growth of crop sink organs can be limited either by photosynthate supply from source leaves (source limitation) or by capacity of the sink to utilize the photosynthates (sink limitation) [35-37]. Green leaves of crops post-anthesis are the major sources of carbon assimilates for grain filling, and more than half of carbohydrate accumulation in grain is derived from photosynthesis post-anthesis [8,10,38]. In our study, warming decreased the source size (flag leaf area) as well as source activity (leaf photosynthetic rate) at the anthesis and seed filling stages (Fig. 3a, d). As a result, both leaf and stem soluble sugar and leaf starch were reduced (Fig. 4a, b, c). The transportation

amount of leaf soluble sugar and contribution rate of transportation amount to seed weight also decreased under warming (Fig. 5a, c). This process finally led to reduction in soybean yield (Table 1). Thus, source limitation under warming can lead to a reduced sink (seed filling, seed yield). Our findings confirm that source limitation plays an important role in the formation of soybean yield.

Theoretical analysis has indicated that a large and strong source (leaf area and photosynthesis) can contribute greatly to sink formation and growth (seed number and seed weight) [10,37]. By contrast, a weak source is not beneficial for sink development. The negative impacts of warming on leaf area and photosynthetic rate are in accord with warming-induced inhibition of photosynthates accumulation of leaf and stem and translocation to seed in our study. These findings were consistent with the source-sink relationship theory. However, sinks may also affect source activity [10]. In our study, warming-induced reduction in photosynthate translocation to seed may also decrease leaf soluble sugar and starch consumption, with consequent feedback to inhibit leaf photosynthesis. This process may likewise lead to losses in soybean yield. However, warming could affect seed yield of soybean through improvement in sources (leaf area and photosynthesis) and changes in sink size [27,28]. As a result, source-sink

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX

□ C □ W

Anthesis Pod setting Seed filling Maturity Growth stage

Fig. 2 - Effects of warming on cumulative, daily mean maximum, and minimum temperatures during the main phenological stages of soybean. Data are mean ± 1 SE. C, control; W, warming. Different letters at the same phenological stage indicate significant difference at the 0.05 level.

in phenological stage could affect soybean yield. However, warming advanced the anthesis stage of soybean and shortened the length of entire growth stage (Table 1). Thus, the negative effect of warming on soybean yield in our study maybe explained by the advance of the anthesis stage, leading to an encounter with heat and drought stress (at about 37 °C) at the post-anthesis stage under warming. Moreover, the concomitant increases of vapor pressure deficit and temperature could exacerbate the drying effects on soybean growth and yield and lead to reductions in photosynthetic rate and yield formation (fertile pods, seed number, and seed size) [25]. In the present study, warming increased leaf VPD at the anthesis, pod setting, and filling stages and led to decreases in leaf photosynthetic rates and yield (Table 1; Fig. 3c, d). In addition, the decreases in 100-seed weight and harvest index of soybean may have contributed to yield reduction.

Yield formation of crop is derived from two sources: (1) leaf photosynthesis post-anthesis and (2) translocation and allocation of photosynthates from stem and sheath storage to grain post-anthesis [35,36,38]. Our results showed that the leaf photosynthetic rate of soybean declined rapidly at post-anthesis and remained at a lower level at the seed filling stage under warming (Fig. 3d). However, there was also lower leaf photosynthate accumulation and translocation to seed from flowering to maturity stages under warming (Fig. 4a, b; Fig. 5a, c). These findings indicate that potential mechanisms of yield reduction of soybean are both reduced leaf photosynthesis and inhibited photosynthate allocation to seed at the post-anthesis stage.

5. Conclusion

In this field study, soybean yield in the North China Plain was reduced under warming. The decrease in soybean yield could be attributed to at least three factors: 1) warming advanced anthesis stage of soybean and shortened the length of entire growth stage. As a result, soybean had less time to grow, develop, and mature; 2) warming decreased leaf photosynthetic rate at the anthesis and seed filling stages and reduced soluble

Table 1 - Effects of warming on length of phenological stage, biomass production, seed yield, and yield components of soybean.

relationships are co-limiting in photosynthesis and photosyn-thate partitioning in soybean.

