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Effects of various warming patterns on Cd transfer in soil-rice systems under Free Air Temperature Increase (FATI) conditions
Ecotoxicology and Environmental Safety 168 (2019) 80–87
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Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv
Effects of various warming patterns on Cd transfer in soil-rice systems under Free Air Temperature Increase (FATI) conditions
T
Liqiang Gea,b, Long Canga, , Syed Tahir Ata-Ul-Karima, Jie Yanga,c, Dongmei Zhoua, ⁎
⁎
a
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China Geological Survey of Jiangsu Province, Nanjing 210018, China c University of Chinese Academy of Sciences, Beijing 100049, China b
ARTICLE INFO
ABSTRACT
Keywords: Cadmium Soil Rice Warming patterns Free Air Temperature Increase (FATI)
Global warming has become an important research topic in different disciplines around the world, especially in the fields of environment quality and food security. As a potential problem in soil environments, cadmium (Cd) contamination of rice under global warming conditions has not been thoroughly investigated. In this study, the fate of Cd in soil-rice systems under various warming patterns was studied via pot experiments under Free Air Temperature Increase (FATI) conditions. The patterns of warming included different temperatures (0.5 °C and 0.8 °C), different day-night durations (nighttime, daytime, and the whole day), and different warming stages (WSx) (including WS1 (seedling to tillering), WS2 (jointing to booting), WS3 (heading), WS4 (grain filling to milk ripening)). At harvest, samples of different rice tissues were collected and the Cd concentrations were measured. The results showed that warming significantly increased Cd concentrations in grain by 1.45 and 2.31 times, which was positively correlated with the two temperature increases (0.5 °C and 0.8 °C), respectively. Both daytime and nighttime warming significantly increased the Cd concentration in grain, and the daytime dominated Cd translocation from roots to shoots. In addition, warming in individual growth stages contributed to increases in Cd accumulation in grain by 31.6% (WS1), 15.0% (WS2), 20.6% (WS3), and 32.8% (WS4), respectively. Specifically, warming during the vegetative phase boosted Cd translocation from roots to shoots, while warming during maturation further increased Cd uptake and remobilization into grain. The projected results could provide a new and in-depth understanding of the fate of Cd in soil-rice systems under global warming conditions in Cd contaminated areas.
1. Introduction In recent years, global warming has been widely accepted and thoroughly investigated (Hartmann et al., 2013) because it is endangering human health via direct mortality and morbidity (extreme heat, cold, drought, or storms) by changing air and water quality as well as food security (Patz et al., 2005; Porter, 2005). The majority of previous studies have focused on the effects of global warming on atmospheric and aquatic environmental quality, as well as crop yield security; however, little attention has been paid to soil environmental quality and crop quality security (Tagaris et al., 2009; Wheeler and Von Braun, 2013; Asseng et al., 2015). The worldwide increase of heavy metal pollution in agriculture soils and the problem of higher cadmium (Cd) concentrations in rice grain have received increasing attention from soil chemists, crop scientists, governments and the public because of the widespread occurrence and chronic human exposure to Cd via
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dietary intake in recent years (Meharg et al., 2013; Larson, 2014; Zhao et al., 2015). However, few studies have mentioned the potential influences of warming on Cd accumulation in rice. Therefore, it is essential to understand the Cd uptake and translocation in soil-rice systems under the future scenarios of global warming, for guiding food production. Studies of the plant-metal-soil interaction under climate change have drawn increased attention from researchers and revealed that soil warming could increase heavy metal bioavailability in soil and accumulation in plants (Rajkumar et al., 2013; Cornu et al., 2016; Fu et al., 2018). Additionally, previous studies reported that warming increased the heavy metal accumulation in different plants, including shrubs, herbaceous plants, and submerged plant (Moreno et al., 2002; Fritioff et al., 2005; Li et al., 2012; Sardans et al., 2008). Earlier investigations of wheat revealed that elevated atmospheric temperature could stimulate the Cd uptake by wheat seedlings by changing rhizosphere soil
Corresponding authors. E-mail addresses: [email protected] (L. Ge), [email protected] (L. Cang), [email protected] (D. Zhou).
https://doi.org/10.1016/j.ecoenv.2018.10.047 Received 8 June 2018; Received in revised form 3 October 2018; Accepted 11 October 2018 0147-6513/ © 2018 Elsevier Inc. All rights reserved.
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properties (Jia et al., 2015). Our previous study under Free Air Temperature Increase (FATI) conditions (with just a single season pot experiment without a warming gradient) revealed that simulated atmospheric warming greatly increased Cd accumulation in rice grain (Ge et al., 2016a). To further investigate and confirm the previous results, a novel pot experiment with two warming amplitudes (0.5 °C and 0.8 °C) was conducted under FATI conditions, in this study. Neither global nor regional warming presents with an asymmetrical or incessant style. Both the maximum and minimum daily temperature increase asymmetrically, which induces changes in the diurnal temperature range (DTR) (Hartmann et al., 2013). The different changed amplitudes of day and night temperature would greatly influence the plant growth, especially for crops. For example, Dhakhwa and Campbell (1998) reported that the effects of asymmetric day-night warming on crop production might be less severe than equal day-night warming. Moreover, Peng et al. (2004) found that rice grain yield decreased significantly under higher night temperature. However, few studies have focused on the effects of asymmetric warming on Cd transfer in soil-rice systems. Therefore, in this study, a pot experiment with half day warming treatment was conducted to evaluate the individual contributions of nighttime or daytime warming to Cd accumulation in rice grain. Zhou and Ren (2012) concluded that the reduction of cool days and nights mainly occurred in winter, while warm days and nights primarily increased in autumn and summer. Therefore, global warming generally leads to increases in globally averaged multi-day heat events, rather than equal increases in daily air temperature. Accordingly, warming climates may result in mismatches between key sensitive growth stages and extreme warming climate events. Specifically, under future warming an entire soil-rice system might be exposed to higher temperatures during short growth periods. Laza et al. (2015) reported that the response of rice to warming varied with the period of treatment and that nighttime warming during the reproduction periods led to a direct reduction in rice yield. However, in their investigation, the effects of warming during different reproduction periods on Cd accumulation in rice were ignored. Therefore, the present study utilized a pot experiment with warming at different growth stages to identify the most critical growth stages influencing Cd accumulation in rice grain under warming. By conducting three groups of warming pot experiments (different warming amplitudes, day and night warming, and growth stage warming), this study provided new and in-depth understanding of the mechanisms of Cd uptake and translocation in the soil-rice system. The results presented herein will facilitate development of effective guidance for rice production in Cd contaminated areas under future warming.
(0.535 g) and heading stages (0.43 g), respectively. Each pot was irrigated with deionized water (DIW) and the thickness of the water layer was kept at 5 cm throughout the crop period to fulfill crop water requirements. The weeds in pots were pulled out manually using tweezers as early as possible during experiments. All pot experiments with four replications were conducted in a greenhouse located in Nanjing, Jiangsu Province. Infrared heaters (89 × 15 cm; Kalglo Electronics Inc, USA) were hung about 1.2 m above the soil surface for warming, while dummy heaters were used to simulate shading effects for controls (Luo et al., 2001). The thermocouples were connected to a datalogger (WTHOT1G, China) to monitor the air temperature (30 cm above soil surface) at intervals every half hour. 2.2. Pot experiments In the present study, pot experiments (PE) were divided in three groups, which shared several treatments together as shown in Table S1. Specifically, the control treatment (CT, without warming, under natural temperature) was shared in all pot experiments. Average daily warming by 0.5 °C (W-0.5 °C) treatment was shared in the first and third group (PE-1 and PE-3), and average daily warming by 0.8 °C (W-0.8 °C) treatment was shared in the first and second group (PE-1 and PE-2). Increases in daily temperature of 0.5 °C and 0.8 °C were selected based on data from the Fifth Assessment Report of the IPCC (Stocker et al., 2013). In this report, near-term (2016–2035) and long-term (21th century) global surface air temperature changes were predicted, and the results indicated that the change in global mean surface air temperature will likely be in the range of 0.3–0.7 °C in the near-term (Kirtman et al., 2013). Therefore, this study set the warming amplitude as 0.5 °C and 0.8 °C. 2.2.1. PE-1: effects of different warming amplitude on the Cd accumulation in rice The first group (PE-1) investigated the effects of different warming amplitudes on Cd accumulation in rice. Three temperature gradients, the control treatment (CT), average daily warming by 0.5 °C (W-0.5 °C), and average daily warming by 0.8 °C (W-0.8 °C), were used in PE-1. Pots were kept submerged and warming treatments were full-day (24 h) warmed during the entire rice growth period (transplanting to harvesting). The transpiration rate of flag leaf (leaf-1) was measured at the beginning of the heading stage using a portable Yaxin-1102 photosynthetic system (Yaxin-1102, Beijing Yaxin Science Instrument Technology Co., Ltd, China). One stem with two leaves (leaf-1 (upper) and leaf-2 (lower)) of a rice plant was sampled from each pot at the end of the heading stage. The stem was then cut into two parts from the second node as stem-1 (upper) and stem-2 (lower). Rice plants (grains, shoots, and roots) were collected from each treatment at harvest, then divided into three sections according to depth: Root-1 (0–5 cm), Root-2 (5–10 cm), and Root-3 (> 10 cm).
