Effects of low-temperature stress during heading stage on carbon and nitrogen allocation in paddy eco-system of northeastern China

doi:10.21203/rs.3.rs-4220217/v1

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Research Article

Effects of low-temperature stress during heading stage on carbon and nitrogen allocation in paddy eco-system of northeastern China

https://doi.org/10.21203/rs.3.rs-4220217/v1

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Background and aims

In high-latitude area, climate change has resulted in frequent chilling stress which affects rice sustainable production as well as changes carbon (C) and nitrogen (N) allocation in paddy ecosystem. However, the response characteristics of C and N allocation in paddy ecosystem to low-temperature stress during key growth stage are not fully understood.

Methods

A rice pot experiment of two varieties combined with ¹³C and ¹⁵N isotope labelling method was conducted to evaluate how low-temperature stress at heading stage affects rice yield, above- and below-ground C and N partitioning, and soil C and N changes.

Results

Low-temperature stress significantly reduced rice grain yield of JN809 (sensitive to low-temperature stress) and J88 (resistant to low-temperature stress) varieties 27.6% and 21.4%, respectively, Low-temperature stress was prone to increase C and N accumulation in stems and leaves of rice and soil. The low temperature tolerance variety (J88) reduced the effects of low temperature stress on rice yield and the allocation of C and N between soil and rice

Conclusion

Low-temperature during rice heading stage significantly hindered transportation of C assimilate and absorbed N from soil. Low temperature tolerant variety reduced the effect of low temperature chilling stress on rice yield, and C and N allocation. Present study provides a basis for rice breeding and cultivation techniques that can enhance rice resilience and adaptability to climate change, as well as optimize C and N sequestration practices in rice fields to ensure high yields and resource use efficiency.

Rice

Chilly stress

Carbon and nitrogen partition

Isotope labelling

High latitude area

Since the beginning of twenty-first century, the frequency and intensity of agricultural meteorological disasters have been on the rise due to the climate change (Palmer 2014; Ju et al. 2013; Chen et al. 2020). Meanwhile, the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC_AR5) pointed out that as global climate warming and extreme weather events become more frequent, the risk of low-temperature stress may also increase, which to a certain extent increases the instability of agricultural production (Pachauri et al. 2014). It is urgent to address the task of coping with agricultural meteorological disasters to maintain the sustainable crop production (Gomez-Zavagliaetal. 2020).

Rice (Oryza sativa L.) is the most important staple food for more than half of the population across the world. It was estimated that global demands of rice would increase from 644 million tons in 2007 to 827 million tons in 2050 (Alexandratos & Bruinsma 2012). China is the world's largest producer and consumer of rice. Along with the global warming, the rice cropping area increased rapidly in northeast China where accounted for more than 14% of China’s total production (National Bureau of Statistics of China, NBSC 2023). Even more, almost 75% of rice production in northeast China was for commodity. In recent years, extreme temperature events have occurred frequently in rice planting areas of China (Wang et al. 2019; Yuan et al. 2021), and cold damage has become the main meteorological disaster facing rice production, especially in northeast China (Tao et al. 2013). Low-temperature stress is one of the main limiting factors affecting stable rice production in high latitude areas (e.g. northeast China). Delayed-type or obstructive-type cold damage seriously affects the growth, development, and grain filling of rice (Tao et al. 2013). However, current research mainly focuses on the characteristics and mechanisms of the expected impact of rising atmospheric temperatures on C and N distribution in rice field systems (Tang et al. 2021 2022; Haas et al. 2022; Xie et al. 2023), while extreme low-temperatures also affect rice growth and lead to differences in the distribution of C and N between rice crops, soil, and atmosphere (Deng et al. 2011).

Rice has a certain minimum suitable temperature at each growth and development stage, low-temperature stress is unfavorable for dry matter accumulation. Especially during the heading stage, rice has the weakest tolerance to low-temperatures. Cold stress at this time can cause floret degradation or pollen sterility, resulting in empty grains (Zhang et al. 2017; Siddik et al. 2019), reducing grain setting rate and hundred grain weight, and seriously reducing yield (Zhu et al. 2012; Sperotto et al. 2013). At present, research on rice low-temperature damage mainly focuses on the degree of low-temperature damage, changes in rice physiological functions during low-temperatures, the impact on yield components and quality (Bhattacharjees 2013; Ren et al. 2017). However, there are few reports on rice low-temperature damage in relation with the distribution of C and N, soil C and N changes. Since paddy eco-system has a strong C sink function and outstanding C sequestration potential (Liu et al. 2023), understanding the response characteristics of C and N in paddy ecosystem to low-temperature stress during key growth stage is of great significance for coping with climate change.

Hereby, we hypothesized that, (i) the biomass and yield of rice were affected by low-temperature during rice heading stage (ii) low-temperature significantly hindered transportation of C assimilate and absorbed N from soil resulting in the re-distribution of C and N in paddy eco-system. To test these hypotheses, an artificial climate chamber combined with pot experiment and ¹³C and ¹⁵N isotope labeling methods were used to simulate extreme low-temperature condition in pad eco-system. The objectives of present study are to evaluate the effects of low-temperature stress during the heading stage on C and N distribution in aboveground and underground parts of rice crops, and changes in soil C and N in soils. It is anticipated to provide a basis for rice breeding and cultivation techniques that can enhance rice resilience and adaptability to climate change, as well as optimize C and N sequestration practices in paddy eco-system to ensure high yields and resilience to climate disaster risks.

Experimental design

The experiment was conducted in Gongzhuling City, Jilin Province of China (124°48´E, 43°32´N) in 2019. Two-factor experiment with randomized block design were used to evaluate how air temperature stress and different rice varieties affect C and N allocation in above-ground and under-ground parts of rice, the changes in C and N in rhizosphere soil and bulk soil. The temperature treatments included in control treatment (CK, no low-temperature stress) and low-temperature stress treatment at heading stage (LT). The rice varieties included Jijing 88 (J88, super japonica rice resistant to low-temperature stress) and Jinongda 809 (JN809, sensitive to low-temperature stress). The experiment adopted pot planting method. There were sixteen pots for each treatment and total of 64 pots for the experiment. Four pots, for each treatment and sampling date, were used for parameters measurement on 5 August, (heading stage), 27 August (filling stage), and 23 September, 2019 (harvesting stage). The pot was 25 cm height with the diameter of 20 cm. A nylon bag with a height of 10 cm and a diameter of 8 cm was buried in the basin as the root bag. The mesh size of the nylon bag is 37 µm, which ensures that the rice root do not extend out of the root bag, but can ensure the exchange of nutrients between the root bag and soil in the pot. The total amount of soil in the basin and the root bag was 5.5 kg. The potting soil was a paddy soil developed from long-term conventional paddy fields and formed by red clay in quaternary soil. The soil characterized as soil organic carbon of 21.3 g kg^− 1, total nitrogen of 2.0 g kg^− 1, alkali-hydrolyzed nitrogen of 176.1 mg kg^− 1, available phosphorus of 19.4 mg kg^− 1, available potassium of 64.1 mg kg^− 1, and pH of 5.6. Two uniformly growing rice seedlings are transplanted in each root bag at the seedling stage, maintaining a 3–4 cm water layer, and fertilized and managed according to conventional local practices. The Rice was grown under natural conditions except for heading stage when low-temperature stress was conducted.

