Effects of low temperature on japonica rice quality in China: A meta-analysis

doi:10.21203/rs.3.rs-4879556/v1

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Effects of low temperature on japonica rice quality in China: A meta-analysis

https://doi.org/10.21203/rs.3.rs-4879556/v1

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To investigate the effect of low temperature on the quality of japonica rice, the literature published in the last 20 years (2005-2024) was collected and a database of japonica rice quality was established. Meta-analysis was used to quantify the effect of low temperature on the quality of japonica rice in China under different conditions at the late reproductive stage. The sensitivity of japonica rice to low temperature decreased in the following order: appearance quality > eating quality > milling quality. The effects of low temperature degree (∆T) on japonica rice quality differed. When 3°C<∆T≤6°C, the foodstuff value decreased the most (-12.57%), which strongly reduced the eating quality; when ∆T>6°C, the chalkiness (23.69%) greatly increased, the brown rice percentage (-3.46%) decreased, the milling quality and appearance quality reached their lowest values. Low temperature occurred in different development stages, with small differences in the degree of low temperatures, had variable effects on rice quality traits. Low temperature was most sensitive before and during grouting and significantly reduced the quality of japonica rice. In the single-double-cropping areas of Central China, the low temperature of 19.7°C averaged at the filling stage after delayed sowing improved the milling and appearance quality. However, low temperatures in the early single-cropping area in Northeast China, single-cropping area in North China and single-double-cropping area in Southwest China reduced the milling and appearance quality, improved the eating quality. Our findings provide important insights for the quantitative simulation and prediction of japonica rice quality under future climate change scenarios.

low temperature

meta-analysis

appearance quality of japonica rice

milling quality of japonica rice

eating quality of japonica rice

Against the backdrop of global warming, the instability of climate systems has increased, leading to increases in both the frequency and intensity of extreme cold events (Ali et al. 2020; Johnson et al. 2018). The influence range of intense cold air outbreaks or cold waves has expanded (Li et al. 2022), posing significant challenges to crop production and food security (Hertel 2016; Kummu et al. 2021; Mirón et al. 2023).

Rice is one of the main food crops in the world (especially in Asia), and 30% of the world's total rice production comes from China, the world's largest rice producer (Tang et al. 2014). The rapid growth of the global population and people's need for a better life put forward higher requirements for rice yield and quality (Kong et al. 2015; Farooq et al. 2022). Compared with indica rice, japonica rice has better taste quality and economic value and has good quality and strong taste (Balindong et al. 2018; Ding et al. 2023). Rice quality has become one of the most important factors for consumers to consider (Bao 2012). Many commonly used indicators, such as milling, appearance, and eating characteristics, are strongly correlated with rice traits and are widely used in rice quality evaluation (Concepcion et al. 2018; Zeng et al. 2019); improving rice quality in the face of adversity has become a key goal (Caffagni et al. 2013).

However, japonica rice grain quality is easily affected by climatic conditions (especially temperature and light intensity), among which temperature is the most limiting factor affecting japonica rice quality (Tu et al. 2022). Approximately 24 countries globally, particularly major rice-producing nations such as China, have experienced cold stress, which significantly affects rice quality (Zhang et al. 2017). The filling stage is the most sensitive period to the temperature response during the whole growth period of rice, and it is also the key period for the improvement of rice quality (Fahad et al., 2019). Low temperatures during the filling stage significantly reduce the quality of japonica rice (Chu et al. 2018; Zhou 2023). Some studies have shown that the booting stage—heading stage—is more sensitive to low temperature than the filling stage and is more strongly affected by low-temperature stress (Lv et al. 2021). Most studies have shown that low temperature can reduce the brown rice percentage and white rice percentage of japonica rice and reduce the processing quality of japonica rice (Xia 2016). Low temperature increases the chalkiness and chalky rice rate decreases the appearance quality of japonica rice (Duan et al. 2019). Low temperature increased the protein and amylose contents and decreased the taste (Chen et al. 2022). There are also studies indicating that moderately low temperatures can improve the appearance and processing quality of japonica rice (Cai et al. 2023). The above research results exhibit some discrepancies, primarily due to variations in japonica rice varieties and environmental conditions, as well as a lack of comprehensive evaluation of the impact of low temperatures on rice quality (Zhu et al. 2017).

Meta-analysis is a statistical method that synthesizes the results of a large number of independent experiments on the same subject (Normand 1999). Compared with a single-study or qualitative literature review, a meta-analysis can identify and evaluate batch literature, clarify the relationships between variables, reveal the main factors affecting the results, and provide a basis for scientific decision-making (Guzzo et al. 1987; Zhang 2017), which can explain the differences in the effects of low temperature on rice quality to a certain extent.