2. Materials and methods 2.1. Materials Rice (Oryza sativa L.) cultivar 6 liangyou 9368, an indica rice cultivar bred by Nanjing Shenzhou Seeds Industry Co., Ltd. at Nanjing Agricultural University, was purchased for pot experiments. The soil was collected by sampling topsoil (0–20 cm) from a contaminated paddy field situated in Guixi, Jiangxi Province, China. The soil pH and organic matter content were 5.05% and 3.08%, respectively, while the total Cd, copper (Cu), and zinc (Zn) concentrations in soil were 0.40, 99, and 110 mg kg−1, respectively. Air-dried soil was passed through a 2 mm pore-sized sieve and weighed. The PVP (polyvinyl pyrrolidone) pots were 10 cm in diameter and 25 cm tall. Each pot was filled with 2.5 kg air-dried soil. After being raised for 25 days, two rice seedlings with a uniform size (about 15 cm long) were selected and transplanted into each pot. Each pot received 0.175 g KH2PO4, 0.095 g KCl, and 0.43 g urea as basal fertilizer before planting. Remaining urea was top-dressed in two splits at tillering
2.2.2. PE-2: effects of daytime and nighttime warming on Cd accumulation in rice The second group (PE-2) was conducted to investigate the effects of daytime and nighttime warming on Cd accumulation in rice. PE-2 included the following treatments: control treatment (CT), average nighttime warming by 1.1 °C (NW), average daytime warming by 0.5 °C (DW), and average daily warming by 0.8 °C (W-0.8 °C). Durations of daytime and nighttime warming were 12 h each (7 a.m. and 7 p.m.), respectively. Pots were kept submerged during the entire rice growth period (transplanting to harvest). Rice plants (grains, shoots, and roots) were collected from each treatment for analysis at harvest. 2.2.3. PE-3: effects of different growth stages warming on Cd accumulation in rice The effects of warming at different growth stages on Cd 81
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Fig. 1. Daily average temperature and temperature increases under different warming treatments (A), daytime and nighttime warming treatments (B), and different growth stage warming treatments (C).
accumulation in rice were examined through the third experimental group (PE-3). The entire rice growth period was divided into four individual warming stages, seedling to tillering (WS1, Jun. 10–Jul. 1), jointing to booting (WS2, Jul. 2–Jul. 25), heading (WS3, Jul. 26–Aug. 24), and grain filling to milk ripening (WS4, Aug. 25–Sep. 26). Additionally, warming from seedling to heading (WS1–3, Jun.10–Aug. 24), warming for the entire rice growth period (W-0.5 °C, Jun. 10–Sep.
26), and control treatments (CT) were also set in PE-3. The lowest quantity leaves of rice plants from each treatment were collected after the individual growth stage warming, after which individual stage warming rice plants were allowed to grow under normal conditions (without warming) until harvesting. Pots were kept submerged during the entire rice growth period. Rice plants (grains, shoots, and roots) were collected from each treatment for analysis. 82
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2.3. Samples preparation and analysis
by reducing biomass production and plant height growth, and these decreases were significant for grain yield and root biomass under W0.8 °C. Warming treatments significantly increased the Cd concentration in different tissues, especially for rice grain, by 1.45 and 2.31 times under W-0.5 °C and W-0.8 °C, respectively (Fig. 2A). At the end of the heading stage, the Cd concentrations in different stems (stem-1 and stem-2) and leaves (leaf-1 and leaf-2) were remarkably increased by warming (Fig. 2B). At harvest, warming significantly increased the root mass distribution at depths of < 10 cm, but decreased it at > 10 cm (Fig. 3A). Moreover, warming treatments increased Cd concentrations at different root depths, with significant increases being observed at 0–5 cm (Fig. 3B). Additionally, the results showed that the translocation of Cd from roots to shoots and from shoots to grains both increased in response to warming (Fig. 4A). Specifically, warming treatments increased the Cd translocation from the lower to the upper stems, but decreased Cd transfer to leaves, especially for W-0.8 °C (Fig. 4B).
The soil pH was measured at a soil to DIW (without CO2) ratio of 1:2.5 using a pH-meter (Orin Star As11, Thermo Scientific, USA). Soil organic matter content was determined using a C/N analyzer (Vario MAX CN Elementar, Germany). The total metals in soils were digested in a HNO3-HF-HClO4 (10:10:1, V/V) mixture using a microwave digestion system (ETHOS-ONE, Milestone, Italy). The rice plants were cut and divided into different parts (roots, shoots, and grains) after measuring the plant height, then washed thoroughly with DIW thrice. The washed plant materials were ovendried at 70 °C for 72 h to a constant weight, then weighed separately to measure the biomass of different plant parts. The dried samples were subsequently ground to a powder to pass through a 1 mm sieve using a ball mill (MM400, Germany). Next, plant samples were digested with HNO3-H2O2 (9:1, v/v) mixture in a microwave digestion system for Cd analysis. The Cd concentrations in the extraction and digestion solutions were analyzed using an AAS (Hitachi Z-2000, Japan) or ICP-MS (Agilent-7700×, USA). Blank and standard reference materials (GBW10015 (spinach leaves), GBW-10010 (rice grains), and GBW-07401 (soil) from the China National Center for Standard Material) were used for quality control in the digestion and analysis processes.
3.3. Growth and Cd accumulation under half/full-day warming in PE-2 Similar to PE-1, both half and full-day warming patterns reduced biomass production (especially on grain production) and plant height, especially for full-day warming W-0.8 °C (Table 1). As shown in Table 2, half-day warming had no significant effect on Cd concentrations in shoots and roots, while full-day warming led to significant increases. Both nighttime and daytime warming increased Cd concentrations in rice grain by 37.3–28.7%; however, these increases were much lower than in the full-day warming treatment (230%). Furthermore, Cd accumulation in rice grain was increased (W-0.8 °C > DW > NW > CT) relative to the control under different warming patterns. Evaluation of Cd accumulation in shoots and roots revealed that it was reduced under half-day warming, but increased under full-day warming. Moreover, both nighttime and daytime warming significantly enhanced the Cd translocation factor and percentage from shoots to grains (Fig. 5B). The situation for Cd translocation from roots to shoots was different in that it was not significantly influenced by nighttime warming, but significantly increased in response to daytime warming relative to the control treatment (Fig. 5A).
2.4. Data acquisition and statistical analysis The daily temperature was the average of the 48 recorded values during each day (each 30 min record). Average daily temperature was the mean of the daily temperature during the entire growth period. The temperature summation was the sum values of daily temperature based on the data acquired from each treatment. The Cd concentrations in plant and soil samples were calculated on a dry weight basis. The Cd accumulation in different rice tissues was calculated by multiplying Cd concentration and dry biomass of different rice tissues. The translocation factor (TF) and translocation percentage (TP) were calculated by the ratio of Cd concentration and accumulation in different tissues, respectively. The individual contribution of warming at different growth stages to Cd accumulation in rice grain was calculated based on the ratio of the added Cd accumulation values in different stages and the total added Cd accumulation value in grain. All data acquired in the present study were subjected to one-way analysis of variance (ANOVA) followed by Duncan's multiple comparisons (p < 0.05) using SPSS 19.0 (IBM, USA). Figures plotting and curve fitting were conducted using Origin 8.0 and Microsoft Excel 2003.