¹³ C and ¹⁵N labelling

In order to differentiate the allocation of C and N assimilation in rice system, ¹³C and ¹⁴N isotope labelling method was used in the present experiment. ¹³C marker is started at the booting stage. For labelling, rice was confined in a transparent labelling chamber (1 m length × 1 m width × 1 m height for each chamber, Fig. 1A) and after half an hour of confinement treatment, H₂SO₄ was dripped into ¹³C-labelled Na₂CO₃ (¹³C abundance > 98%, Shanghai Research Institute of Chemical Technology, Shanghai, China) to produce ¹³CO₂, which was aired after 4 hours of confinement and labelled continuously for 7 days (Fig. 1A). The ¹⁵N labelling was carried out simultaneously with ¹³C labelling by adding ¹⁵NH₄Cl (¹⁵N abundance 99.9%, Shanghai Research Institute of Chemical Technology, Shanghai, China) in pots. Fans and ice packs were placed inside for physical cooling during the marking period to prevent high temperatures in the labelling chamber.

Low-temperature stress simulation

An artificial climate chamber was used for simulating low-temperature stress at heading stage of rice. After the ¹³C and ¹⁴N labelling, half of the pots for each rice variety were moved into the artificial climate chamber (Fig. 1B and 1C), and the low-temperature treatment was conducted from 20: 00 pm to 8: 00 am the next day. The extreme low-temperature treatment was divided into four periods of 3 hours each, and the temperature of each period from the beginning to the end was 14℃, 11℃, 10℃ and 13℃ in order. And the temperature of the control treatment from the beginning to the end was 25℃, 23℃, 22℃ and 24℃ in order (Fig. 1D). The artificial climate chamber was controlled to give potted plants light at 5:00 a.m. The extreme low-temperature treatment lasted for 7 days (night of July 30 to morning of August 5). Figure 2 presented the effect of low-temperature treating on air and soil temperatures. The mean air and soil temperatures of 20:00 to 8:00 under low-temperature treatment were 12.4 ~ 13.2^oC, and 15.2 ~ 16.8 ^oC, respectively, which was suitable for simulating chilling stress in the experimental site. After the low-temperature treating completed, all the pots were moved from the artificial climate chamber to the natural conditions.

Plant and soil sampling and measurement

Plant and soil samples were collected three times at 5 August, 27 August, and 7 September, 2019. The rice was pulled out with the root and the rhizosphere soil was collected by shaking method when sampling. The bulk soil was also sampled from the pot. The rice plants were separated according to the root, stem, leaf and panicle, then put into the oven at 105°C for 30 min to kill, and then baked at 65°C until constant weight. After taking out, the dry matter weight of each part was weighed on a one-hundredth scale. The rhizosphere and bulk soil was placed in a cool and dry environment to dry naturally. The soil and plant samples were ground with a ball mill until they met the test criteria. The processed samples were determined by isotope mass spectrometry (Elementar Isoprime 100, Germany) to determine the values of total C and N as well as δ¹³C and δ¹⁵N for each fraction.

The contents of ¹³C and ¹⁵N in plants (root, stem, leaf, panicle) and soil (rhizosphere and bulk soils) can be calculated by the following formula.

¹³C_i=C_i×(δ¹³C_i -δ¹³C_n)/100×1000 (1)

¹⁵N_i=C_i×(δ¹⁵N_i -δ¹⁵N_n)/100×1000 (2)

¹³C_i and ¹⁵N_i represent ¹³C and ¹⁵N contents (mg· pot^− 1), δ¹³C_i and ¹³C_n represent abundance of ¹³C in labeled and unlabeled samples (‰), δ¹⁵N_i and ¹⁵N_n represent abundance of ¹⁵N in labeled and unlabeled samples (‰), respectively. C_i and N_i represent the total C and N content (mg· pot^− 1) in plants (panicle, stem, leaf, and root) and soil (rhizosphere and bulk soil).

The total assimilation of ¹³C and ¹⁵N was the sum of ¹³C and ¹⁵N of plants (root, stem, leaf, panicle) and soils (rhizosphere soil, bulk soil) measured at the end of labeling.

Total ¹³C assimilation = ¹³C in panicle + ¹³C in stem + ¹³C in leaf + ¹³C in root + ¹³C in rhizosphere soil + ¹³C in bulk soil (3)

Total ¹⁵N assimilation = ¹⁵N in panicle + ¹⁵N in stem + ¹⁵N in leaf + ¹⁵N in root + ¹⁵N in rhizosphere soil + ¹⁵N in bulk soil (4)

The incorporation of ¹³C (% of assimilated ¹³C) and ¹⁵N (% of assimilated ¹⁵N) into panicle, stem, leaf, root, rhizosphere, and bulk soil at each sampling date were calculated as follows:

¹³C incorporation (%) =¹³C_i / Total ¹³C assimilation×100% (5)

¹⁵N incorporation (%) = ¹⁵N_i / Total ¹⁵N assimilation×100% (6)

Statistical analysis

The PROC GLM procedure in SAS (SAS Institute Inc., Version 9.2, Cary, NC) was used to analyze the effects of treatments on rice biomass, rice yield and its component factors, ¹⁵N and ¹³C contents, percentage distribution of the assimilated ¹⁵N and ¹³C. The parameters mentioned above were analyzed using the MIXED procedure of SAS, with sampling date, temperature treatment, and variety were used as fixed effects (Littell, Milliken, Stroup, Wolfnger, & Schabenberger, 2006), and Compound symmetry covariance structure was used for repeated measures analysis. Means were compared using Fisher’s protected least significant difference (LSD) test at the 0.05 probability level.

Rice biomass

Both low-temperature at the heading stage and rice variety treatments affected dry matter accumulation and distribution of rice at each growing stage (Table 1). Generally, low-temperature treatment reduced total dry matter accumulation of rice plants. while rice varieties affected stem and total biomass. The interaction of low-temperature and variety also significantly affected rice stem and total biomass. On 5 August (heading stage), the low-temperature treatment reduced the rice biomass of both rice varieties, with the total rice biomass of the JN809 and J88 varieties being 11.6% and 6.5% lower than CK, respectively. The low-temperature treatment mainly reduced the biomass of rice stem and leaf, with the biomass of rice stem of JN809 and J88 varieties being 12.5% and 6.5% lower than CK, respectively, and the biomass of rice leaf of JN809 and J88 varieties being 13.7% and 15.4% lower than CK, respectively. There was no difference in biomass of each part between the two varieties. On 27 August, the low-temperature treatment reduced rice biomass. The root, stem, leaf, panicle and total biomass of rice of J88 under low-temperature treatment were all lower than CK, respectively. Rice leaf and panicle biomass of JN809 under low-temperature treatment were 12.8% and 12.6% lower than CK. On 23 September (rice harvesting period), low-temperature treatment reduced rice biomass, with rice panicle biomass of JN809 being 29.3% lower than CK. The root, panicle and total biomass of rice of J88 under low-temperature treatment were 10.7%, 25.0% and 5.7% lower than CK, respectively. There was no difference in the biomass of all parts of rice of the two varieties under low-temperature treatment.