Based on this meta-analysis, this study integrates and summarizes a large number of independent experiments conducted at different times and locations to assess the impact of low temperatures on the quality of japonica rice. The relationships between low temperatures and various quality indicators of japonica rice were quantified, and the effects of low temperatures under different conditions (degree of low temperature, timing of low temperature exposure, experimental methods and locations) were investigated. The results provide a theoretical basis for scientific irrigation under low-temperature stress and post-disaster emergency measures, provide important insights for the quantitative simulation and prediction of japonica rice quality under future climate change scenarios, and provide a scientific reference for promoting domestic climate change and food security meta-analysis research.

2.1 Data collection

The PRISMA flowchart (Fig. 1) shows the procedure used to select research papers for this study (https://www.prisma-statement.org/). Through the Web of Science (https://webofscience.Clarivate.Cn/), the China database (https://www.cnki.net/), "low temperature, chilling, cold stress", "rice" and "quality" were used as the main keywords for the search.

The initial search yielded 1,870 articles (the total results of the two databases), with duplicate studies removed by comparing article titles, author lists, publication years, journal names, etc., and abstracts checked for relevance, of which 36 articles were considered relevant. The full texts of the articles were examined to determine whether the articles were suitable for meta-analysis according to the following criteria:

(1) The experimental crop was defined as japonica rice.

(2) At least two temperature treatments (low temperature and control) were included in the same study, and each experiment was repeated independently;

(3) The study included at least one quality dataset, and the corresponding mean and standard deviation (SD) were calculated directly or indirectly from the chart in the literature.

(4) The number of repetitions of each test was not less than two. When the same trial data appeared in multiple papers, they were entered into the meta-analysis only once.

(5) Studies of other crop control conditions (drought, CO₂ concentration) were excluded.

Based on the above criteria, a total of 27 studies were selected and included in the study, and a total of 1285 pairs of valid data were included.

2.2 Data Extraction

The following indices were selected for rice quality: milling quality (brown rice percentage, milled rice percentage, and head rice percentage), appearance quality (chalky rice rate, chalkiness, and length-width ratio), and eating quality (amylose content, gel consistency, foodstuff value, and protein content). The chalky rice rate is the ratio of the opaque portion of the endosperm to the total number of grains, while the chalkiness refers to the percentage of chalky area to the estimated grain area (He et al. 2023).

When conducting meta-analyses on continuous data, the sample size, average and standard deviation need to be considered (Chen et al. 2019). Other information, such as the experimental location, variety name, type of low-temperature treatment and type of experiment, was also extracted for further analysis. During literature data extraction, some data may not be able to be extracted directly. Instead, the GetData Graph Digitizer (http://www.getdata-graph-digitizer.com/) can be used to indirectly extract literature image information to improve the data.

The phenomenon of missing standard deviation exists in variables in the dataset used in this paper. For this reason, in the dataset of each variable, the standard deviation of missing variables is calculated according to the following methods: (1) if the coefficient of variation is known, the standard deviation of the missing variable is calculated by multiplying the known mean coefficient of variation of the variable by the arithmetic mean of each missing variable (van Groenigen et al. 2017; Liao et al. 2021); (2) if the standard deviation is calculated according to the intergroup significance or 95% confidence interval, the specific calculation method is referred to (Liu et al. 2017).

2.3 Meta-analysis

The meta-analysis included two primary steps: (1) calculating the individual effect sizes and their variance in each study to place the data from the primary studies on a common scale and (2) assessing the cumulative effect size.

In the present study, the natural log-transformed response ratio (lnR) was used as the effect value to calculate the individual effects of rice traits. The formula for calculating the effect value and its variance is as follows:

$$\:lnR=ln\frac{{X}_{e}}{{X}_{c}}={ln}\left({X}_{e}\right)-ln\left({X}_{c}\right)$$

$$\:{V}_{\text{l}\text{n}\text{R}}=\frac{{{(SD}_{c})}^{2}}{{N}_{c}{X}_{c}}+\frac{({{SD}_{e})}^{2}}{{N}_{e}{X}_{e}}$$

SD_c and SD_e are the standard deviations in the control and low temperature treatments, respectively; N_c and N_e are the sample sizes in the control and low-temperature treatments, respectively; and X_e and X_c are the mean values of all comparisons in the control and low temperature treatments, respectively.

To quantify the comprehensive effect of the above independent experiments and calculate the cumulative effect of low temperature treatment, random effects model analysis was used to calculate the weighted average response ratio (lnRR).

$$\:\text{l}\text{n}\text{R}\text{R}=\raisebox{1ex}{$\sum\:_{\text{i}=1}^{\text{k}}{\omega\:}_{i}{\text{R}}_{\text{i}}$}\!\left/\:\!\raisebox{-1ex}{$\sum\:_{\text{i}=1}^{\text{k}}{\omega\:}_{i}$}\right.$$

$$\:{\omega\:}_{i}=1/{V}_{i}$$

where V_i is the variance of the independent individual and $\:{\omega\:}_{i}$ is the weight of each study.