3.4. Growth and Cd accumulation under warming in different growth stages in PE-3 Evaluation of rice plant growth showed that different warming stages (WS1, WS2, WS3, and WS4) all tended to increase the grain yield but decrease the plant height (Table 1). After warming treatment during each stage, the Cd concentration in rice leaves increased significantly relative to the control treatment; however, the increases were smaller than those observed under continuous warming (Fig. S1). Additionally, the results at harvest revealed that the individual warming at different growth stages (WS1, WS2, WS3, and WS4) did not obviously influence the Cd concentrations in rice grain relative to the control treatment. Conversely, the treatments of WS1–3 and W-0.5 °C significantly increased the Cd concentration in rice grain, although there was no significant difference between them (Table 2). Evaluation of Cd accumulation in rice grain revealed that warming in individual growth stages resulted in increases of 31.6%, 15.0%, 20.6% and 32.8% for WS1, WS2, WS3 and WS4, respectively (Table 2). Interestingly, there was no significant difference in Cd accumulation in rice plants or Cd translocation percentage from roots to shoots between warming from the seedling to heading stage (WS1–3) and warming for the entire growth period (W-0.5 °C). When compared to warming from grain filling to milk ripening (WS4), WS1–3 showed a higher Cd translocation percentage from roots to shoots (Table 2 and Fig. 5C).
3. Results 3.1. Temperature change of different treatments The air temperature was monitored every 30 min, and the average of the 48 temperature readings acquired throughout the day represented the mean air temperature on a whole day. In PE-1, the infrared heater led to an average increase in daily air temperature of approximately 0.5 °C (W-0.5 °C) and 0.8 °C (W-0.8 °C) relative to the control (CT) (Fig. 1A). In PE-2, the infrared heater increased the average daytime and nighttime temperature by 0.5 °C and 1.1 °C, respectively (Fig. 1B). For PE-3, warming in different growth stages significantly increased the temperature summation by 11.2, 10.2, 8.1, 24.7, 29.5, and 54.2 day-degrees for WS1, WS2, WS3, WS4, WS1–3, and W-0.5 °C, respectively (Fig. 1C). Overall, the amplitudes of temperature summation increases were negatively related to the average air temperature. 3.2. Growth and Cd accumulation under different warming amplitudes in PE-1
4. Discussion The temperature record data acquired in this study revealed that the
As shown in Table 1, warming had negative effects on rice growth 83
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Table 1 Biomass production of rice tissues (root, shoot, and grain), ear number, and plant height at harvest under different treatments. Experiment
Treatments
Biomass production (g pot−1) Grain
PE−1 PE−2
PE−3
CT W−0.5 °C W−0.8 °C CT NW DW W−0.8 °C CT WS1 WS2 WS3 WS1–3 WS4 W−0.5 °C
23.9 20.2 12.8 23.9 21.0 23.8 12.8 23.9 28.4 29.2 28.0 24.0 28.4 20.2
± ± ± ± ± ± ± ± ± ± ± ± ± ±
Shoot 3.8 3.1 2.1 3.8 1.7 2.3 2.1 3.8 4.0 2.1 3.9 1.8 3.0 3.1
ab b b ab a a b ab a a a ab a b
20.4 20.0 18.9 20.4 19.4 18.3 18.9 20.4 20.1 23.8 22.2 20.6 23.8 20.0
± ± ± ± ± ± ± ± ± ± ± ± ± ±
Ear number
Height (cm)
9.7 8.5 7.0 9.7 9.4 9.0 7.0 9.7 9.5 11.8 11.5 9.3 11.0 8.5
95.8 91.3 84.6 95.8 88.2 91.4 84.6 95.8 91.8 89.3 91.8 91.5 92.5 91.3
Root 2.3 1.8 2.5 2.3 1.7 0.9 2.5 2.3 2.1 1.2 2.0 0.7 2.2 1.8
b b a b a a a b b a ab b a b
3.5 2.6 2.4 3.5 2.8 2.7 2.4 3.5 2.9 3.4 3.6 2.4 3.8 2.6
± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.3 ab 0.5c 0.3 b 0.3 ab 0.2 ab 0.2 ab 0.3 b 0.3 ab 0.3 BCE 0.2 ab 0.7 ab 0.5c 0.6 a 0.5c
± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.9 ab 1.7 d 2.1 b 0.9 ab 1.8 a 0.7 a 2.1 b 0.9 ab 0.6 cd 1.5 a 0.6 ab 1.0 cd 1.4 abc 1.7 d
± ± ± ± ± ± ± ± ± ± ± ± ± ±
5.3 a 1.7 ab 2.1c 5.3 a 2.6 BCE 2.5 ab 2.1c 5.3 a 2.9 ab 3.0 b 2.9 ab 3.8 ab 1.3 ab 1.7 ab
Note: Values are the means ± SD with a sample size n = 4. Values in rows with different lowercase letters denote significant differences among treatments at p < 0.05. CT, W-0.5 °C and W-0.8 °C denote the control, warming by 0.5 °C and warming by 0.8 °C treatments, respectively. NW and DW denote only nighttime warming and daytime warming, respectively. WS1, WS2, WS3, WS1–3 and WS4 denote warming of different growth stages (S1: seedling to tillering stage, S2: jointing to booting stage, S3: heading stage, S1–3: seedling to heading stage, S4: filling to milk-ripe stage).
Fig. 2. Cd concentrations in different rice tissues (grains, shoots, and roots) at harvest (A), Cd concentration in different parts of shoots at the end of the heading stage (B) under different warming amplitude treatments. Different letters above the column indicate significant differences between different warming treatments (p < 0.05, n = 4).
infrared heaters could change the warming amplitude by increasing the average daily air temperature. The warming amplitudes presented in PE-1 (0.5 and 0.8 °C) were smaller than those of 2.0–2.6 °C reported by Wan et al. (2002), and closer to the actual situation. The asymmetric increase of air temperature during daytime and nighttime in PE-2 was
concordant with the narrowing of DTR previously reported by Easterling et al. (1997), which might be attributed to the competitive effect between visible light and infrared radiation. Additionally, the higher warming amplitude during nighttime was also associated with the high humidity, which absorbed more infrared radiation during 84
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nighttime (Wild et al., 2007). As shown in Fig. 1C, the sum increase in temperature of the WS4 treatment was largest among all stages. The finding that a lower air temperature was associated with a greater increase in temperature amplitude under FATI was in accordance with the results of a previous study that showed wintertime warming was more obvious than that in summertime under global warming (Zhou and Ren, 2012). The significant decline of grain yield and plant height with increasing warming amplitude observed in PE-1 was in consensus with the inhibiting effect by García et al. (2015). The obvious increases of Cd concentration and accumulation under warming in rice plants were in agreement with those observed in our previous report (Ge et al., 2016a), which might be attributed to growth of root being the major region of nutrition uptake (Ge et al., 2016b). Previous reports revealed that warming was involved in changes in the root morphological growth by increasing the fine root surface area (Björk et al., 2007), which in turn can serve as a good predicator of root capacity to capture nutrients from the environment (Hodge et al., 2000). Thus, in PE-1, the increased Cd uptake and higher Cd concentration in roots might have resulted from the increased root mass distribution and surface area (Berkelaar and Hale, 2000; Ge et al., 2016b). Evaluation of the enhanced translocation of Cd in rice plants indicated that warming enhanced the process of Cd unloading in the xylem flow, which is essential for controlling root-to-shoot Cd translocation, and is partly dependent on leaf transpiration capacity (Uraguchi et al., 2009; Liu et al., 2010). Previous studies of Indian mustard and durum wheat reported that Cd translocation and accumulation in shoots was driven by transpiration (Salt et al., 1995; Van Der Vliet et al., 2007). In the present study, leaf transpiration and total water use were significantly increased in PE-1 by warming (Fig. 4C and D) because of the increased vapor pressure deficit between leaves and the surrounding atmosphere by warming (Trenberth et al., 2005). The PE-2 experiment was conducted to further investigate the individual effects of nighttime and daytime warming on rice growth and Cd accumulation. Our results indicated that half-day warming (NW and DW) had weaker negative effects on rice growth than full-day warming, which was consistent with the results of earlier studies by Dhakhwa and
Fig. 3. Rice root mass distribution percentage (A) and Cd concentration (B) at different soil depths under different warming amplitude treatments. Different letters above the column indicate significant differences between different warming treatments (p < 0.05, n = 4).