Table 1

Rice biomass in different sampling period (Unit: g pot^− 1).
Date	Temperature	Variety	Root	Stem	Leaf	Panicle	Total biomass
5 Aug.	CK	JN809	14.75 ± 0.81 a A	29.02 ± 2.41 a A	19.75 ± 0.58 a A	5.50 ± 0.41 a A	69.01 ± 3.10 a A
		J88	14.02 ± 0.16 a A	30.66 ± 0.16 a A	20.26 ± 1.08 a A	4.76 ± 0.37 a A	69.70 ± 0.93 a A
	LT	JN809	13.64 ± 1.38 a A	25.38 ± 0.71 b B	17.05 ± 0.47 b A	4.94 ± 0.05 a A	61.01 ± 1.98 b A
		J88	14.11 ± 0.86 a A	28.68 ± 1.13 b A	17.13 ± 0.76 b A	5.28 ± 0.43 a A	65.20 ± 2.17 b A
27 Aug.	CK	JN809	16.09 ± 0.83 a B	28.80 ± 0.58 b B	19.26 ± 0.71 a A	24.19 ± 0.44 a A	88.34 ± 1.95 a B
		J88	18.64 ± 0.34 a A	41.60 ± 0.93 a A	19.00 ± 1.05 a A	21.42 ± 1.25 a B	100.66 ± 0.36 a A
	LT	JN809	16.13 ± 0.69 a A	32.34 ± 0.55 a A	16.79 ± 0.88 b A	21.15 ± 2.10 b A	86.41 ± 2.50 a A
		J88	17.38 ± 0.62 b A	32.02 ± 0.56 b A	14.80 ± 0.25 b B	18.15 ± 0.24 b B	82.35 ± 1.59 b A
23 Sept.	CK	JN809	24.20 ± 0.60 a A	41.92 ± 3.39 a B	16.20 ± 0.36 a B	24.26 ± 1.94 a A	106.58 ± 2.68 a B
		J88	23.82 ± 0.37 a A	47.94 ± 1.64 a A	18.75 ± 1.01 a A	25.78 ± 0.51 a A	113.75 ± 1.90 a A
	LT	JN809	25.16 ± 0.61 a A	47.04 ± 3.28 a A	16.15 ± 0.65 a A	17.15 ± 1.68 b A	105.50 ± 1.90 a A
		J88	21.27 ± 0.17 b B	47.04 ± 0.50 a A	17.04 ± 0.37 a A	19.33 ± 0.11 b A	107.24 ± 0.76 b A
			P value
Low-temperature (T)			0.61	0.06	< 0.01	< 0.01	< 0.01
Variety (V)			0.77	< 0.01	0.49	0.47	< 0.01
T × V			0.55	< 0.01	0.15	0.65	0.01

CK and LT denote control treatment and low-temperature treatment, respectively. Different lowercase letters in the same column indicate significant differences between the CK and LT treatment for the same variety at the probability level of 0.05. While different capital letters in the same column indicate significant differences between different varieties of the same temperature treatment at the probability level of 0.05. The same below.

Rice yield and its component factors

The low-temperature treatment affected rice panicle number and yield (Fig. 3). The number of rice panicle, kernels per panicle, thousand grain weight, and yield were different between varieties, and the low-temperature treatment × variety had no effect on rice yield and yield components. The number of kernels per panicle was 20.2% and 15.1% lower in JN809 and J88 than in CK, respectively. Rice yield of JN809 and J88 under low-temperature treatment was 27.6% and 21.4% lower than those of CK, respectively. The low-temperature treatment had no effect on the number of panicle and thousand grain weight of rice. The kernels per panicle and yield of JN809 were 57.4% and 32.3% lower than those of J88 variety, respectively.

CK and LT denote control treatment and low-temperature treatment, respectively. Bar means the standard error. Different lowercase letters for same variety indicate significant differences between the CK and LT treatments at the probability level of 0.05, while different capital letters for same temperature treatment indicate significant differences between different varieties at the probability level of 0.05.

N uptake

The sampling period, low-temperature treatment, rice variety and their interaction all affected N uptake by rice (Table 2). On 5 August (heading stage), the rice rhizosphere soil ¹⁵N isotopic content of both varieties of rice under the low-temperature treatment was lower than that of CK, while the bulk soil ¹⁵N content was higher than that of CK. The rice rhizosphere soil ¹⁵N contents of JN809 and J88 under low-temperature treatment were 50.0% and 20.2% lower than CK, respectively, while the bulk soil ¹⁵N contents were 41.6% and 20.6% higher than CK, respectively. Rice leaf and panicle ¹⁵N contents under the low-temperature treatment was 26.5% and 104.0% higher in the J88 variety than CK, respectively. The contents of ¹⁵N in different parts of the rice-soil system differed among varieties, with rice rhizosphere soil, rice stem, leaf and panicle of J88 variety accumulating 66.7%, 42.2%, 20.5% and 27.2% more ¹⁵N than JN809 under the low-temperature treatment, respectively.

On 27 August (filling stage), the low-temperature treatment reduced the ¹⁵N accumulations of rice rhizosphere soil, rice leaf and rice panicle. The ¹⁵N contents of rice panicle of JN809 and J88 were 18.1% and 18.9% lower than that of CK, respectively. In contrast, the bulk soil ¹⁵N content of rice of J88 variety under low-temperature treatment was 171.7% higher than that of CK. The bulk soil ¹⁵N content of J88 was 115.5% higher than that of JN809 under the low-temperature treatment, while the rice leaf ¹⁵N content was 33.5% lower than that of JN809. On 23 September (harvesting stage), the low-temperature treatment increased ¹⁵N accumulation of rice rhizosphere soil, bulk soil and rice stem, while it decreased ¹⁵N accumulation in rice panicle. The bulk soil ¹⁵N content was 31.6% and 23.8% higher in the JN809 and J88 than CK, and rice stem ¹⁵N content was 15.5% higher in the J88 variety than CK, while rice panicle ¹⁵N contents was lower in the JN809 and J88 than CK by 18.9% and 26.0%, respectively. Under the low-temperature treatment, rice soil, rice stem and root ¹⁵N contents of J88 variety was 56.0%, 28.2% and 32.2% higher than that of JN809, respectively.

Table 2

The content of ¹⁵N retained in rice-soil system during different growing stages (Unit: mg pot^− 1)
Date	Temperature	Variety	¹⁵N in each compartment
Date	Temperature	Variety	Rhizosphere soil	Bulk soil	Stem	Leaf	Root	Panicle
5 Aug.	CK	JN809	2.70 ± 0.06 a A	1.01 ± 0.02 b B	5.26 ± 0.29 a A	7.50 ± 0.30 a A	1.99 ± 0.12 a B	1.28 ± 0.13 a A
		J88	2.82 ± 0.20 a A	1.26 ± 0.01 b A	5.01 ± 0.20 b A	6.10 ± 0.22 a B	2.59 ± 0.27 a A	1.01 ± 0.05 b A
	LT	JN809	1.35 ± 0.02 b B	1.43 ± 0.22 a A	4.46 ± 0.06 a B	5.50 ± 0.39 a B	1.73 ± 0.12 a A	1.62 ± 0.01 a B
		J88	2.25 ± 0.11 b A	1.52 ± 0.08 a A	6.34 ± 0.36 a A	6.63 ± 0.09 a A	1.88 ± 0.12 b A	2.06 ± 0.13 a A
27 Aug.	CK	JN809	2.51 ± 0.20 a A	0.50 ± 0.04 a A	4.50 ± 0.12 a A	4.11 ± 0.13 a A	1.48 ± 0.03 a B	3.60 ± 0.21 a A
		J88	1.17 ± 0.17 a B	0.46 ± 0.02 b A	5.03 ± 0.23 a A	4.20 ± 0.28 a A	1.87 ± 0.05 a A	3.92 ± 0.07 a A
	LT	JN809	1.26 ± 0.04 b A	0.58 ± 0.02 a B	5.07 ± 0.28 a A	4.27 ± 0.19 a A	1.81 ± 0.10 a A	2.95 ± 0.08 b A
		J88	1.40 ± 0.09 a A	1.25 ± 0.05 a A	4.82 ± 0.04 a A	2.84 ± 0.35 b B	1.81 ± 0.09 a A	3.18 ± 0.02 b A
23 Sept.	CK	JN809	0.69 ± 0.10 b A	0.38 ± 0.02 b B	6.45 ± 0.64 a B	2.43 ± 0.25 a A	1.90 ± 0.19 a B	3.71 ± 0.04 a B
		J88	0.82 ± 0.00 a B	0.63 ± 0.01 b A	7.60 ± 0.14 b A	2.26 ± 0.01 a A	2.35 ± 0.26 a A	4.31 ± 0.12 a A
	LT	JN809	0.94 ± 0.10 a A	0.50 ± 0.03 a B	6.85 ± 0.11 a B	2.33 ± 0.03 a A	2.36 ± 0.15 a B	3.01 ± 0.04 b A
		J88	0.79 ± 0.11 a A	0.78 ± 0.03 a A	8.78 ± 0.40 a A	2.84 ± 0.35 a A	3.12 ± 0.20 a A	3.19 ± 0.07 b A
			P value
Date (A)			< 0.01	< 0.01	< 0.01	< 0.01	0.01	< 0.01
Low-temperature (B)			< 0.01	< 0.01	0.06	0.63	0.44	< 0.01
Variety (C)			0.71	< 0.01	< 0.01	0.67	< 0.01	< 0.01
A×B			< 0.01	0.08	0.44	0.04	< 0.01	< 0.01
A×C			< 0.01	0.50	0.04	0.68	0.36	0.21
B×C			< 0.01	0.07	0.10	< 0.01	0.44	0.66
A×B×C			< 0.01	< 0.01	0.03	0.02	0.34	0.01