Due to the asymmetry of the positive and negative effects of lnR, estimating the response effect as the percentage change relative to the control (%) can more directly explain the results of the meta-analysis.

$$\:D=\frac{{(X}_{e}-{X}_{c})}{{X}_{c}}\times\:100\text{\%}=({e}^{lnR}-1)\times\:100\text{\%}$$

The heterogeneity test was used to analyze the differences among the included studies. The total heterogeneity was composed of intergroup heterogeneity (Q_b) and intragroup heterogeneity (Q_w):

$$\:{Q}_{b}=\sum\:_{j=1}^{m}\sum\:_{i=1}^{{k}_{j}}{{\omega\:}}_{ij}{(lnR{R}_{j}-lnRR)}^{2}$$

$$\:{Q}_{w}=\sum\:_{j=1}^{m}\sum\:_{i=1}^{{k}_{j}}{{\omega\:}}_{ij}{(ln{R}_{ij}-lnR{R}_{j})}^{2}$$

where m is the number of groups, k_j is the number of studies in the j^th group, w_ij is the weight for the i^th study in the j^th group, lnRR_j is the cumulative effect size for the j^th group and lnR_ij is the effect size for the ij study in the j^th group.

2.4 Classification standard

(1) Low temperature degree: In this study, the temperature deviation between the low temperature group and the control group was used to characterize the degree of low temperature (∆T).

∆T = X_c-X_e (8)

(2) Experimental type: According to the different methods of low-temperature treatment, the data were divided into two categories: artificial climate box (climate box) and delayed seeding.

(3) Low-temperature period: According to the rice growth period when low temperature occurs, the data can be divided into heading, early filling, middle filling, late filling and whole filling periods.

(4) Experimental sites: According to the rice planting division, China's rice region is divided into six rice farming regions, four of which are involved in this study: the early single-cropping rice region in Northeast China (Northeast China), the single-cropping rice region in North China (North China), the single-double-cropping rice region in Central China (Central China) and the single-double-cropping rice region in Southwest China (Southwest China).

Table 1

The temperature range and means of the different classification standard included in the meta-analysis.
Classification		No.	LT range (°C)	LT mean (°C)	CK range (°C)	CK mean (°C)	∆T range (°C)	∆T mean (°C)
∆T	∆T ≤ 3	500	17.5–22.7	20.4	20.0-24.7	22.2	0.2-3	1.8
	3<∆T ≤ 6	585	16.0-21.3	18.3	19.7–26.0	22.9	3.1-6.0	4.6
	∆T > 6	420	14.0–19.0	17.0	22.2–27.0	27	6.2–11.0	7.3
Experiment type	climate box	664	14.0–21.0	17.3	19.7–26.0	23.4	2.5–11.0	6.2
Experiment type	delayed seeding	841	17.1–22.7	19.7	21.1–27.0	22.8	0.2-8.0	3.1
LT periods	Heading	171	15.0–19.0	17.4	19.7–26.0	23.9	3.0–11.0	6.5
	Early filling	169	15.0–21.0	17.6	20.0–26.0	23.7	2.5-8.0	6.2
	Middle filling	143	15.0-18.8	17.3	20.5–25.0	23.5	2.6-8.0	6.2
	Late filling	83	14.0-17.5	16.1	20.6–25.0	23.3	3.6–11.0	7.2
	Whole filling	887	17.1–22.7	19.6	21.0–27.0	22.7	0.2-8.0	3.1
Experimental sites	Northeast China	351	15.0–20.0	17.0	19.7–26.0	23.2	2.6–11.0	6.3
	North China	80	19.8–21.4	20.6	21.1–21.7	21.4	0.2–1.4	0.8
	Central China	984	14.0-22.7	19.1	20.0–27.0	23.1	1.0–11.0	4.0
	Southwest China	90	17.0–19.0	17.9	23.0-24.7	23.8	5.7-6.0	5.9

No., number of data points included in the meta-analysis; CK, control check; LT, low temperature; ∆T, CK-LT.

3.1 General effect of low temperature on rice quality

A total of 1285 valid data points were included in this paper. When the average temperature of the rice during the heading and filling periods decreased from 23.1°C to 18.6°C, the appearance quality and eating quality significantly decreased but had little impact on the milling quality (Fig. 2).

Table 2

The temperature range and means included in the meta-analysis.
Meta-analysis	No.	LT range (°C)	LT mean (°C)	CK range (°C)	CK mean (°C)	∆T range (°C)	∆T mean (°C)
Total data	1505	14.0-22.7	18.6	19.7–27.0	23.1	0.2–11.0	4.4

No., number of data points included in the meta-analysis; CK, control check; LT, low temperature; ∆T, CK-LT.