Fig. 4. Translocation factors of Cd between different tissues (A, B), total water usage (C), and transpiration rate of rice leaves (D) under different warming amplitude treatments. Different letters above a column indicate significant differences between warming treatments (p < 0.05, n = 4). 85
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Table 2 Cd concentrations and accumulation in the shoots, roots and grains of rice in different treatments. Experiment
Treatment
Cd concentration, (mg kg−1) Shoot
PE−2
PE−3
CT NW DW W−0.8 °C CT WS1 WS2 WS3 WS1–3 WS4 W−0.5 °C
0.98 0.77 0.97 1.94 0.98 0.98 0.82 0.75 1.62 1.02 1.69
± ± ± ± ± ± ± ± ± ± ±
Cd accumulation, (ug pot−1)
Root 0.17 b 0.15 b 0.16 b 0.50 a 0.17 b 0.07 b 0.04c 0.02c 0.40 a 0.04 b 0.12 a
1.55 1.44 1.47 2.56 1.55 1.85 1.66 1.79 2.42 2.03 2.24
Grain ± ± ± ± ± ± ± ± ± ± ±
0.19 b 0.36 b 0.28 b 0.37 a 0.19c 0.06 BCE 0.22 BCE 0.32 BCE 0.28 a 0.27 ab 0.06 a
0.10 0.13 0.12 0.32 0.09 0.11 0.09 0.10 0.19 0.11 0.23
Shoot
± ± ± ± ± ± ± ± ± ± ±
0.01c 0.03 b 0.01 b 0.18 a 0.01 b 0.02 b 0.02 b 0.03 b 0.06 a 0.01 b 0.03 a
20.0 14.9 17.8 36.7 20.0 19.6 19.5 16.7 33.4 24.2 33.8
± ± ± ± ± ± ± ± ± ± ±
Root 2.3 b 1.3c 0.9 BCE 6.5 a 2.3 b 2.0 b 1.0 b 1.5c 1.2 a 2.2 ab 3.1 a
5.3 4.0 3.9 6.0 5.3 5.3 5.7 6.5 5.7 7.8 5.7
± ± ± ± ± ± ± ± ± ± ±
Grain 0.9 0.4 0.5 1.2 0.9 0.5 0.3 1.3 1.2 1.3 1.2
ab b b a b b b ab b a b
2.3 2.7 3.1 3.7 2.3 3.0 2.7 2.7 4.6 3.1 4.8
± ± ± ± ± ± ± ± ± ± ±
0.6c 0.6 BCE 0.4 b 1.3 a 0.6 b 0.8 b 0.5 b 0.7 b 2.1 a 1.1 b 0.9 a
Note: Mean values followed by different lowercase letters in each line indicate significant differences (p < 0.05, n = 4).
Campbell (1998). The observed Cd concentrations and accumulation in rice grain implied that both nighttime and daytime warming contributed to the increase of Cd accumulation in rice grain under warming conditions. This is the first study to report such findings; accordingly, additional studies are needed to elucidate the reasons for these result. One potential reason may be related to the enhanced Cd translocation from shoots to grains under both nighttime and daytime warming. Additionally, Cd root to shoot translocation mainly increased during daytime warming, while the Cd transfer from shoots to grains increased under both daytime and nighttime warming. Consequently, the warming resulted in overall increases in Cd accumulation in rice grain. The increased Cd translocation from shoots to grains in PE-1 and PE2 implied that warming might be of great importance to Cd accumulation in rice grain during different growth stages. The PE-3 experiments were conducted to further elucidate the contribution of warming treatments in individual growth stages. The results clearly demonstrated that warming during each growth stage would contribute to Cd accumulation in rice grain. Specifically, the increases in Cd accumulation in rice shoots and roots were attributed to warming from the seedling to the heading stage, during which time Cd translocation from roots to shoots was enhanced significantly. Previous studies reported
that 60% of the total Cd in rice grain was remobilized from that accumulated in rice plants during the pre-anthesis growth period, while the remaining 40% came from uptake during the post-anthesis growth period (Rodda et al., 2011). Therefore, pre-anthesis warming (WS1–3) increased Cd accumulation in rice shoots by increasing the Cd translocation from roots to shoots, while post-anthesis warming (WS4) increased Cd accumulation in rice shoots by increasing the Cd uptake in roots (Table 2 and Fig. 5C). Later, the increased Cd that accumulated in shoots during crop growth was translocated to rice grain, resulting in higher Cd accumulation in grain (Arao and Ishikawa, 2006). In contrast, WS1–3 treatment increased the Cd translocation from shoots to grain during maturation, yet no such trend was observed in the case of WS4 (Fig. 5D). Taken together, these results indicated that warming increased Cd accumulation in rice grain mainly by improving Cd translocation to shoots during the pre-anthesis growth period as well as by increasing Cd uptake through roots during maturation, which synergistically promoted the Cd remobilization into rice grain. 5. Conclusion This study confirmed our previous findings that simulated warming Fig. 5. Cd translocation factors (TF) and translocation percentages (TP) in different tissues under different day-night warming patterns (A, B) and growth stage warming treatments (C, D). Different letters (capital letter: TF; lowercase letter: TP) above a column indicate significant differences between different warming treatments (p < 0.05, n = 4).
86
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could significantly increase the Cd concentration in rice grain, as indicated by changes of 0.10 mg kg−1 to 0.23 mg kg−1 and 0.32 mg kg−1 after average warming of 0.5 °C and 0.8 °C, respectively. Further investigation of the potential controlling factors revealed that warming during nighttime and daytime both boosted Cd accumulation in rice grain, while daytime warming generally controlled the Cd translocation from roots to shoots during this process. Moreover, warming in individual growth stages (from seedling to milk-ripening) contributed to the increase of Cd accumulation in grain to different extents. Specifically, warming from the seedling to the heading stage greatly enhanced the Cd translocation from roots to shoots and warming during maturation further increased the Cd uptake by roots, which synergistically promoted the Cd remobilization into the rice grain. The above findings can be used to provide early warnings for food security production with global warming and help explain the effects of diurnal asymmetry of warming on rice growth and nutrient uptake. In the long term, the projected results will provide an in-depth understanding of the Cd fates in the soil-rice system and provide guidance for rice production in Cd contaminated areas under global warming.