C uptake

Sampling period, low-temperature treatment, rice variety and their interaction all affected the partitioning of photosynthetic products in rice (Table 3). On August 5 (heading stage), The ¹³C contents of the bulk soil of JN809 and J88 varieties under the low-temperature treatment was 26.7% and 113.3% higher than those of CK, respectively. The ¹³C isotope contents of panicle of JN809 and J88 varieties under the low-temperature treatment was 37.9% and 69.2% lower than those of CK, respectively. Under the low-temperature treatment, the ¹³C isotope accumulations in various parts of different rice varieties differed, among which the ¹³C isotope accumulations in rice rhizosphere soil, bulk soil and rice stem of J88 variety was 50.0%, 68.4% and 13.1% higher than that of JN809, respectively

Table 3

The content of ¹³C retained in rice-soil system (Unit: mg pot^− 1)
Date	Temperature	Variety	¹³C in each compartment
Date	Temperature	Variety	Rhizosphere soil	Bulk soil	Stem	Leaf	Root	Panicle
5 Aug.	CK	JN809	1.61 ± 0.07 a A	0.15 ± 0.00 b A	19.58 ± 0.66 a A	13.92 ± 1.02 a B	5.23 ± 0.10 a B	2.43 ± 0.07 a B
		J88	0.83 ± 0.06 a B	0.15 ± 0.01 b A	19.07 ± 0.52 a A	16.24 ± 1.55 a A	8.45 ± 0.38 a A	3.35 ± 0.09 a A
	LT	JN809	0.64 ± 0.04 b B	0.19 ± 0.00 a B	16.96 ± 1.12 b B	12.25 ± 0.53 a A	6.43 ± 0.81 a A	1.51 ± 0.14 b A
		J88	0.96 ± 0.04 a A	0.32 ± 0.02 a A	19.18 ± 0.89 a A	9.16 ± 0.22 b B	4.71 ± 0.11 b B	1.03 ± 0.08 b A
27 Aug.	CK	JN809	1.30 ± 0.02 a A	0.15 ± 0.01 b B	12.44 ± 0.23 b A	11.38 ± 0.28 b A	5.22 ± 0.36 a A	2.92 ± 0.09 a A
		J88	1.42 ± 0.21 a A	0.20 ± 0.01 a A	9.21 ± 0.27 b B	6.81 ± 0.59 a B	5.68 ± 0.18 b A	2.34 ± 0.39 a A
	LT	JN809	0.95 ± 0.02 b A	0.23 ± 0.01 a A	15.85 ± 0.30 a A	14.02 ± 0.67 a A	5.45 ± 0.33 a A	1.73 ± 0.21 b A
		J88	0.87 ± 0.08 b A	0.16 ± 0.03 b B	13.41 ± 0.11 a B	6.13 ± 0.10 a B	8.04 ± 0.26 a A	2.02 ± 0.08 a A
23 Sept.	CK	JN809	1.02 ± 0.04 a A	0.18 ± 0.01 a B	25.88 ± 0.16 b A	5.41 ± 0.23 b B	3.85 ± 0.05 b B	2.91 ± 0.17 a A
		J88	1.03 ± 0.07 a A	0.14 ± 0.01 b B	24.33 ± 0.61 b A	5.04 ± 0.17 b B	4.29 ± 0.08 b B	2.79 ± 0.15 a A
	LT	JN809	0.64 ± 0.05 b A	0.21 ± 0.02 a A	28.64 ± 0.29 a A	6.29 ± 0.16 a A	6.54 ± 0.63 a A	1.75 ± 0.28 b B
		J88	0.73 ± 0.03 b A	0.23 ± 0.01 a A	28.55 ± 2.11 a A	6.13 ± 0.10 a A	6.73 ± 0.88 a A	2.28 ± 0.17 a A
			P value
Date (A)			< 0.01	0.35	< 0.01	< 0.01	0.08	0.11
Low-temperature (B)			< 0.01	< 0.01	< 0.01	0.03	0.01	< 0.01
Variety (C)			0.32	0.12	0.12	< 0.01	0.01	0.48
A×B			0.70	< 0.01	< 0.01	< 0.01	< 0.01	0.02
A×C			0.09	< 0.01	0.04	< 0.01	0.30	0.43
B×C			< 0.01	0.15	0.16	< 0.01	0.11	0.87
A×B×C			< 0.01	< 0.01	0.78	0.04	< 0.01	< 0.01

On 27 August (filling stage), the ¹³C isotope contents of rice rhizosphere soil of varieties JN809 and J88 under the low-temperature treatment was 26.9% and 38.7% lower than that of CK, respectively. The ¹³C isotope content of bulk soil of J88 variety under low-temperature treatment was 20.0% lower than that of CK, whereas the ¹³C isotope contents of bulk soil and rice leaf of JN809 variety under low-temperature treatment were 16.7% and 23.2% higher than that of CK, respectively. The ¹³C isotopic contents of rice stem under the low-temperature treatment was 27.4% and 45.6% higher than that of CK for JN809 and J88 varieties, respectively, while the ¹³C content of rice panicle under the low-temperature treatment was 40.8% lower than that of CK for JN809 variety. On 23 September (harvesting stage), rice rhizosphere soil ¹³C accumulations was 37.3% and 29.1% lower under the low-temperature treatment than CK for JN809 and J88 varieties, respectively, while rice panicle ¹³C accumulation was 39.9% lower for JN809 variety than CK. Rice stem, leaf and root ¹³C accumulations under the low-temperature treatment was 10.7%, 16.3% and 69.9% higher than CK for the JN809 variety, while bulk soil, rice stem, leaf and root ¹³C accumulations were 64.3%, 17.3%, 21.6% and 56.9% higher than CK for the J88 variety, respectively. The accumulation of ¹³C in rice panicle of J88 variety was 30.3% higher than that of JN809 variety under low-temperature treatment.