Low temperature significantly decreased the chalky rice rate (-15.15%, 95% CI of -19.56% to -10.53%), chalkiness (-20.03%, 95% CI of -27.67% to -11.58%) and length-width ratio (-4.64%, 95% CI of -6.91% to -2.32%). The results showed that low temperature could promote the quality of japonica rice. Low temperature significantly increased the amylose content (2.50%, 95% CI of 0.98–4.04%) and protein content (2.23%, 95% CI of 0.50–3.99%) of japonica rice and significantly decreased the gel consistency (-13.72%, 95% CI of -17.53% to -9.73%) and foodstuff value (-9.72%, 95% CI of -11.75% to -7.82%), and the eating quality of japonica rice decreased. Analysis of japonica rice milling quality revealed that low temperature significantly decreased the percentage of brown rice (-1.97%, 95% CI of -2.65% to -1.28%), but low temperature had no significant effect on the percentage of milled rice or head rice. In summary, the effects of low temperature on japonica rice quality were as follows: appearance quality > eating quality > milling quality.

3.2 Heterogeneity analysis

Between-group heterogeneity (Q_b) rather than within-group heterogeneity (Q_w) may be of considerable scientific value, as Q_b can determine whether there are differences between groups. A comparison against the critical value of the χ² distribution tested the significance of Q_b (Gurevitch and Hedges 1999). If Q_b was significant (P < 0.05), there was a difference in the cumulative effect size between the different groups, and the difference was considered statistically significant (Fonturbel et al. 2015; Koricheva and Gurevitch 2014).

The between-group heterogeneity analysis of the effects of low temperature on different categorical variables is shown in Table 3. Among them, the length-width ratio cannot be grouped in the classification of experimental types due to insufficient data. In the classification of low temperature, there were no significant differences among the milled rice percentage, head rice percentage, gel consistency or protein content. In terms of the experimental type, experimental location and low-temperature period, there were no significant differences between the low-temperature groups in terms of gel consistency and foodstuff value (P > 0.05); therefore, the above indices were not included in the subgroup analysis.

Table 3

Between-group heterogeneity (Q_b) for low-temperature effect size across different categorical variables.
Variable	No.	LT degree	Experiment type	LT periods	Experiment sites
Brown rice	124	7.57*	45.27**	39.81**	31.18**
Milled rice	156	3.74	34.89**	24.98**	33.13**
Head rice	173	1.50	16.94**	14.08**	15.44**
Chalky rice	165	54.14**	125.64**	151.19**	157.41**
Chalkiness	163	15.21**	46.65**	56.77**	62.85**
Length-width ratio	27	38.44**	NA	95.77**	36.88**
Amylose	177	9.98**	37.84**	67.89**	75.99**
Gel	60	1.79	2.08	2.95	0.01
Foodstuff value	77	14.59**	0.14	2.89	1.06
Protein	163	3.07	6.49*	38.18**	11.49**

The experiment types included artificial climate boxes and delayed seeding; the LT periods included heading, early filling, middle filling, late filling and whole filling; and the experiment sites included Northeast China, North China, Central China and Southwest China. No., the number of data points. * P < 0.05; ** P < 0.01; NA, no data available.

3.3 Effect of different low temperatures on the quality of japonica rice

The effects of different low-temperature treatments (∆T) on the quality of japonica rice differed. The percentage of brown rice in japonica rice decreased with increasing ∆T; When ∆T > 6℃, the percentage of brown rice decreased the most (-3.46%, with a 95% CI of -4.74% to -2.16%), and the milling quality was the lowest.

Low temperature has different effects on appearance quality, even completely opposite effects. With increasing ∆T, the chalky rice rate and chalkiness decreased first and the length-width ratio increased by 3.13%, which improved the appearance quality; When ∆T increases above 6℃, the chalky rice rate (23.69%) and chalkiness (13.99%) significantly increased, the length-width ratio significantly decreased (-6.78%, 95% CI of -8.63% to -4.89%) with increasing ∆T, which decreased the japonica rice appearance quality.

With increasing ∆T, the amylose content and foodstuff value first increased and then decreased (Fig. 3e). When 3℃<∆T ≤ 6℃, the amylose content increased significantly (5.63%, 95% CI of -3.08–8.25%), the foodstuff value decreased the most (-12.57%), and the eating quality decreased the least.

3.4 Effect of low temperature on the quality of japonica rice under different experimental conditions

The response of japonica grain quality to low temperature was affected by experiment type (Fig. 4). Analysis of the milling quality of japonica rice revealed that under the sowing stage with a relatively low temperature (3.1°C), the milled rice percentage (1.86%, 95% CI of 0.43–3.31%) and the head rice percentage (8.45%, 95% CI of 3.39–13.76%) significantly increased. However, under the artificial climate box treatment with a relatively high low temperature (6.2°C), the percentage of brown rice (-4.82%, 95% CI of -5.87% to -3.76%), milled rice (-4.67%, 95% CI of -6.32% to -3.01%), and head rice (-6.53%, 95% CI of -11.40% to -1.38%) significantly decreased (Fig. 4a).