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Acknowledgments The present study was financially supported by the National Natural Science Foundation of China (41471261, 21177135). Ethics & conflict of interest All experiments comply with the current laws of China. This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study. The authors declare that they have no conflicts of interest. Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at doi:10.1016/j.ecoenv.2018.10.047. References Arao, T., Ishikawa, S., 2006. Genotypic differences in cadmium concentration and distribution of soybean and rice. Jpn. Agr. Res. Q. 40, 21–30. Asseng, S., Ewert, F., Martre, P., Rotter, R.P., Lobell, D.B., Cammarano, D., Kimball, B.A., Ottman, M.J., Wall, G.W., White, J.W., 2015. Rising temperatures reduce global wheat production. Nat. Clim. Chang. 5, 143–147. Berkelaar, E., Hale, B., 2000. The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can. J. Bot. 78, 381–387. Björk, R.G., Majdi, H., Klemedtsson, L., Lewis‐Jonsson, L., Molau, U., 2007. Long‐term warming effects on root morphology, root mass distribution, and microbial activity in two dry tundra plant communities in northern Sweden. New Phytol. 176, 862–873. Cornu, J.Y., Denaix, L., Lacoste, J., Sappin-Didier, V., Nguyen, C., Schneider, A., 2016. Impact of temperature on the dynamics of organic matter and on the soil-to-plant transfer of Cd, Zn and Pb in a contaminated agricultural soil. Environ. Sci. Pollut. Res. 23, 2997–3007. Dhakhwa, G.B., Campbell, C.L., 1998. Potential effects of differential day-night warming in global climate change on crop production. Clim. Chang. 40, 647–667. Easterling, D.R., Horton, B., Jones, P.D., Peterson, T.C., Karl, T.R., Parker, D.E., Salinger, M.J., Razuvayev, V., Plummer, N., Jamason, P., 1997. Maximum and minimum temperature trends for the globe. Science 277, 364–367. Fritioff, A., Kautsky, L., Greger, M., 2005. Influence of temperature and salinity on heavy metal uptake by submersed plants. Environ. Pollut. 133, 265–274. Fu, Q.L., Weng, N.Y., Fujii, M., Zhou, D.M., 2018. Temporal variability in Cu speciation, phytotoxicity, and soil microbial activity of Cu-polluted soils as affected by elevated temperature. Chemosphere 194, 285–296. García, G.A., Dreccer, M.F., Miralles, D.J., Serrago, R.A., 2015. High night temperatures during grain number determination reduce wheat and barley grain yield: a field study. Glob. Chang. Biol. 21, 4153–4164. Ge, L.Q., Cang, L., Liu, H., Zhou, D.M., 2016a. Effects of warming on uptake and translocation of cadmium (Cd) and copper (Cu) in a contaminated soil-rice system under Free Air Temperature Increase (FATI). Chemosphere 155, 1–8. Ge, L.Q., Cang, L., Yang, J., Zhou, D.M., 2016b. Effects of root morphology and leaf
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Effects of various warming patterns on Cd transfer in soil-rice systems under Free Air Temperature Increase (FATI) conditions
T
Liqiang Gea,b, Long Canga, , Syed Tahir Ata-Ul-Karima, Jie Yanga,c, Dongmei Zhoua, ⁎
⁎
a
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China Geological Survey of Jiangsu Province, Nanjing 210018, China c University of Chinese Academy of Sciences, Beijing 100049, China b
ARTICLE INFO
ABSTRACT
Keywords: Cadmium Soil Rice Warming patterns Free Air Temperature Increase (FATI)
Global warming has become an important research topic in different disciplines around the world, especially in the fields of environment quality and food security. As a potential problem in soil environments, cadmium (Cd) contamination of rice under global warming conditions has not been thoroughly investigated. In this study, the fate of Cd in soil-rice systems under various warming patterns was studied via pot experiments under Free Air Temperature Increase (FATI) conditions. The patterns of warming included different temperatures (0.5 °C and 0.8 °C), different day-night durations (nighttime, daytime, and the whole day), and different warming stages (WSx) (including WS1 (seedling to tillering), WS2 (jointing to booting), WS3 (heading), WS4 (grain filling to milk ripening)). At harvest, samples of different rice tissues were collected and the Cd concentrations were measured. The results showed that warming significantly increased Cd concentrations in grain by 1.45 and 2.31 times, which was positively correlated with the two temperature increases (0.5 °C and 0.8 °C), respectively. Both daytime and nighttime warming significantly increased the Cd concentration in grain, and the daytime dominated Cd translocation from roots to shoots. In addition, warming in individual growth stages contributed to increases in Cd accumulation in grain by 31.6% (WS1), 15.0% (WS2), 20.6% (WS3), and 32.8% (WS4), respectively. Specifically, warming during the vegetative phase boosted Cd translocation from roots to shoots, while warming during maturation further increased Cd uptake and remobilization into grain. The projected results could provide a new and in-depth understanding of the fate of Cd in soil-rice systems under global warming conditions in Cd contaminated areas.
1. Introduction In recent years, global warming has been widely accepted and thoroughly investigated (Hartmann et al., 2013) because it is endangering human health via direct mortality and morbidity (extreme heat, cold, drought, or storms) by changing air and water quality as well as food security (Patz et al., 2005; Porter, 2005). The majority of previous studies have focused on the effects of global warming on atmospheric and aquatic environmental quality, as well as crop yield security; however, little attention has been paid to soil environmental quality and crop quality security (Tagaris et al., 2009; Wheeler and Von Braun, 2013; Asseng et al., 2015). The worldwide increase of heavy metal pollution in agriculture soils and the problem of higher cadmium (Cd) concentrations in rice grain have received increasing attention from soil chemists, crop scientists, governments and the public because of the widespread occurrence and chronic human exposure to Cd via
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dietary intake in recent years (Meharg et al., 2013; Larson, 2014; Zhao et al., 2015). However, few studies have mentioned the potential influences of warming on Cd accumulation in rice. Therefore, it is essential to understand the Cd uptake and translocation in soil-rice systems under the future scenarios of global warming, for guiding food production. Studies of the plant-metal-soil interaction under climate change have drawn increased attention from researchers and revealed that soil warming could increase heavy metal bioavailability in soil and accumulation in plants (Rajkumar et al., 2013; Cornu et al., 2016; Fu et al., 2018). Additionally, previous studies reported that warming increased the heavy metal accumulation in different plants, including shrubs, herbaceous plants, and submerged plant (Moreno et al., 2002; Fritioff et al., 2005; Li et al., 2012; Sardans et al., 2008). Earlier investigations of wheat revealed that elevated atmospheric temperature could stimulate the Cd uptake by wheat seedlings by changing rhizosphere soil
Corresponding authors. E-mail addresses: [email protected] (L. Ge), [email protected] (L. Cang), [email protected] (D. Zhou).
https://doi.org/10.1016/j.ecoenv.2018.10.047 Received 8 June 2018; Received in revised form 3 October 2018; Accepted 11 October 2018 0147-6513/ © 2018 Elsevier Inc. All rights reserved.
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properties (Jia et al., 2015). Our previous study under Free Air Temperature Increase (FATI) conditions (with just a single season pot experiment without a warming gradient) revealed that simulated atmospheric warming greatly increased Cd accumulation in rice grain (Ge et al., 2016a). To further investigate and confirm the previous results, a novel pot experiment with two warming amplitudes (0.5 °C and 0.8 °C) was conducted under FATI conditions, in this study. Neither global nor regional warming presents with an asymmetrical or incessant style. Both the maximum and minimum daily temperature increase asymmetrically, which induces changes in the diurnal temperature range (DTR) (Hartmann et al., 2013). The different changed amplitudes of day and night temperature would greatly influence the plant growth, especially for crops. For example, Dhakhwa and Campbell (1998) reported that the effects of asymmetric day-night warming on crop production might be less severe than equal day-night warming. Moreover, Peng et al. (2004) found that rice grain yield decreased significantly under higher night temperature. However, few studies have focused on the effects of asymmetric warming on Cd transfer in soil-rice systems. Therefore, in this study, a pot experiment with half day warming treatment was conducted to evaluate the individual contributions of nighttime or daytime warming to Cd accumulation in rice grain. Zhou and Ren (2012) concluded that the reduction of cool days and nights mainly occurred in winter, while warm days and nights primarily increased in autumn and summer. Therefore, global warming generally leads to increases in globally averaged multi-day heat events, rather than equal increases in daily air temperature. Accordingly, warming climates may result in mismatches between key sensitive growth stages and extreme warming climate events. Specifically, under future warming an entire soil-rice system might be exposed to higher temperatures during short growth periods. Laza et al. (2015) reported that the response of rice to warming varied with the period of treatment and that nighttime warming during the reproduction periods led to a direct reduction in rice yield. However, in their investigation, the effects of warming during different reproduction periods on Cd accumulation in rice were ignored. Therefore, the present study utilized a pot experiment with warming at different growth stages to identify the most critical growth stages influencing Cd accumulation in rice grain under warming. By conducting three groups of warming pot experiments (different warming amplitudes, day and night warming, and growth stage warming), this study provided new and in-depth understanding of the mechanisms of Cd uptake and translocation in the soil-rice system. The results presented herein will facilitate development of effective guidance for rice production in Cd contaminated areas under future warming.