4.2. Effects of warming on soybean yield

The optimum temperatures for soybean are 15-22 °C at the emergence stage, 20-25 °C at the flowering stage, and 15-22 °C at the maturity stage [36]. Seed yield and yield formation of soybean are frequently reduced by temperatures above approximately 30 °C [22,39]. In the present study, mean air temperatures ranged from 20 to 37 °C under warming from anthesis to maturity stages (Fig. 1a), above the optimum temperature ranges of soybean growth. Thus, warming was not beneficial for soybean yield.

Shortened phenological stages could result in decreased crop yield [2,23]. Alternatively, concomitant increases of temperature and vapor pressure deficit may delay the flowering, seed filling, and pod setting stages and also lead to a reduction in soybean yield [25,27]. These studies indicate that change

Variable Control Warming

Pre-anthesis (days) 44.67 ± 1.48 a 40.83 ± 0.75 b

Post-anthesis (days) 74.83 ± 2.09 a 74.17 ± 1.14 a

Length of entire growth 119.50 ± 1.20 a 115.00 ± 1.37 b

stage (days)

Plant density (plant per m2) 22.33 ± 0.88 a 20.83 ± 0.60 a

Pod number per plant 76.87 ± 5.19 a 68.83 ± 3.88 a

Seed number per plant 44.03 ± 11.49 a 39.23 ± 13.90 a

Seed mass per plant (g) 9.60 ± 1.73 a 9.38 ± 1.08 a

100-seed weight (g) 15.02 ± 1.21 a 11.89 ± 0.30 b

Aboveground biomass (g m-2) 979.10 ± 44.60 a 895.79 ± 57.40 a

Yield (g m-2) 379.87 ± 3.04 a 209.09 ± 15.44 b

Harvest index (%) 0.39 ± 0.02 a 0.23 ± 0.01 b

Data are mean ± SE. Different letters in the same row indicate significant difference at the 0.05 probability level.

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX

Q CL > 1

a. 2 о

30 1 ел

06 ô E

0.3 <5

Anthesis Pod setting Seed filling Anthesis Pod setting Seed filling Growthstage

Fig. 3 - Effects of warming on leaf area, chlorophyll content, vapor pressure deficit (VPD), photosynthetic rate (Pn), transpiration rate (Tr), and stomatal conductance (Cond) of soybean. Data are mean ± SE. C, control; W, warming. Different letters at the same phenological stage indicate significant difference at the 0.05 level.

0) 1 150

« -S- 100

Anthesis Maturity Anthesis

Growth stage

Maturity

_(D 1 20 -§ 1 ^ d)

Fig. 4 - Effects of warming on soluble sugar and starch accumulation in leaf and stem of soybean. Data are mean ± 1 SE. C, control; W, warming. Different letters at the same phenological stage indicate significant difference at the 0.05 level.

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX

Hz с «

ГО CD

■с о. o. Я 1.0

(Л „ § §

.2 го

£= О

О ■

с <л £= ГО

£= О

1= о О

0.0 40

.2 Œ го Ф ■с о.

& S <л „

§ !i - I

.2 го

£= О

tz о^

.2 го

£= О

1= о О

Leaf soluble sugar

Stem soluble sugar

Fig. 5 - Effects of warming on translocation of leaf and stem soluble sugar of soybean. Data are mean ± SE. C, control; W, warming. Different letters between warming and control indicate significant difference at the 0.05 level.

sugar and starch in leaf and stem. Consequently, less biomass was produced under warming; and 3) warming reduced the transportation of leaf soluble sugars to seeds, reducing the harvest index and 100-seed weight. These findings not only improve our understanding of soybean yield response to climate warming but also provide useful information for developing more strategies (such as new variety breeding and agronomic innovation) for adapting soybean yield to future climate change.

Acknowledgments

We thank Shiqiang Wan at Henan University for designing the experiment and Dafeng Hui at Tennessee State University for technical review of the manuscript. This study was financially supported by Scientific Innovation Talent of Henan Province (114200510016).

REFERENCES

[1] IPCC, Climate Change 2007: The physical science basis, in: S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller (Eds.), Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom and New York, USA 2007, pp. 1-996.