The differences in the results caused by the different experimental methods were also reflected in the quality of the japonica rice. The low temperature in the artificial climate box treatment increased chalkiness (22.23%, 95% CI of 7.93–50.67%), and the chalky rice rate (22.23%, 95% CI of 12.51–32.76%) decreased the appearance quality. However, low temperature significantly reduced the chalkiness (-35.90%, 95% CI of -42.73% to -28.27%) and chalky rice rate (-27.92%, 95% CI of -31.85% to -23.78%) of japonica rice during the sowing stage, and the appearance quality improved (Fig. 4b).

Compared with the other qualities, the response of japonica rice taste to low temperature under different experimental methods was very small, and there was no significant difference in the response of gel consistency (Q_b=2.08, P = 0.15) or foodstuff value (Q_b=0.14, P = 0.71) to low temperature. Under the stage seeding method, low temperature significantly increased the amylose content (7.26%, 95% CI of 5.10–9.46%) and protein content (5.07%, 95% CI of 3.42–6.60%) and decreased the eating quality (Fig. 4c), but there was no significant difference under the artificial climate chamber treatment.

In summary, the milling quality and appearance quality of japonica rice decreased under the low-temperature treatment, with an average temperature of 17.3°C in the artificial climate box, while the low temperature, with an average temperature of 19.7°C in the filling stage after delayed sowing, was conducive to improving the milling quality and appearance quality of japonica rice and reducing its eating quality.

The temperature at the filling stage was controlled by delaying the sowing time in the stage seeding treatment. When the average temperature of the filling stage was 19.7°C, the milling quality and appearance quality of japonica rice could be improved by increasing the percentage of head rice (8.45%) and decreasing the chalkiness (-35.90%) at low temperature.

To determine the suitable sowing date for japonica rice, the effects of different sowing dates on the milling quality and appearance quality of japonica rice were further analyzed. With the delay of sowing, the milled rice percentage and head rice percentage in Jiangsu Province and Henan Province both first increased and then decreased. In Jiangsu Province and Henan Province, the milling quality of japonica rice reached a maximum when the average temperature was 20.3°C on June 4 and 19.4°C on June 9.

The lower the chalkiness and chalky rice rate were, the better the appearance quality of japonica rice. In Jiangsu Province, the chalkiness and chalky rice rate changed the most when the average temperature was 20.2°C on May 31, at -38.10% and − 39.97%, respectively. The minimum chalkiness and chalky rice rate occurred on June 24 in Henan Province, and the average temperature at the filling stage was 18.2°C.

Therefore, when the sowing period of Jiangsu Province was from May 31 to June 4 and the sowing period of Henan Province was from June 9 to June 24, the average temperatures during the filling period were 20.2°C and 18.8°C, respectively, and the milling quality and appearance quality of japonica rice were the best. In practical applications, the sowing date should be appropriately advanced according to the market demand for japonica rice.

3.5 Effects of low temperature on rice quality at different developmental stages

The data were divided into the heading stage, early filling stage, middle filling stage, late filling stage and whole filling stage according to the growth stage of the rice plants at which low temperatures occurred. The mean temperature at low temperatures differed little among the different periods (Table 1), but the effect on the quality of japonica rice significantly differed (Fig. 6).

Analysis of japonica rice milling quality revealed that low temperature at the heading stage significantly decreased the percentage of brown rice (-3.71%, 95% CI of -5.87% to -1.49%). Low temperatures during the early and middle filling periods significantly reduced the percentage of brown rice and milled rice. Low temperature at the later stage of grouting had little effect on the milling quality, and there was no significant difference in the brown rice percentage, milled rice percentage or head rice percentage. However, low temperature throughout the whole filling stage significantly increased the rice milling rate of japonica rice (1.85%, 95% CI of 0.40–3.31%) (Fig. 6a).

The low temperature in the middle filling period had the greatest effect on the appearance of japonica rice, which significantly reduced the length-width ratio (-15.84%, 95% CI of -20.23% to -11.19%) and significantly increased the chalky rice rate and chalkiness, among which the chalkiness increased by 84.43%. The appearance quality of japonica rice decreased in response to low temperature in the early filling period, and its effect was slightly weaker than that in the middle filling period.

Low temperature at the heading stage significantly increased the chalky rice rate (18.70%, 95% CI of 0.26–40.52%) and length-width ratio (3.32%, 95% CI of 0.15–6.61%) but had no significant effect on chalkiness. Low temperature had little effect on the appearance of japonica rice during the late filling period, and the chalky rice rate and chalkiness did not significantly differ. Low temperature throughout the filling stage significantly reduced the chalky rice rate and chalkiness and improved the appearance of japonica rice.