Variation of the assimilated ¹⁵N in rice-soil system

Sampling period, low-temperature treatment, rice variety and their interaction all affected the proportion of ¹⁵N partitioning (Table 4). On August 5 (heading stage), the percentage of soil ¹⁵N isotope allocation in the rice rhizosphere soil of different rice varieties under the low-temperature treatment was higher than that in CK. The percentage distribution of soil ¹⁵N in the rice rhizosphere soil of JN809 and J88 varieties were 5.00 and 2.79 percentage points lower than that of CK, while the percentage distribution of soil ¹⁵N in bulk soil was 1.55 and 1.24 percentage points higher than that of CK, respectively. The percentage of ¹⁵N allocated to rice stem and leaf of JN809 variety was 2.96 and 7.35 percentage points lower than that of CK, while the percentage of ¹⁵N allocated to rice root of J88 variety was 3.52 percentage points lower than that of CK. The proportion of ¹⁵N in the rice panicle was 1.26 and 5.17 percentage points lower in JN809 and J88 varieties, respectively, than in CK. The proportion of ¹⁵N allocated to each part of the rice-soil system differed among varieties. Among them, the ¹⁵N allocation ratios of rice rhizosphere soil, bulk soil, rice stem, leaf and root of J88 variety were 6.17, 2.20, 14.86, 12.46 and 2.91 percentage points higher than those of JN809 variety under the low-temperature treatment, respectively.

On 27 August (filling stage), the low-temperature treatment reduced the ¹⁵N allocation ratio of rice rhizosphere soil, and rice panicle. The ¹⁵N allocation ratio of rice rhizosphere soil of JN809 variety was 4.59 percentage points lower than that of CK, and the ¹⁵N allocation ratio of rice panicle of JN809 and J88 varieties were 2.39 and 3.66 percentage points lower than that of CK, respectively. In contrast, the proportion of soil ¹⁵N allocated to rice panicle of J88 variety under the low-temperature treatment was 3.91 percentage points higher than that of CK. The proportion of ¹⁵N allocated to bulk soil, rice stem, root and panicle of J88 variety under low-temperature treatment was 4.04, 5.13, 2.31 and 4.84 percentage points higher than that of JN809 variety, respectively. On 23 September (harvesting stage), the low-temperature treatment increased the proportion of ¹⁵N allocated to rice stem, leaf and root, while it decreased the proportion of ¹⁵N allocated to rice panicle. The low-temperature treatment increased the ¹⁵N allocation to rice stem, leaf and root of J88 variety by 5.81, 2.83 and 3.79 percentage points, respectively, while the low-temperature treatment decreased the ¹⁵N allocation to rice panicle of JN809 and J88 varieties by 2.56 and 5.56 percentage points, respectively, compared with CK. Bulk soil, rice stem, leaf, root and panicle ¹⁵N accumulations of J88 variety under low-temperature treatment were 2.01, 18.11, 5.42, 6.70 and 4.64 percentage points higher than that of JN809 variety, respectively.

Table 4

Percentage distribution of the assimilated ¹⁵N in rice-soil system (Unit: %)
Date	Temperature	Variety	Percentage distribution of the assimilated ¹⁵N in each compartment
			Rhizosphere soil	Bulk soil	Stem	Leaf	Root	Panicle
5 Aug.	CK	JN809	9.96 ± 0.22 a B	3.73 ± 0.08 b B	19.39 ± 1.08 a B	27.63 ± 1.09 a B	7.33 ± 0.44 a B	5.97 ± 0.02 a B
		J88	13.92 ± 0.99 a A	6.24 ± 0.03 b A	24.75 ± 0.98 b A	30.14 ± 1.09 b A	12.79 ± 1.33 a A	10.17 ± 0.62 a A
	LT	JN809	4.96 ± 0.09 b B	5.28 ± 0.83 a B	16.43 ± 0.20 b B	20.28 ± 1.42 b B	6.36 ± 0.44 a B	4.71 ± 0.49 b A
		J88	11.13 ± 0.54 b A	7.48 ± 0.39 a A	31.29 ± 1.78 a A	32.74 ± 0.46 a A	9.27 ± 0.61 b A	5.00 ± 0.23 b A
27 Aug.	CK	JN809	9.24 ± 0.73 a A	1.83 ± 0.13 a A	16.59 ± 0.45 a B	15.13 ± 0.49 a B	5.44 ± 0.11 a B	13.26 ± 0.76 a B
		J88	5.78 ± 0.83 a B	2.25 ± 0.11 b A	24.83 ± 1.12 a A	20.73 ± 1.36 a A	9.24 ± 0.27 a A	19.37 ± 0.35 a A
	LT	JN809	4.65 ± 0.16 b A	2.12 ± 0.07 a B	18.67 ± 1.04 a B	15.72 ± 0.71 a A	6.65 ± 0.38 a B	10.87 ± 0.29 b B
		J88	6.89 ± 0.43 a A	6.16 ± 0.23 a A	23.80 ± 0.21 a A	14.01 ± 1.74 b A	8.96 ± 0.44 a A	15.71 ± 0.10 b A
23 Sept.	CK	JN809	2.53 ± 0.37 a B	1.42 ± 0.08 a B	23.76 ± 2.37 a B	8.97 ± 0.92 a B	7.00 ± 0.70 a B	13.65 ± 0.17 a B
		J88	4.07 ± 0.02 a A	3.10 ± 0.05 a A	37.54 ± 0.68 b A	11.18 ± 0.03 b A	11.62 ± 1.3 b A	21.29 ± 0.61 a A
	LT	JN809	3.45 ± 0.36 a A	1.85 ± 0.11 a B	25.24 ± 0.42 a B	8.59 ± 0.09 a B	8.71 ± 0.56 a B	11.09 ± 0.15 b B
		J88	3.90 ± 0.56 a A	3.86 ± 0.13 a A	43.35 ± 2.00 a A	14.01 ± 1.74 a A	15.41 ± 1.01 a A	15.73 ± 0.37 b A
			P value
Date (A)			< 0.01	< 0.01	< 0.01	< 0.01	< 0.01	< 0.01
Low-temperature (B)			< 0.01	< 0.01	0.03	0.99	0.54	< 0.01
Variety (C)			< 0.01	< 0.01	< 0.01	< 0.01	< 0.01	< 0.01
A×B			< 0.01	0.02	0.35	0.09	< 0.01	< 0.01
A×C			< 0.01	0.57	< 0.01	0.13	0.14	< 0.01
B×C			< 0.01	< 0.01	0.05	< 0.01	0.53	0.83
A×B×C			< 0.01	< 0.01	0.02	0.05	0.18	< 0.01

Variation of the assimilated ¹³C in rice-soil system

Sampling period, low-temperature treatment, rice variety and their interaction all affected the proportion of photosynthetic products allocated to rice (Table 5). On August 5 (heading stage), the proportion of ¹³C assigned to the bulk soil of varieties JN809 and J88 under the low-temperature treatment was 0.08 and 0.36 percentage points higher than that of CK, respectively. The proportions of ¹³C isotopes in rice stem and panicle of JN809 variety were 5.64 and 1.98 percentage points lower than those in CK, whereas the proportions of ¹³C isotopes in rice leaf, root and panicle of J88 variety were 14.75, 7.80 and 4.84 percentage points lower than those in CK, respectively. The ¹³C isotope distribution ratios of different parts of rice varieties under low-temperature treatment were different. The ¹³C isotope allocation ratios of bulk soil and rice stem of J88 variety were 0.26 and 3.45 percentage points higher than those of JN809 variety, respectively, while those of rice leaf and root of J88 variety were 7.29 and 4.05 percentage points lower than those of JN809 variety, respectively.