F.L. Tao, M. Yokozawa, Y.L. Xu, Y. Hayashi, Z. Zhang, Climate changes and trends in phenology and yields of field crops in China, 1981-2000, Agric. For. Meteorol. 138 (2006) 82-92. P.Q. Craufurd, T.R. Wheeler, Climate change and the flowering time of annual crops, J. Exp. Bot. 60 (2009) 2529-2539.

J.W. White, B.A. Kimball, G.W. Wall, M.J. Ottman, L.A. Hunt, Responses of time of anthesis and maturity to sowing dates and infrared warming in spring wheat, Field Crops Res. 124 (2011) 213-222.

R. Wassmann, S.V.K. Jagadish, S. Heuer, A. Ismail, E. Redona, R. Serraj, R.K. Singh, G. Howell, H. Pathak, K. Sumfleth, Climate change affecting rice production: the physiological and agronomic basis for possible adaptation strategies, Adv. Agron. 101 (2009) 59-122.

F. Shah, J.L. Huang, K.H. Cui, L.X. Nie, T. Shah, C. Chen, K. Wang, Impact of high-temperature stress on rice plant and its traits related to tolerance, J. Agric. Sci. 149 (2011) 545-556. J. Kobza, G.E. Edwards, Influences of leaf temperature on photosynthetic carbon metabolism in wheat, Plant Physiol. 83 (1987) 69-74.

I.S.A. Tahir, N. Nakata, Remobilization of nitrogen and carbohydrate from stems of bread wheat in response to heat stress during grain filling, J. Agron. Crop Sci. 191 (2005) 106-115.

C.M. Cossani, M.P. Reynolds, Physiological traits for improving heat tolerance in wheat, Plant Physiol. 160 (2012) 1710-1718.

[10] J. Chen, Y.L. Tian, X. Zhang, C.Y. Zheng, Z.W. Song, A.X. Deng, W.J. Zhang, Nighttime warming will increase winter wheat yield through improving plant development and grain growth in North China, J. Plant Growth Regul. 33 (2014) 397-407.

ARTICLE IN PRESS

THE CROP JOURNAL XX (2016) XXX - XXX

[11] S.B. Peng, J.L. Huang, J.E. Sheehy, R.C. Laza, R.M. Visperas, X.H. Zhong, G.S. Centeno, G.S. Khush, K.G. Cassman, Rice yields decline with higher night temperature from global warming, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9971-9975.

[12] D.B. Lobell, M.B. Burke, C. Tebaldi, M.D. Mastrandrea, W.P. Falcon, R.L. Naylor, Prioritizing climate change adaptation needs for food security in 2030, Science 319 (2008) 607-610.

[13] M.J. Ottman, B.A. Kimball, J.W. White, G.W. Wall, Wheat growth response to increased temperature from varied planting dates and supplemental infrared heating, Agron. J. 104 (2012) 7-16.

[14] S.B. Fang, H. Su, W. Liu, K.Y. Tan, S.X. Ren, Infrared warming reduced winter wheat yields and some physiological parameters, which were mitigated by irrigation and worsened by delayed sowing, PLoS One 8 (2013), e67518.

[15] Y.L. Tian, C.Y. Zheng, J. Chen, C.Q. Chen, A.X. Deng, Z.W. Song, B.M. Zhang, W.J. Zhang, Climatic warming increases winter wheat yield but reduces grain nitrogen concentration in East China, PLoS One 9 (2014), e95108.

[16] FAO, FAO Statistical Databases. Food and Agriculture Organization of the United Nations, http://faostat.fao.org 2013 (May 1, 2015).

[17] R.K. Mall, M. Lal, V.S. Bhatia, L.S. Rathore, R. Singh, Mitigating climate change impact on soybean productivity in India: a simulation study, Agric. For. Meteorol. 121 (2004) 113-125.

[18] C.J. Kucharik, S.P. Serbin, Impacts of recent climate change on Wisconsin corn and soybean yield trends, Environ. Res. Lett. 3 (2008) 034003.

[19] D.B. Lobell, G.P. Asner, Climate and management contributions to recent trends in U.S. agricultural yields, Science 299 (2003) 1032.

[20] N. Sionit, B.R. Strain, E.P. Flint, Interaction of temperature and CO2 enrichment on soybean: photosynthesis and seed yield, Can. J. Plant Sci. 67 (1987) 629-636.