In terms of eating quality, low temperature in the early filling period significantly increased the japonica rice protein content (7.40%, 95% CI of 2.95–12.04%), but there was no significant difference in the amylose content. Low temperature at the heading stage and filling stage significantly reduced the amylose content (-5.88%, -4.29%) but had no significant effect on the protein content. The effect of low temperature in the late filling stage on eating quality was not significant. Low temperature during the whole filling stage significantly increased the amylose content (7.25%, 95% CI of 5.13–9.43%) and protein content (5.09%, 95% CI of 2.64–7.57%) and decreased the eating quality of japonica rice.

3.6 Effects of low temperature on rice quality at different experimental sites

The low-temperature strength is different at different test sites. The low-temperature intensity (∆T) of early-maturing single-cropping rice in Northeast China and single- and double-cropping rice on the Southwest Plateau was relatively high (6.3°C and 5.9°C, respectively), and the average low temperature was only 17.0°C and 17.9°C, respectively. The average low temperatures of single-cropping rice in North China and single-double-cropping rice in Central China were 20.6°C and 19.1°C, respectively, and the low-temperature intensities (∆T) were 0.8°C and 4.0°C, respectively.

The response of japonica rice quality to low temperature varied among the experimental sites. The japonica rice growing in the early single cropping area of Northeast China was the most sensitive to low temperature, and the lowest temperature intensity was the most sensitive. Low temperature significantly decreased the percentage of brown rice (-4.85%) and milled rice (-5.68%), and the milling quality of japonica rice decreased. The chalky rice rate and chalkiness increased significantly by 116.24% and 140.44%, respectively, which strongly affected the appearance quality. Low temperature reduced the amylose content and protein content of rice grains by 3.21% and 1.19%, respectively, which slightly improved the eating quality of japonica rice. The response of japonica rice to low temperature was similar to that of early-maturing single-crop rice in Northeast China; low temperature reduced milling quality and slightly increased eating quality. Although the low-temperature intensity of single- and double-cropping rice on the southwestern Plateau was similar to that in the Northeast Region, low temperature had the least effect on japonica rice quality in this cropping area (Fig. 7), affecting only the brown rice percentage of japonica rice (-5.65%, with a 95% CI of -9.26% to -1.90%), and had no significant effect on the effect of low temperature on the other quality traits of japonica rice.

Compared with those in the other three rice farming areas, the effects of low temperature on the quality traits of single- and double-cropping rice in Central China differed to some extent: low temperature significantly increased the percentage of head rice (7.35%, 95% CI of 2.43–12.50%) and significantly decreased the percentage of chalky rice (-26.29%, 95% CI of -30.40% to -21.96%) and chalkiness (-32.83%, 95% CI of -39.80% to -25.05%) and improved the milling quality and appearance of japonica rice; low temperature significantly increased the amylose content (8.61%, 95% CI of 6.55–10.72%) and protein content (3.92%, 95% CI of 1.38–6.50%) and decreased the eating quality of japonica rice.

4.1 Discussion

Rice quality is a comprehensive characteristic, and there are different evaluation indices for different uses, which are generally measured from three aspects: milling quality, appearance quality and eating quality. Rice quality is an important commodity attribute of rice and is jointly affected by variety, ecological environment, planting location and cultivation system (Liu et al. 2021; Cai et al. 2022). Consumers mainly evaluate rice quality through grain size, milled rice percentage, chalkiness, etc. (Moulick et al. 2020).

As rice is a tropical and subtropical plant, the optimal temperature of rice in most rice-producing areas is 22–28°C (Siddik et al. 2019). When the temperature was lower than the optimal temperature, the photosynthetic rate, stomatal conductance and transpiration rate of japonica rice decreased, the accumulation of photosynthetic products in panicles decreased, and the rice quality decreased (Rehmani et al. 2014).

Low temperatures significantly affect the appearance of rice (Fig. 2), primarily by reducing the chalkiness (-20.03%) and chalky rice rate (-15.15%) of japonica rice (Zeng et al. 2017; Cong et al. 2022). However, studies by Yang et al. (2023) and Zhang et al. (2019) suggest that low temperatures can enhance chalkiness and the chalky rice rate. The fundamental reason for the differences in the above conclusions lies in the varying degrees of low temperature among studies. Our research indicated that when ∆T ≤ 6°C, low temperatures significantly decreased the chalky rice rate and chalkiness of japonica rice while increasing the grain length-to-width ratio by 3.13%, thereby enhancing the appearance quality of japonica rice. In contrast, when ∆T > 6°C, low temperatures substantially increased the chalky rice rate (23.69%) and chalkiness percentage (13.99%) while significantly decreasing the grain length-width ratio (-6.78%), resulting in a decrease in the appearance of japonica rice (Fig. 3). Zhou et al. (2021) suggested that with decreasing temperature, the chalky rice rate and chalkiness of late-maturing japonica rice initially decrease and then increase; this finding is consistent with our study. During the grain filling stage, low-temperature stress can induce uneven grain filling, impairing storage biosynthesis and leading to chalk formation. Grains with high chalkiness become more brittle due to gaps caused by the failure of starch particle formation (Sreenivasulu et al. 2015). This brittleness makes the grains more susceptible to breakage during processing, thereby increasing the number of broken grains. Therefore, high chalkiness in japonica rice is often associated with the percentage of brown rice.