(0.535 g) and heading stages (0.43 g), respectively. Each pot was irrigated with deionized water (DIW) and the thickness of the water layer was kept at 5 cm throughout the crop period to fulfill crop water requirements. The weeds in pots were pulled out manually using tweezers as early as possible during experiments. All pot experiments with four replications were conducted in a greenhouse located in Nanjing, Jiangsu Province. Infrared heaters (89 × 15 cm; Kalglo Electronics Inc, USA) were hung about 1.2 m above the soil surface for warming, while dummy heaters were used to simulate shading effects for controls (Luo et al., 2001). The thermocouples were connected to a datalogger (WTHOT1G, China) to monitor the air temperature (30 cm above soil surface) at intervals every half hour. 2.2. Pot experiments In the present study, pot experiments (PE) were divided in three groups, which shared several treatments together as shown in Table S1. Specifically, the control treatment (CT, without warming, under natural temperature) was shared in all pot experiments. Average daily warming by 0.5 °C (W-0.5 °C) treatment was shared in the first and third group (PE-1 and PE-3), and average daily warming by 0.8 °C (W-0.8 °C) treatment was shared in the first and second group (PE-1 and PE-2). Increases in daily temperature of 0.5 °C and 0.8 °C were selected based on data from the Fifth Assessment Report of the IPCC (Stocker et al., 2013). In this report, near-term (2016–2035) and long-term (21th century) global surface air temperature changes were predicted, and the results indicated that the change in global mean surface air temperature will likely be in the range of 0.3–0.7 °C in the near-term (Kirtman et al., 2013). Therefore, this study set the warming amplitude as 0.5 °C and 0.8 °C. 2.2.1. PE-1: effects of different warming amplitude on the Cd accumulation in rice The first group (PE-1) investigated the effects of different warming amplitudes on Cd accumulation in rice. Three temperature gradients, the control treatment (CT), average daily warming by 0.5 °C (W-0.5 °C), and average daily warming by 0.8 °C (W-0.8 °C), were used in PE-1. Pots were kept submerged and warming treatments were full-day (24 h) warmed during the entire rice growth period (transplanting to harvesting). The transpiration rate of flag leaf (leaf-1) was measured at the beginning of the heading stage using a portable Yaxin-1102 photosynthetic system (Yaxin-1102, Beijing Yaxin Science Instrument Technology Co., Ltd, China). One stem with two leaves (leaf-1 (upper) and leaf-2 (lower)) of a rice plant was sampled from each pot at the end of the heading stage. The stem was then cut into two parts from the second node as stem-1 (upper) and stem-2 (lower). Rice plants (grains, shoots, and roots) were collected from each treatment at harvest, then divided into three sections according to depth: Root-1 (0–5 cm), Root-2 (5–10 cm), and Root-3 (> 10 cm).
2. Materials and methods 2.1. Materials Rice (Oryza sativa L.) cultivar 6 liangyou 9368, an indica rice cultivar bred by Nanjing Shenzhou Seeds Industry Co., Ltd. at Nanjing Agricultural University, was purchased for pot experiments. The soil was collected by sampling topsoil (0–20 cm) from a contaminated paddy field situated in Guixi, Jiangxi Province, China. The soil pH and organic matter content were 5.05% and 3.08%, respectively, while the total Cd, copper (Cu), and zinc (Zn) concentrations in soil were 0.40, 99, and 110 mg kg−1, respectively. Air-dried soil was passed through a 2 mm pore-sized sieve and weighed. The PVP (polyvinyl pyrrolidone) pots were 10 cm in diameter and 25 cm tall. Each pot was filled with 2.5 kg air-dried soil. After being raised for 25 days, two rice seedlings with a uniform size (about 15 cm long) were selected and transplanted into each pot. Each pot received 0.175 g KH2PO4, 0.095 g KCl, and 0.43 g urea as basal fertilizer before planting. Remaining urea was top-dressed in two splits at tillering
2.2.2. PE-2: effects of daytime and nighttime warming on Cd accumulation in rice The second group (PE-2) was conducted to investigate the effects of daytime and nighttime warming on Cd accumulation in rice. PE-2 included the following treatments: control treatment (CT), average nighttime warming by 1.1 °C (NW), average daytime warming by 0.5 °C (DW), and average daily warming by 0.8 °C (W-0.8 °C). Durations of daytime and nighttime warming were 12 h each (7 a.m. and 7 p.m.), respectively. Pots were kept submerged during the entire rice growth period (transplanting to harvest). Rice plants (grains, shoots, and roots) were collected from each treatment for analysis at harvest. 2.2.3. PE-3: effects of different growth stages warming on Cd accumulation in rice The effects of warming at different growth stages on Cd 81
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Fig. 1. Daily average temperature and temperature increases under different warming treatments (A), daytime and nighttime warming treatments (B), and different growth stage warming treatments (C).
accumulation in rice were examined through the third experimental group (PE-3). The entire rice growth period was divided into four individual warming stages, seedling to tillering (WS1, Jun. 10–Jul. 1), jointing to booting (WS2, Jul. 2–Jul. 25), heading (WS3, Jul. 26–Aug. 24), and grain filling to milk ripening (WS4, Aug. 25–Sep. 26). Additionally, warming from seedling to heading (WS1–3, Jun.10–Aug. 24), warming for the entire rice growth period (W-0.5 °C, Jun. 10–Sep.
26), and control treatments (CT) were also set in PE-3. The lowest quantity leaves of rice plants from each treatment were collected after the individual growth stage warming, after which individual stage warming rice plants were allowed to grow under normal conditions (without warming) until harvesting. Pots were kept submerged during the entire rice growth period. Rice plants (grains, shoots, and roots) were collected from each treatment for analysis. 82
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2.3. Samples preparation and analysis
by reducing biomass production and plant height growth, and these decreases were significant for grain yield and root biomass under W0.8 °C. Warming treatments significantly increased the Cd concentration in different tissues, especially for rice grain, by 1.45 and 2.31 times under W-0.5 °C and W-0.8 °C, respectively (Fig. 2A). At the end of the heading stage, the Cd concentrations in different stems (stem-1 and stem-2) and leaves (leaf-1 and leaf-2) were remarkably increased by warming (Fig. 2B). At harvest, warming significantly increased the root mass distribution at depths of < 10 cm, but decreased it at > 10 cm (Fig. 3A). Moreover, warming treatments increased Cd concentrations at different root depths, with significant increases being observed at 0–5 cm (Fig. 3B). Additionally, the results showed that the translocation of Cd from roots to shoots and from shoots to grains both increased in response to warming (Fig. 4A). Specifically, warming treatments increased the Cd translocation from the lower to the upper stems, but decreased Cd transfer to leaves, especially for W-0.8 °C (Fig. 4B).
The soil pH was measured at a soil to DIW (without CO2) ratio of 1:2.5 using a pH-meter (Orin Star As11, Thermo Scientific, USA). Soil organic matter content was determined using a C/N analyzer (Vario MAX CN Elementar, Germany). The total metals in soils were digested in a HNO3-HF-HClO4 (10:10:1, V/V) mixture using a microwave digestion system (ETHOS-ONE, Milestone, Italy). The rice plants were cut and divided into different parts (roots, shoots, and grains) after measuring the plant height, then washed thoroughly with DIW thrice. The washed plant materials were ovendried at 70 °C for 72 h to a constant weight, then weighed separately to measure the biomass of different plant parts. The dried samples were subsequently ground to a powder to pass through a 1 mm sieve using a ball mill (MM400, Germany). Next, plant samples were digested with HNO3-H2O2 (9:1, v/v) mixture in a microwave digestion system for Cd analysis. The Cd concentrations in the extraction and digestion solutions were analyzed using an AAS (Hitachi Z-2000, Japan) or ICP-MS (Agilent-7700×, USA). Blank and standard reference materials (GBW10015 (spinach leaves), GBW-10010 (rice grains), and GBW-07401 (soil) from the China National Center for Standard Material) were used for quality control in the digestion and analysis processes.