On 27 August (filling stage), the ¹³C isotope partitioning ratios of rice rhizosphere soil of JN809 and J88 varieties under the low-temperature treatment were 0.77 and 1.15 percentage points lower than those of CK, respectively. In contrast, the proportion of ¹³C isotopes assigned to bulk soil of the JN809 variety under the low-temperature treatment was 0.20 percentage points higher than that of CK. The proportion of ¹³C assigned to rice stem and leaf of JN809 variety under low-temperature treatment was 7.35 and 5.69 percentage points higher than that of CK, respectively, while the proportion of ¹³C assigned to rice panicle of JN809 variety was 2.6 percentage points lower than that of CK. The proportion of ¹³C isotopes assigned to rice stem and root of J88 variety under low-temperature treatment was 8.74 and 4.91 percentage points higher than that of CK, respectively. On September 23 (harvesting stage), the proportion of ¹³C isotopes assigned to rice rhizosphere soil of JN809 and J88 varieties under low-temperature treatment were 0.83 and 0.64 percentage points lower than CK, respectively, while the proportion of ¹³C isotope assigned to rice panicle of JN809 variety was 2.49 percentage points lower than CK. The proportions of ¹³C isotopes assigned to bulk soil, rice stem, leaf and root of J88 variety were 0.21, 8.80, 2.27 and 5.07 percentage points higher than CK, respectively. There was no difference in ¹³C allocation proportions between JN809 and J88 varieties under the low-temperature treatment.

Table 5

Percentage distribution of the assimilated ¹³C in rice-soil system (Unit: %)
Date	Temperature	Variety	Percentage distribution of the assimilated ¹³C in each compartment
Date	Temperature	Variety	Rhizosphere soil	Bulk soil	Stem	Leaf	Root	Panicle
5 Aug.	CK	JN809	3.47 ± 0.16 a A	0.33 ± 0.01 b A	42.18 ± 1.41 a A	29.98 ± 2.20 a A	11.26 ± 0.21 a B	5.23 ± 0.15 a B
		J88	1.73 ± 0.13 a B	0.31 ± 0.01 b A	39.76 ± 1.09 a B	33.85 ± 3.23 a A	17.61 ± 0.79 a A	6.99 ± 0.19 a A
	LT	JN809	1.38 ± 0.10 b A	0.41 ± 0.00 a B	36.54 ± 2.42 b B	26.39 ± 1.14 a A	13.86 ± 1.75 a A	3.25 ± 0.31 b A
		J88	1.50 ± 0.44 a A	0.67 ± 0.04 a A	39.99 ± 1.86 a A	19.10 ± 0.46 b B	9.81 ± 0.23 b B	2.15 ± 0.17 b A
27 Aug.	CK	JN809	2.81 ± 0.03 a A	0.31 ± 0.02 b B	26.79 ± 0.50 b A	24.52 ± 0.60 b A	11.24 ± 0.77 a B	6.30 ± 0.19 a A
		J88	2.95 ± 0.43 a A	0.41 ± 0.01 a A	19.21 ± 0.57 b B	20.91 ± 1.29 a B	11.84 ± 0.37 b A	4.87 ± 0.81 a B
	LT	JN809	2.04 ± 0.05 b A	0.51 ± 0.02 a A	34.14 ± 0.64 a A	30.21 ± 1.44 a A	11.74 ± 0.72 a A	3.73 ± 0.46 b A
		J88	1.80 ± 0.16 b A	0.34 ± 0.05 a B	27.95 ± 0.23 a B	12.77 ± 0.20 b B	16.75 ± 0.53 a A	4.21 ± 0.17 a A
23 Sept.	CK	JN809	2.20 ± 0.08 a A	0.40 ± 0.01 a A	55.76 ± 0.35 b A	11.66 ± 0.49 b B	8.29 ± 0.10 b B	6.26 ± 0.36 a A
		J88	2.15 ± 0.15 a A	0.28 ± 0.02 b B	50.73 ± 1.27 b B	10.50 ± 0.36 b B	8.95 ± 0.17 b B	5.81 ± 0.31 a A
	LT	JN809	1.37 ± 0.11 b A	0.45 ± 0.05 a A	61.69 ± 0.63 a A	13.56 ± 0.33 a A	14.09 ± 1.36 a A	3.77 ± 0.60 b A
		J88	1.51 ± 0.06 b A	0.49 ± 0.02 a A	59.53 ± 4.40 a A	12.77 ± 0.20 a A	14.02 ± 1.84 a A	4.76 ± 0.36 a A
			P value
Date (A)			< 0.01	0.34	< 0.01	< 0.01	0.08	0.11
Low-temperature (B)			< 0.01	< 0.01	< 0.01	0.04	0.01	< 0.01
Variety (C)			0.12	0.44	0.01	< 0.01	0.04	0.88
A×B			0.71	< 0.01	< 0.01	< 0.01	< 0.01	0.02
A×C			0.09	< 0.01	0.06	< 0.01	0.3	0.43
B×C			< 0.01	0.16	0.18	< 0.01	0.11	0.76
A×B×C			< 0.01	< 0.01	0.74	0.04	< 0.01	< 0.01

Effect of low-temperature on rice biomass and yield

Rice spikelet fertility, filling and setting rate are most susceptible to temperature extremes mainly in the last week before and during heading stage, and low-temperatures during heading stage resulted in reduced rice biomass and yield (Lü et al. 2013; Ren et al. 2017). In the present study, it was found that rice yield of JN809 and J88 treated with low-temperature during heading stage was 27.6% and 21.4% lower than CK, which is consistent with previous studies (Ghadirnezhad and Fallah 2014; Zeng et al. 2017). The reasons might be that low-temperature stress led to spikelet abortion and reduced kernels per panicle and yield (Jia et al. 2019). Furthermore, low-temperature stress also reduced photosynthetic rate, chlorophyll fluorescence and dry matter accumulation, therefore resulted in lower yield (Siddik et al. 2019; Ai et al. 2023). Moreover, the reduction in N uptake under low-temperature treatment could likewise lead to a decrease in leaf area index and net photosynthetic rate, which in turn inhibited normal panicle development (Jia et al. 2019).

Different varieties have different ability to tolerate low temperature stress (Geraldine et al. 2020). In this study, the yield decline of low temperature tolerant variety J88 after low-temperature stress treatment was significantly lower than that of JN809 variety. This may be because the low-temperature tolerant variety J88, with higher physiological adaptive capacity, secreted more antioxidant enzymes from the leaves after being subjected to low-temperature stress to resist the adversity stress, thus slowing down the effect of low-temperature stress on the development of rice pollen mother cells and glumes (Shimono et al. 2007), which resulted in a lower rate of rice empty shells and a smaller decrease in yield (Susanti et al. 2019). This phenomenon was confirmed by the significantly higher kernel number of J88 variety than that of JN809 variety in the present study. Ali et al. (2021) similarly found that low-temperature tolerant varieties showed less yield reduction after exposure to low-temperature stress.

Effect of low-temperature on N allocation

Low-temperature cold damage interferes with plant physiological metabolic processes such as water metabolism, mineral nutrition, photosynthesis, respiration, and metabolism, and has a significant effect on their uptake of soil N (Lu et al. 2005; Zhao et al. 2015). Our results showed that the rhizosphere soil ¹⁵N contents of JN809 and J88 under low-temperature treatment were significantly lower than CK, while the bulk soil ¹⁵N contents were significantly higher than CK, respectively. These results indicate that low-temperature treatment reduced soil N uptake by rice root, which was mainly due to the weakened photosynthesis and reduced physiological metabolism of rice due to low-temperature, thus leading to lower nutrient demand of rice plants (Jia et al. 2019). Moreover, the total biomass of JN809 and J88 was lower under the low-temperature treatment than CK, respectively, which indicated that low-temperature could reduce nutrient requirement of the rice plant. Low-temperature stress leads to a reduction in the rate of N transport and a decrease in N accumulation in the rice panicle (Shimono et al. 2012). In this study, it was found that low-temperature stress during the heading stage led to a tendency for N accumulation in the bulk soil and stem and leaf parts, while the accumulation in the panicle was reduced (Table 3). At rice harvest, the bulk soil ¹⁵N isotope contents of JN809 and J88 varieties treated at low-temperature stress were higher than CK, respectively, while the panicle ¹⁵N isotope contents were lower than CK, respectively. This suggests that low-temperature stress reduced N uptake by rice and affects N translocation to the rice panicle (Shimono et al. 2012; Liu et al. 2018). Jia et al. (2019) also found that low-temperature chilling reduced the ability of rice to absorb N and reduced rice N production by 4%-47%.