Studies on the general impact of low temperature on the quality of japonica rice grains indicate that low temperature decreases the milled rice percentage while increasing the head rice percentage, but these effects are not statistically significant (Fig. 2). In fact, the japonica brown rice percentage decreased significantly with increasing ∆T. When ∆T > 6°C, the percentage of brown rice was the lowest (-3.46%, with a 95% CI of -4.74% to -2.16%), and the milling quality of japonica rice was the worst (Fig. 3).

Moreover, significant differences in the impact of low temperature on the milling quality of japonica rice were observed under different experimental conditions. In the staggered planting method, a delay in sowing led to a decrease in temperature at the filling stage and a difference in grain quality (Tu et al. 2020). Under this processing method, the low temperature during the filling stage is improved mainly by increasing the percentage of head rice (8.45%) and reducing chalkiness (-35.90%), thereby enhancing the milling quality and appearance of japonica rice (Fig. 4a, b). Specifically, Jiangsu Province was sown from May 31 to June 4, and the average temperature at the filling stage was 20.2°C. Henan Province was sown from June 9 to June 24, and the average temperature at the filling stage was 18.8°C. The milling quality and appearance quality of japonica rice were the best (Fig. 5). A delayed sowing date improved japonica rice milling quality, probably due to the gradual decrease in the number of days and average daily temperature that were affected by high temperature (Yao et al. 2015), but a late sowing date resulted in decreased grain maturity and reduced japonica rice appearance quality (Zhao et al. 2019). Low-temperature treatment in the artificial climate box significantly reduced the brown rice percentage (-4.82%), milled rice percentage (-4.67%), and head rice percentage (-6.53%) of japonica rice, while increasing the chalkiness (22.23%) and chalky rice rate (22.23%) significantly decreased its milling quality and appearance quality. In this study, the degradation of japonica rice quality under low-temperature treatment in an artificial climate box was more serious than that under delayed sowing. Interestingly, delaying seeding to the filling stage under low temperatures could even enhance rice milling quality (Fig. 4a) and appearance quality (Fig. 4b). This is primarily because, in contrast to the artificial climate box treatment, the low temperature under the delayed sowing method was lower. Methodologically, creating significant temperature gradients under field conditions is much more challenging than under artificial climate box conditions, and very few field studies have reached extremely low temperatures; in our study, the average temperature during the filling stage under delayed seeding was 19.7°C, indicating relatively mild low-temperature conditions. In addition, other outdoor environmental factors are difficult to control, and the interaction between low temperature and other environmental factors may be the cause of this difference; more field studies are still needed to confirm the temperature effect (Matsui et al. 2014).

The effects of low temperature on the quality of japonica rice vary among different development stages (Siddik et al. 2019). Low temperatures at the heading stage, early filling stage and middle filling stage reduced the milling quality and appearance quality of japonica rice. There was no significant difference in the degree of low temperature in the above growing stages (Table 1), but the influence on the quality of japonica rice was different: middle filling stage > early filling stage > heading stage. This indicated that japonica rice was most sensitive to low temperature in the early and middle filling stages. The influence of temperature on eating quality at the filling stage mainly occurred in the early filling stage, which was consistent with previous studies (Cheng and Zhu 1998). Low temperature in the early filling period significantly increased the amylose content (3.94%) and protein content (7.30%) in japonica rice, which was likely attributable to increased expression of GBSS granule-bound starch synthase (GBSS) at low temperature (Ahmed et al. 2015; Kato et al. 2019) and decreased japonica rice taste quality.

The temperature decrease in the late filling period was the greatest, but it had no significant effect on japonica rice quality, especially on the chalky rice rate and chalkiness. The reason may be that the chalkiness of japonica rice grains was mainly concentrated 5–30 days after heading, and the other periods had little effect on japonica rice appearance quality (Yang 2002).

The response of japonica rice quality to low temperature significantly differed with changes in the experimental site (Fig. 7). Among them, the single-double cropping area of central China has a subtropical warm and humid monsoon climate, while the early-maturing single-cropping area of Northeast China has a cold temperate zone-warm temperate zone and humid-semiarid monsoon climate. The average daily temperature and average daily radiation of early-maturing single-cropping rice in Northeast China were 37% and 15% lower than those of single-cropping and double-cropping rice in Central China, respectively (Matsui et al. 2014). This rice farming area was the most sensitive to low temperature and prone to low temperature cold damage. Low temperature hindered rice filling (Zhang et al. 2019), significantly increased the chalky rice rate and chalkiness, both of which were greater than 110%, and seriously reduced the appearance quality of japonica rice (Fig. 7b).