3.3. Growth and Cd accumulation under half/full-day warming in PE-2 Similar to PE-1, both half and full-day warming patterns reduced biomass production (especially on grain production) and plant height, especially for full-day warming W-0.8 °C (Table 1). As shown in Table 2, half-day warming had no significant effect on Cd concentrations in shoots and roots, while full-day warming led to significant increases. Both nighttime and daytime warming increased Cd concentrations in rice grain by 37.3–28.7%; however, these increases were much lower than in the full-day warming treatment (230%). Furthermore, Cd accumulation in rice grain was increased (W-0.8 °C > DW > NW > CT) relative to the control under different warming patterns. Evaluation of Cd accumulation in shoots and roots revealed that it was reduced under half-day warming, but increased under full-day warming. Moreover, both nighttime and daytime warming significantly enhanced the Cd translocation factor and percentage from shoots to grains (Fig. 5B). The situation for Cd translocation from roots to shoots was different in that it was not significantly influenced by nighttime warming, but significantly increased in response to daytime warming relative to the control treatment (Fig. 5A).
2.4. Data acquisition and statistical analysis The daily temperature was the average of the 48 recorded values during each day (each 30 min record). Average daily temperature was the mean of the daily temperature during the entire growth period. The temperature summation was the sum values of daily temperature based on the data acquired from each treatment. The Cd concentrations in plant and soil samples were calculated on a dry weight basis. The Cd accumulation in different rice tissues was calculated by multiplying Cd concentration and dry biomass of different rice tissues. The translocation factor (TF) and translocation percentage (TP) were calculated by the ratio of Cd concentration and accumulation in different tissues, respectively. The individual contribution of warming at different growth stages to Cd accumulation in rice grain was calculated based on the ratio of the added Cd accumulation values in different stages and the total added Cd accumulation value in grain. All data acquired in the present study were subjected to one-way analysis of variance (ANOVA) followed by Duncan's multiple comparisons (p < 0.05) using SPSS 19.0 (IBM, USA). Figures plotting and curve fitting were conducted using Origin 8.0 and Microsoft Excel 2003.
3.4. Growth and Cd accumulation under warming in different growth stages in PE-3 Evaluation of rice plant growth showed that different warming stages (WS1, WS2, WS3, and WS4) all tended to increase the grain yield but decrease the plant height (Table 1). After warming treatment during each stage, the Cd concentration in rice leaves increased significantly relative to the control treatment; however, the increases were smaller than those observed under continuous warming (Fig. S1). Additionally, the results at harvest revealed that the individual warming at different growth stages (WS1, WS2, WS3, and WS4) did not obviously influence the Cd concentrations in rice grain relative to the control treatment. Conversely, the treatments of WS1–3 and W-0.5 °C significantly increased the Cd concentration in rice grain, although there was no significant difference between them (Table 2). Evaluation of Cd accumulation in rice grain revealed that warming in individual growth stages resulted in increases of 31.6%, 15.0%, 20.6% and 32.8% for WS1, WS2, WS3 and WS4, respectively (Table 2). Interestingly, there was no significant difference in Cd accumulation in rice plants or Cd translocation percentage from roots to shoots between warming from the seedling to heading stage (WS1–3) and warming for the entire growth period (W-0.5 °C). When compared to warming from grain filling to milk ripening (WS4), WS1–3 showed a higher Cd translocation percentage from roots to shoots (Table 2 and Fig. 5C).
3. Results 3.1. Temperature change of different treatments The air temperature was monitored every 30 min, and the average of the 48 temperature readings acquired throughout the day represented the mean air temperature on a whole day. In PE-1, the infrared heater led to an average increase in daily air temperature of approximately 0.5 °C (W-0.5 °C) and 0.8 °C (W-0.8 °C) relative to the control (CT) (Fig. 1A). In PE-2, the infrared heater increased the average daytime and nighttime temperature by 0.5 °C and 1.1 °C, respectively (Fig. 1B). For PE-3, warming in different growth stages significantly increased the temperature summation by 11.2, 10.2, 8.1, 24.7, 29.5, and 54.2 day-degrees for WS1, WS2, WS3, WS4, WS1–3, and W-0.5 °C, respectively (Fig. 1C). Overall, the amplitudes of temperature summation increases were negatively related to the average air temperature. 3.2. Growth and Cd accumulation under different warming amplitudes in PE-1
4. Discussion The temperature record data acquired in this study revealed that the
As shown in Table 1, warming had negative effects on rice growth 83
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Table 1 Biomass production of rice tissues (root, shoot, and grain), ear number, and plant height at harvest under different treatments. Experiment
Treatments
Biomass production (g pot−1) Grain
PE−1 PE−2
PE−3
CT W−0.5 °C W−0.8 °C CT NW DW W−0.8 °C CT WS1 WS2 WS3 WS1–3 WS4 W−0.5 °C
23.9 20.2 12.8 23.9 21.0 23.8 12.8 23.9 28.4 29.2 28.0 24.0 28.4 20.2
± ± ± ± ± ± ± ± ± ± ± ± ± ±
Shoot 3.8 3.1 2.1 3.8 1.7 2.3 2.1 3.8 4.0 2.1 3.9 1.8 3.0 3.1
ab b b ab a a b ab a a a ab a b
20.4 20.0 18.9 20.4 19.4 18.3 18.9 20.4 20.1 23.8 22.2 20.6 23.8 20.0
± ± ± ± ± ± ± ± ± ± ± ± ± ±
Ear number
Height (cm)
9.7 8.5 7.0 9.7 9.4 9.0 7.0 9.7 9.5 11.8 11.5 9.3 11.0 8.5
95.8 91.3 84.6 95.8 88.2 91.4 84.6 95.8 91.8 89.3 91.8 91.5 92.5 91.3
Root 2.3 1.8 2.5 2.3 1.7 0.9 2.5 2.3 2.1 1.2 2.0 0.7 2.2 1.8
b b a b a a a b b a ab b a b
3.5 2.6 2.4 3.5 2.8 2.7 2.4 3.5 2.9 3.4 3.6 2.4 3.8 2.6
± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.3 ab 0.5c 0.3 b 0.3 ab 0.2 ab 0.2 ab 0.3 b 0.3 ab 0.3 BCE 0.2 ab 0.7 ab 0.5c 0.6 a 0.5c
± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.9 ab 1.7 d 2.1 b 0.9 ab 1.8 a 0.7 a 2.1 b 0.9 ab 0.6 cd 1.5 a 0.6 ab 1.0 cd 1.4 abc 1.7 d
± ± ± ± ± ± ± ± ± ± ± ± ± ±
5.3 a 1.7 ab 2.1c 5.3 a 2.6 BCE 2.5 ab 2.1c 5.3 a 2.9 ab 3.0 b 2.9 ab 3.8 ab 1.3 ab 1.7 ab
Note: Values are the means ± SD with a sample size n = 4. Values in rows with different lowercase letters denote significant differences among treatments at p < 0.05. CT, W-0.5 °C and W-0.8 °C denote the control, warming by 0.5 °C and warming by 0.8 °C treatments, respectively. NW and DW denote only nighttime warming and daytime warming, respectively. WS1, WS2, WS3, WS1–3 and WS4 denote warming of different growth stages (S1: seedling to tillering stage, S2: jointing to booting stage, S3: heading stage, S1–3: seedling to heading stage, S4: filling to milk-ripe stage).