Effect of low-temperature on C allocation

Plant photosynthetic C is an important component of the atmosphere-plant-soil C cycle in terrestrial ecosystem (Schlesinger and Andrews 2000). Plants convert CO₂ into organic matter through the photosynthetic C assimilation pathway, and the resulting photosynthetic C is transported through the plant phloem and distributed to the plant-soil system. A portion of this photosynthetic C is imported into the below-ground part for root growth, while C is imported to the soil in the form of root deposits (Uchida et al. 2010). The other part is stored in the above-ground part of the plant. Low-temperature treatment affected photosynthetic C allocation in rice (Jia et al. 2019, 2022). In this study, we found that at the end of the low-temperature treatment, the soil ¹³C isotope contents of the low-temperature treated JN809 and J88 varieties was 26.7% and 113.3% higher than CK, while the rice panicle ¹³C isotope contents of JN809 and J88 were significantly lower than CK, respectively. This may be due to the low-temperature treatment slowing down the fertility process in rice. The proportion of photosynthetic C allocated to the root system and soil was high in the vegetative growth stage of the rice-soil system (Werth and Kuzyakov 2010). The proportion of photosynthetic C allocated to the root system and soil tended to decrease as the reproductive period progresses (Deng et al. 2017; Zang et al. 2019), and photosynthetic C tended to be allocated more towards the panicle portion. In addition, the reduction in soil N uptake by rice plants under the low-temperature treatment led to a decrease in leaf area index and net photosynthetic rate, which inhibited normal panicle development (Jia et al. 2019), then likewise resulted in reduced photosynthetic C transport to the panicle in rice. The ¹³C isotope contents of rice stem, leaf and root of different varieties under low-temperature treatment during rice harvest were higher than CK, and the ¹³C isotope content of rice panicle of J809 variety was lower than CK. This could also indicate that the low-temperature treatment affected the photosynthetic C transport in rice, leading to a reduction in photosynthetic C accumulation in the panicle, which in turn affected the formation of rice yield. As this study was only carried out once for ¹³C isotope labelling prior to the low-temperature treatment, it could not reveal the transport pathways of the newly transformed photosynthetic C after the low-temperature treatment. Follow-up studies could be carried out several times after the end of the low-temperature treatment for ¹³C isotope labelling, which could provide more clarity on the allocation of photosynthetic C to rice by the low-temperature treatment.

Low-temperature stress during the heading stage of rice reduced biomass and yield, mainly due to a decrease in the number of rice panicle and setting rate under low-temperature treatment. Low-temperature stress also affected C and N distribution in the rice-soil system. The C, N accumulation in bulk soil and rice stems and leaves tended to increase, while that in rice panicles decreased under low-temperature stress during the heading stage. The low temperature tolerance variety reduced the effects of low temperature stress on rice yield and the allocation of C and N between soil and rice. Considering the limitations of this experiment, further research is needed to better understand the mechanisms involved and find more effective countermeasures for rice encountering low-temperature damage.

The authors have no relevant financial or non-financial interests to disclose.

Acknowledgement

This work was funded by National Natural Science Founds of China (32172129), National Key Research and Development Program of China (2017YFD0300104), Modern Agro-industry Technology Research System-Green manure (CARS-22-G-16), Innovation Program of Chinese Academy of Agricultural Sciences (01-ICS-20), and Agricultural Scientific and Technological Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2023F03).

Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working paper No. 12 – 03. FAO, Rome
Ali I, Tang L, Dai J et al (2021) Responses of Grain Yield and Yield Related Parameters to Post-Heading Low-Temperature Stress in Japonica Rice. Plants 10(7):1425. https://doi.org/10.3390/plants10071425
Ai X, Xiong R, Tan X et al (2023) Low-temperature and light combined stress after heading on starch fine structure and physicochemical properties of late-season indica rice with different grain quality in southern China. Food Res Int 164:112320. https://doi.org/10.1016/j.foodres.2022.112320
Bhattacharjees S (2013) Heat and chilling induced disruption of redox homeostasis and its regulation by hydrogen peroxide in germinating rice seeds (Oryza sativa L, cultivar Ratna). Physiol Mol Biol Pla 19 (2):199–207. https://doi.org/10.1007/s12298-012-0159-x
Chen X, Wang L, Niu Z et al (2020) The effects of projected climate change and extreme climate on maize and rice in the Yangtze River Basin, China. Agr For Meteorol 282–283:107867. https://doi.org/10.1016/j.agrformet.2019.107867
Deng H, Che F, Xiao Y et al (2011) Effects of low-temperature stress during flowering period on pollen characters and flag leaf physiological and biochemical characteristics of rice. Chin J Appl Ecol 22(1):66–72 (In Chinese with English abstract). https://doi.org/10.13287/j.1001-9332.2011.0022
Deng YW, Tang C, Yuan HC et al (2017) The ¹³C-CO₂ pulsing labeling method: distribution of rice photosynthetic carbon in plant-soil system during different rice growth stages. Acta Ecol Sin 37(19):6466–6471 (in Chinese with English abstract). http://dx.doi.org/10.5846/stxb201607241506
Geraldine A, Junior A, Gastmann R et al (2020) Root responses of contrasting rice genotypes to low-temperature stress. J Plant Physiol 255:153307. https://doi.org/10.1016/j.jplph.2020.153307
Ghadirnezhad R, Fallah A (2014) Temperature effect on yield and yield components of different rice cultivars in flowering stage. Int J Agron 1–4. https://doi.org/10.1186/s12870-021-03056-9
Gomez-Zavaglia A, Mejuto JC, Simal-Gandara J (2022) Mitigation of emerging implications of climate change on food production system. Food Res Int 134:109256. https://doi.org/10.1016/j.foodres.2020.109256
Haas E, Carozzi M, Massad RS et al (2022) Long term impact of residue management on soil organic carbon stocks and nitrous oxide emissions from European croplands. Sci Total Environ 836:154932. https://doi.org/10.1016/j.scitotenv.2022.154932
Jia Y, Liu H, Wang H et al (2022) Effects of root characteristics on panicle formation in japonica rice under low-temperature water stress at the reproductive stage. Field Crop Res 277:108395. https://doi.org/10.1016/j.fcr.2021.108395
Jia Y, Wang J, Qu Z et al (2019) Effects of low water temperature during reproductive growth on photosynthetic production and nitrogen accumulation in rice. Field Crop Res 242:107587. https://doi.org/10.1016/j.fcr.2019.107587
Ju H, Marijn V, Lin E et al (2013) The impacts of climate change on agricultural production systems in China. Clim Change 120(1–2):313–324. https://doi.org/10.1007/s10584-013-0803-7
Littell RC, Milliken GA, Stroup WW et al (2006) SAS system for mixed models, 2nd edn. SAS Inst, Cary, NC
Liu Y, Ge T, Wang P et al (2023) Residence time of carbon in paddy soils. J Clean Prod 400:136707. https://doi.org/10.1016/j.jclepro.2023.136707
Liu Z, Tao L, Liu T et al (2018) Nitrogen Application after Low-Temperature Exposure Alleviates Tiller Decrease in Rice. Environ Exp Bot 158:205–214. https://doi.org/10.1016/j.envexpbot.2018.11.001
Lu B, Yuan Y, Zhang C et al (2005) Modulation of key enzymes involved in ammonium assimilation and carbon metabolism by low-temperature in rice (Oryza sativa L.) root. Plant Sci 169:295–302. https://doi.org/10.1016/j.plantsci.2004.09.031
Lü GH, Wu YF, Bai WB et al (2013) Influence of high temperature stress on net photosynthesis, dry matter partitioning and rice grain yield at flowering and grain filling Stages. J Integr Agr 12:603–609. https://doi.org/10.1016/S2095-3119(13)60278-6
National Bureau of Statistics of China (NBSC) (2023) China Statistics Yearbook. China Statistics, Beijing
Pachauri RK, Meyer L, Plattner GK et al (2014) IPCC, 2014: Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Geneva. IPCC, Switzerland
Palmer T (2014) Record-breaking winters and global climate change. Science 344(6186):803–804. https://doi.org/10.1126/science.1255147
Ren H, Jing P, Chen Y et al (2017) Effects of low-temperature at booting stage on growth and yield formation of rice. Chin Rice 23(04):56–62 (In Chinese with English abstract). https://doi.org/10.16819/j.1001-7216.2022.210602
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48(1):7–20. https://doi.org/10.1023/A:1006247623877
Shimono H, Fujimura S, Nishimura T et al (2012) Nitrogen uptake by rice (Oryza sativa L.) exposed to low water temperatures at different growth stages. J Agron Crop Sci 198:145–151. https://doi.org/10.1111/j.1439-037X.2011.00503.x
Shimono H, Okada M, Kanda E et al (2007) Low-temperature-induced sterility in rice: Evidence for the effects of temperature before panicle initiation. Field Crop Res 101(2):221–231. https://doi.org/10.1016/j.fcr.2006.11.010
Siddik MA, Zhang J, Chen J et al (2019) Responses of indica rice yield and quality to extreme high and low-temperatures during the reproductive period. Eur J Agron 106:30–38. https://doi.org/10.1016/j.eja.2019.03.004
Sperotto RA, Cruz R, Cargnelutti D et al (2013) Avoiding damage and achieving cold tolerance in rice plants. Food Energy Secur 2:96–119. https://doi.org/10.1002/fes3.25
Susanti Z, Snell P, Fukai S et al (2019) Importance of anther dehiscence for low-temperature tolerance in rice at the young microspore and flowering stages. Crop Pasture Sci 70(2):113–120. https://doi.org/10.1071/CP18212
Tang S, Cheng W, Hu R et al (2021) Five-year soil warming changes soil C and N dynamics in a single rice paddy field in Japan. Sci Total Environ 756:143845. https://doi.org/10.1016/j.scitotenv.2020.143845
Tang S, Yuan P, Tawaraya K et al (2022) Winter nocturnal warming affects the freeze-thaw frequency, soil aggregate distribution, and the contents and decomposability of C and N in paddy fields. Sci Total Environ 802:149870. https://doi.org/10.1016/j.scitotenv.2021.149870
Tao F, Zhang S, Zhang Z (2013) Changes in rice disasters across China in recent decades and the meteorological and agronomic causes. Reg Environ Change 13(4):743–759. https://doi.org/10.1007/s10113-012-0357-7
Uchida Y, Hunt JE, Barbour MM et al (2010) Soil properties and presence of plants affect the temperature sensitivity of carbon dioxide production by soils. Plant Soil 337(1/2):375–387. https://doi.org/10.1007/s11104-010-0533-9
Wang P, Hu T, Kong F et al (2019) Rice exposure to cold stress in China: how has its spatial pattern changed under climate change? Eur J Agron 103:73–79. https://doi.org/10.1016/j.eja.2018.11.004
Werth M, Kuzyakov Y (2010) ¹³C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42(9):1372–1384. https://doi.org/10.1016/j.soilbio.2010.04.009
Xie Y, Shen Q, Li F et al (2023) Temperature response of plants and heat tolerance in Rice: A review. Adv Agron 179:135–203. https://doi.org/10.1016/bs.agron.2023.01.003
Yuan M, Cai C, Wang CZ et al (2021) Warm air temperatures increase photosynthetic acclimation to elevated CO₂ concentrations in rice under field conditions. Field Crop Res 262:108036. https://doi.org/10.1016/j.fcr.2020.108036
Zang H, Xiao M, Wang Y et al (2019) Allocation of assimilated carbon in paddies depending on rice age, chase period and N fertilization: Experiment with ¹³CO₂ labelling and literature synthesis. Plant Soil 445:113–123. https://doi.org/10.1007/s11104-019-03995-1
Zeng Y, Zhang Y, Xiang J et al (2017) Effects of low-temperature stress on spikelet-related parameters during anthesis in indica–japonica hybrid rice. Front Plant Sci 8:1–11. https://doi.org/10.3389/fpls.2017.01350
Zhang Z, Chen Y, Wang C et al (2017) Future extreme temperature and its impact on rice yield in China. Int J Climatol 37(14):4814–4827. https://doi.org/10.1002/joc.5125
Zhao L, Li M, Zheng D et al (2015) Research Progress of Physiological Changes and Regulation of Exogenous Substance of Chilling Injury on Plant. Chin. Agr Sci Bull 31(12):217–223 (in Chinese with English abstract). https://doi.org/10.11924/j.issn.1000-6850.2014-2411
Zhu H, Wang Q, Yan P et al (2012) Effect of low-temperature at heading stage on seed setting rate of major rice cultivars in Heilongjiang Province. Chin J Agrometeorol 32(2):304–309 (In Chinese with English abstract). https://doi.org/10.3969/j.issn.1000-6362.2012.02.024

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Effects of low-temperature stress during heading stage on carbon and nitrogen allocation in paddy eco-system of northeastern China

Status:

Version 1

Abstract

Background and aims

Methods

Results

Conclusion

Figures

Introduction

Materials and methods

Experimental design

Low-temperature stress simulation

Plant and soil sampling and measurement

Statistical analysis

Results

Rice biomass

Rice yield and its component factors

N uptake

C uptake

Variation of the assimilated ¹⁵N in rice-soil system

Variation of the assimilated ¹³C in rice-soil system

Discussions

Effect of low-temperature on rice biomass and yield

Effect of low-temperature on N allocation

Effect of low-temperature on C allocation

Conclusions

Declarations

Acknowledgement

References

Status:

Version 1

Effects of low-temperature stress during heading stage on carbon and nitrogen allocation in paddy eco-system of northeastern China

Status:

Version 1

Abstract

Background and aims

Methods

Results

Conclusion

Figures

Introduction

Materials and methods

Experimental design

Low-temperature stress simulation

Plant and soil sampling and measurement

Statistical analysis

Results

Rice biomass

Rice yield and its component factors

N uptake

C uptake

Variation of the assimilated 15N in rice-soil system

Variation of the assimilated 13C in rice-soil system

Discussions

Effect of low-temperature on rice biomass and yield

Effect of low-temperature on N allocation

Effect of low-temperature on C allocation

Conclusions

Declarations

Acknowledgement

References

Status:

Version 1

Variation of the assimilated ¹⁵N in rice-soil system

Variation of the assimilated ¹³C in rice-soil system