Low temperature also decreased the milled rice percentage (-5.68%) and amylose content (-3.21%), thus reducing the milling quality of japonica rice (Siddik et al. 2019). However, the relatively high temperature at the filling stage of single- and double-cropping rice in central China can enhance grain nitrogen metabolism and increase the enzyme activities of glutamine synthetase and glutamate synthetase, thus accelerating the conversion of amino acids to proteins (Shao et al. 2021), increasing the protein content (5.10%), increasing the hardness of rice, decreasing the viscosity (Amagliani et al. 2017), and decreasing the eating quality (Fig. 7c).

The reason for the above differences may be the differences among japonica rice varieties in different rice-growing areas (Yang et al. 2023). Under the same experimental conditions, compared with nonsoft rice and japonica rice, soft rice and japonica rice had lower hardness and amylose content, higher chalky rice rate and chalkiness, higher taste quality and poor appearance quality (Ma et al. 2022). The varieties of japonica rice used in different studies differed, and the response to low temperature also had a certain effect. For example, there was a large difference between cold-sensitive and cold-tolerant japonica rice varieties in response to low temperature. The contents of malondialdehyde (MDA), soluble sugars and proline increased significantly after low-temperature stress, and the increase rate of cold-sensitive rice varieties was greater than that of cold-tolerant rice varieties, while the above indices decreased slightly after cold-sensitive rice varieties resumed growth. The plants were unable to recover to the pre-low temperature treatment level (Guo et al. 2019).

Due to data limitations, this study omitted the different responses of different japonica rice varieties to low-temperature treatment. In the near future, we could conduct field experiments with cold resistant varieties, shifting sowing date agronomic technologies to mitigate the adverse effects of low temperature.

4.2 Conclusion

According to the total effect of low temperature on japonica rice grain quality, the degree of sensitivity of japonica rice quality to low temperature decreased in the following order: appearance quality > eating quality > milling quality. The effects of low temperature on rice quality differed at different growth stages, and low temperature had the greatest effect on early and middle grout filling. Low temperatures during this period seriously reduce the milling quality, appearance quality and eating quality of japonica rice.

The effects of low temperature on japonica rice quality differed. With increasing ∆T, the brown rice percentage and foodstuff value decreased significantly, and the amylose content increased, which decreased the milling quality and eating quality of japonica rice. The chalky rice rate and chalkiness decreased first but then increased significantly with increasing low temperature degree. When 3°C<∆T ≤ 6°C, the amylose content (5.63%) and foodstuff value (-12.57%) change the most, and the eating quality is the lowest. When ∆T > 6°C, the brown rice percentage is the lowest, the chalky rice rate increases significantly, which reduce the milling quality and appearance quality.

The effects of low temperature on japonica rice growth were as follows: Northeast China early single-cropping area > North China single-cropping area > Central China single- and double-cropping area > Southwest China Plateau single- and double-cropping area. In Northeast China, North and Southwest China, low temperatures decreased the milling quality and appearance quality of japonica rice and improved the eating quality. An average temperature of 19.7°C during the filling period after delayed sowing in the Central China rice farming area was beneficial for improving the milling quality and appearance quality of japonica rice and reducing its eating quality. Jiangsu Province was sown from May 31 to June 4, and the average temperature at the filling stage was 20.2°C; Henan Province was sown from June 9 to June 24, and the average temperature at the filling stage was 18.8°C, the milling quality and appearance quality of japonica rice were the best.

Author contributions

All authors contributed to the study conception and design. Qianyu Wang: Visualization, Methodology, Writing- Original draft; Ruipeng Ji: Conceptualization, Funding acquisition, Writing- Review and Editing; Jinwen Wu, Rui Feng, Siwen Zhao: Data curation; Mingjie Xu and Tao Zhang: Writing- Review and Editing.

Statements and Declarations

We have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding

This research was funded by the Basic Research Plan of Liaoning Province [Grant numbers 2023JH2/101300090, 2022JH2/101300193]; the Science and Technology Research Project of Liaoning Meteorological Bureau Research [Grant number ZD202405]; the Scientific Research Project assignment of the Central Level Public Welfare Research Institute of Atmospheric Environment, China Meteorological Administration [Grant number 2021SYIAEZD1]; and Liaoning Province Key Laboratory of Agricultural Meteorological disaster joint opening fund [grant number 2024SYIAEKFZD08].

Data Availability

Data will be made available on request.

Acknowledgments

We are grateful to the authors and organizations who contributed to the data used in this study.

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Effects of low temperature on japonica rice quality in China: A meta-analysis

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