Fig. 2. Cd concentrations in different rice tissues (grains, shoots, and roots) at harvest (A), Cd concentration in different parts of shoots at the end of the heading stage (B) under different warming amplitude treatments. Different letters above the column indicate significant differences between different warming treatments (p < 0.05, n = 4).
infrared heaters could change the warming amplitude by increasing the average daily air temperature. The warming amplitudes presented in PE-1 (0.5 and 0.8 °C) were smaller than those of 2.0–2.6 °C reported by Wan et al. (2002), and closer to the actual situation. The asymmetric increase of air temperature during daytime and nighttime in PE-2 was
concordant with the narrowing of DTR previously reported by Easterling et al. (1997), which might be attributed to the competitive effect between visible light and infrared radiation. Additionally, the higher warming amplitude during nighttime was also associated with the high humidity, which absorbed more infrared radiation during 84
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nighttime (Wild et al., 2007). As shown in Fig. 1C, the sum increase in temperature of the WS4 treatment was largest among all stages. The finding that a lower air temperature was associated with a greater increase in temperature amplitude under FATI was in accordance with the results of a previous study that showed wintertime warming was more obvious than that in summertime under global warming (Zhou and Ren, 2012). The significant decline of grain yield and plant height with increasing warming amplitude observed in PE-1 was in consensus with the inhibiting effect by García et al. (2015). The obvious increases of Cd concentration and accumulation under warming in rice plants were in agreement with those observed in our previous report (Ge et al., 2016a), which might be attributed to growth of root being the major region of nutrition uptake (Ge et al., 2016b). Previous reports revealed that warming was involved in changes in the root morphological growth by increasing the fine root surface area (Björk et al., 2007), which in turn can serve as a good predicator of root capacity to capture nutrients from the environment (Hodge et al., 2000). Thus, in PE-1, the increased Cd uptake and higher Cd concentration in roots might have resulted from the increased root mass distribution and surface area (Berkelaar and Hale, 2000; Ge et al., 2016b). Evaluation of the enhanced translocation of Cd in rice plants indicated that warming enhanced the process of Cd unloading in the xylem flow, which is essential for controlling root-to-shoot Cd translocation, and is partly dependent on leaf transpiration capacity (Uraguchi et al., 2009; Liu et al., 2010). Previous studies of Indian mustard and durum wheat reported that Cd translocation and accumulation in shoots was driven by transpiration (Salt et al., 1995; Van Der Vliet et al., 2007). In the present study, leaf transpiration and total water use were significantly increased in PE-1 by warming (Fig. 4C and D) because of the increased vapor pressure deficit between leaves and the surrounding atmosphere by warming (Trenberth et al., 2005). The PE-2 experiment was conducted to further investigate the individual effects of nighttime and daytime warming on rice growth and Cd accumulation. Our results indicated that half-day warming (NW and DW) had weaker negative effects on rice growth than full-day warming, which was consistent with the results of earlier studies by Dhakhwa and
Fig. 3. Rice root mass distribution percentage (A) and Cd concentration (B) at different soil depths under different warming amplitude treatments. Different letters above the column indicate significant differences between different warming treatments (p < 0.05, n = 4).
Fig. 4. Translocation factors of Cd between different tissues (A, B), total water usage (C), and transpiration rate of rice leaves (D) under different warming amplitude treatments. Different letters above a column indicate significant differences between warming treatments (p < 0.05, n = 4). 85
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Table 2 Cd concentrations and accumulation in the shoots, roots and grains of rice in different treatments. Experiment
Treatment
Cd concentration, (mg kg−1) Shoot
PE−2
PE−3
CT NW DW W−0.8 °C CT WS1 WS2 WS3 WS1–3 WS4 W−0.5 °C
0.98 0.77 0.97 1.94 0.98 0.98 0.82 0.75 1.62 1.02 1.69
± ± ± ± ± ± ± ± ± ± ±
Cd accumulation, (ug pot−1)
Root 0.17 b 0.15 b 0.16 b 0.50 a 0.17 b 0.07 b 0.04c 0.02c 0.40 a 0.04 b 0.12 a
1.55 1.44 1.47 2.56 1.55 1.85 1.66 1.79 2.42 2.03 2.24
Grain ± ± ± ± ± ± ± ± ± ± ±
0.19 b 0.36 b 0.28 b 0.37 a 0.19c 0.06 BCE 0.22 BCE 0.32 BCE 0.28 a 0.27 ab 0.06 a
0.10 0.13 0.12 0.32 0.09 0.11 0.09 0.10 0.19 0.11 0.23
Shoot
± ± ± ± ± ± ± ± ± ± ±
0.01c 0.03 b 0.01 b 0.18 a 0.01 b 0.02 b 0.02 b 0.03 b 0.06 a 0.01 b 0.03 a
20.0 14.9 17.8 36.7 20.0 19.6 19.5 16.7 33.4 24.2 33.8
± ± ± ± ± ± ± ± ± ± ±
Root 2.3 b 1.3c 0.9 BCE 6.5 a 2.3 b 2.0 b 1.0 b 1.5c 1.2 a 2.2 ab 3.1 a
5.3 4.0 3.9 6.0 5.3 5.3 5.7 6.5 5.7 7.8 5.7
± ± ± ± ± ± ± ± ± ± ±
Grain 0.9 0.4 0.5 1.2 0.9 0.5 0.3 1.3 1.2 1.3 1.2
ab b b a b b b ab b a b
2.3 2.7 3.1 3.7 2.3 3.0 2.7 2.7 4.6 3.1 4.8
± ± ± ± ± ± ± ± ± ± ±
0.6c 0.6 BCE 0.4 b 1.3 a 0.6 b 0.8 b 0.5 b 0.7 b 2.1 a 1.1 b 0.9 a
Note: Mean values followed by different lowercase letters in each line indicate significant differences (p < 0.05, n = 4).
Campbell (1998). The observed Cd concentrations and accumulation in rice grain implied that both nighttime and daytime warming contributed to the increase of Cd accumulation in rice grain under warming conditions. This is the first study to report such findings; accordingly, additional studies are needed to elucidate the reasons for these result. One potential reason may be related to the enhanced Cd translocation from shoots to grains under both nighttime and daytime warming. Additionally, Cd root to shoot translocation mainly increased during daytime warming, while the Cd transfer from shoots to grains increased under both daytime and nighttime warming. Consequently, the warming resulted in overall increases in Cd accumulation in rice grain. The increased Cd translocation from shoots to grains in PE-1 and PE2 implied that warming might be of great importance to Cd accumulation in rice grain during different growth stages. The PE-3 experiments were conducted to further elucidate the contribution of warming treatments in individual growth stages. The results clearly demonstrated that warming during each growth stage would contribute to Cd accumulation in rice grain. Specifically, the increases in Cd accumulation in rice shoots and roots were attributed to warming from the seedling to the heading stage, during which time Cd translocation from roots to shoots was enhanced significantly. Previous studies reported
that 60% of the total Cd in rice grain was remobilized from that accumulated in rice plants during the pre-anthesis growth period, while the remaining 40% came from uptake during the post-anthesis growth period (Rodda et al., 2011). Therefore, pre-anthesis warming (WS1–3) increased Cd accumulation in rice shoots by increasing the Cd translocation from roots to shoots, while post-anthesis warming (WS4) increased Cd accumulation in rice shoots by increasing the Cd uptake in roots (Table 2 and Fig. 5C). Later, the increased Cd that accumulated in shoots during crop growth was translocated to rice grain, resulting in higher Cd accumulation in grain (Arao and Ishikawa, 2006). In contrast, WS1–3 treatment increased the Cd translocation from shoots to grain during maturation, yet no such trend was observed in the case of WS4 (Fig. 5D). Taken together, these results indicated that warming increased Cd accumulation in rice grain mainly by improving Cd translocation to shoots during the pre-anthesis growth period as well as by increasing Cd uptake through roots during maturation, which synergistically promoted the Cd remobilization into rice grain. 5. Conclusion This study confirmed our previous findings that simulated warming Fig. 5. Cd translocation factors (TF) and translocation percentages (TP) in different tissues under different day-night warming patterns (A, B) and growth stage warming treatments (C, D). Different letters (capital letter: TF; lowercase letter: TP) above a column indicate significant differences between different warming treatments (p < 0.05, n = 4).
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could significantly increase the Cd concentration in rice grain, as indicated by changes of 0.10 mg kg−1 to 0.23 mg kg−1 and 0.32 mg kg−1 after average warming of 0.5 °C and 0.8 °C, respectively. Further investigation of the potential controlling factors revealed that warming during nighttime and daytime both boosted Cd accumulation in rice grain, while daytime warming generally controlled the Cd translocation from roots to shoots during this process. Moreover, warming in individual growth stages (from seedling to milk-ripening) contributed to the increase of Cd accumulation in grain to different extents. Specifically, warming from the seedling to the heading stage greatly enhanced the Cd translocation from roots to shoots and warming during maturation further increased the Cd uptake by roots, which synergistically promoted the Cd remobilization into the rice grain. The above findings can be used to provide early warnings for food security production with global warming and help explain the effects of diurnal asymmetry of warming on rice growth and nutrient uptake. In the long term, the projected results will provide an in-depth understanding of the Cd fates in the soil-rice system and provide guidance for rice production in Cd contaminated areas under global warming.
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