[21] D.L. Dornbos Jr., R.E. Mullen, Influence of stress during soybean seed fill on seed weight, germination, and seedling growth rate, Can. J. Plant Sci. 71 (1991) 373-383.

[22] L.R. Gibson, R.E. Mullen, Influence of day and night temperature on soybean seed yield, Crop Sci. 36 (1996) 98-104.

[23] Y. Liu, E.L. Wang, X.G. Yang, J. Wang, Contributions of climatic and crop varietal changes to crop production in the North China Plain, since 1980s, Glob. Chang. Biol. 16 (2010) 2287-2299.

[24] P.Q. Craufurd, V. Vadeza, K.S.V. Jagadish, P.V.V. Prasad, M. Zaman-Allaha, Crop science experiments designed to inform crop modeling, Agric. For. Meteorol. 170 (2013) 8-18.

[25] C.R.P. Tacarindua, T. Shiraiwa, K. Homma, E. Kumagai, R. Sameshima, The effects of increased temperature on crop growth and yield of soybean grown in a temperature gradient chamber, Field Crops Res. 154 (2013) 74-81.

[26] U.M. Ruiz-Vera, M. Siebers, S.B. Gray, D.W. Drag, D.M. Rosenthal, B.A. Kimball, D.R. Ort, C.J. Bernacchi, Global

warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the Midwestern United States, Plant Physiol. 162 (2013) 410-423.

[27] C.R.P. Tacarindua, T. Shiraiwa, K. Homma, E. Kumagai, R. Sameshima, The response of soybean seed growth characteristics to increased temperature under near-field conditions in a temperature gradient chamber, Field Crops Res. 131 (2012) 26-31.

[28] E. Kumagai, R. Sameshima, Genotypic differences in soybean yield responses to increasing temperature in a cool climate are related to maturity group, Agric. For. Meteorol. 265-272 (2014).

[29] M. Thuzar, A.B. Puteh, N.A.P. Abdullah, M.B.M. Lassim, K. Jusoff, The effects of temperature stress on the quality and yield of soybean [(Glycine max L.) Merrill.], J. Agric. Sci. 2 (2010) 172-179.

[30] S.Q.. Wan, J.Y. Xia, W.X. Liu, S.L. Niu, Photosynthetic overcompensation under nocturnal warming enhances grassland carbon sequestration, Ecology 90 (2009) 2700-2710.

[31] W.R. Fehr, C.F. Caviness, D.T. Burmood, J.S. Pennington, Stage of development descriptions for soybeans, Glycine max (L.) Merrill, Crop Sci. 11 (1971) 929-931.

[32] X.C. Chen, F.J. Chen, Y.L. Chen, Q. Gao, X.L. Yang, L.X. Yuan, F.S. Zhang, G.H. Mi, Modern maize hybrids in Northeast China exhibit increased yield potential and resource use efficiency despite adverse climate change, Glob. Chang. Biol. 19 (2013) 923-936.

[33] H.S. Li, Principles and Techniques of Plant Physiological Biochemical Experiment, Higher Education Press, Beijing, 2000.

[34] W.J. Dong, J. Chen, B. Zhang, Y.L. Tian, W.J. Zhang, Responses of biomass growth and grain yield of midseason rice to the anticipated warming with FATI facility in East China, Field Crops Res. 123 (2011) 259-265.

[35] H. Schnyder, The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling, New Phytol. 123 (1993) 233-245.

[36] X.B. Liu, J. Jin, G.H. Wang, S.J. Herbert, Soybean yield physiology and development of high-yielding practices in Northeast China, Field Crops Res. 105 (2008) 157-171.

[37] H.P. Zhang, N.C. Turner, M.L. Poole, Source-sink balance and manipulating sink-source relations of wheat indicate that the yield potential of wheat is sink-limited in high-rainfall zones, Crop Pasture Sci. 61 (2010) 852-861.

[38] W. Yang, S.B. Peng, M.L. Dionisio-Sese, R.C. Laza, R.M. Visperas, Grain filling duration, a crucial determinant of genotypic variation of grain yield in field-grown tropical irrigated rice, Field Crops Res. 105 (2008) 221-227.

[39] W. Schlenker, M.J. Roberts, Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 15594-15598.