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Article

Biochar Regulates 2-Acetyl-1-Pyrroline, Grain Yield and Quality in Fragrant Rice Cropping Systems in Southern China

by
Xuechan Zhang
1,2,3,
Xinfeng Qiu
1,2,3,
Xiangbin Yao
1,2,3,
Jianjiao Wei
1,2,3,
Shaojie Tong
1,2,3,
Zhaowen Mo
1,2,3,
Jianying Qi
1,2,3,
Meiyang Duan
1,2,3 and
Xiangru Tang
1,2,3,*
1
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China
2
Scientific Observing and Experimental Station of Crop Cultivation in South China, Ministry of Agriculture and Rural Affairs, Guangzhou 510642, China
3
Guangzhou Key Laboratory for Science and Technology of Fragrant Rice, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(12), 2860; https://doi.org/10.3390/agronomy13122860
Submission received: 25 October 2023 / Revised: 16 November 2023 / Accepted: 17 November 2023 / Published: 21 November 2023
Browse Figures
Versions Notes

Abstract

:
With the existing model of chemical fertilizer application faces, improving grain yield and quality is challenging. Fragrant rice is known for its distinctive aroma and flavor, but it generally produces less grain than non-fragrant rice varieties. Limited research has been conducted on the potential of biochar as a solution for increasing the grain yield of fragrant rice. In a two-year field trial conducted in 2022 and 2023, two fragrant rice cultivars, Meixiangzhan2 (MXZ2) and Xiangyaxiangzhan (XYXZ), were selected as the experimental materials. These rice cultivars were subjected to four different rates of biochar application: no biochar treatment(T1); biochar with 0.375 t ha−1 (T2); biochar with 0.75 t ha−1 (T3); and biochar with 1.50 t ha−1 (T4). The results showed that the grain yield of both cultivars increased to an extent in both 2022 and 2023 (an 8.57–33.77% increase for MXZ2; a 6.00–21.59% increase for XYXZ). Furthermore, under the T2, T3, and T4 treatments, there was an increase in the number of effective panicles, seed setting rate, 1000-grain weight, biomass accumulation, net photosynthetic rate, and intercellular CO2 concentration. However, the transpiration rate and stomatal conductance decreased. The content of 2-acetyl-1-pyrroline (2-AP) increased with an increased rate of biochar application, and the highest content was observed under the T4 treatment (153.54–178.32 µg kg−1 in 2022; 163.93–180.28 µg kg−1 in 2023). The activities of proline dehydrogenase (PDH) and 1-pyrrolin-5-carboxylic acid synthase (P5CS), as well as the contents of proline (PRO), 1-pyrrolin-5-carboxylic acid (P5C), ∆1-pyrroline, and methylglyoxal, were improved under the T2, T3, and T4 treatments compared to the T1 treatment. Moreover, under the T2, T3, and T4 treatments, the brown rice rate, milled rice rate, and head rice rate increased, while the chalkiness degree and chalk rice rate decreased. Our correlation analysis showed that grain yield was positively correlated with total biomass accumulation, the number of grains per panicle, and the seed setting rate. Additionally, the content of 2-AP showed positive correlations with PRO, P5C, ∆1-pyrroline and methylglyoxal, and the activities of PDH and P5CS. In conclusion, applying biochar at a rate of 1.5 t ha−1 can be more effective in increasing the grain yield and 2-AP content of fragrant rice.

1. Introduction

Rice (Oryza sativa L.) is a key food crop in many countries around the world, and approximately 70% of the population consume it as a staple food in China [1,2]. The rice planting area accounts for approximately 20% of the total planted area of food crops in the world, and accordingly, rice production accounts for approximately 20% of the world’s total crop production (FAOSTAT, 2019). Fragrant rice is known for its unique fragrance and good taste. With the demand for high-quality rice, the demand for fragrant rice in domestic and foreign markets is increasing. At present, the yield of fragrant rice is generally lower than that of non-fragrant rice. Therefore, the question of how to improve the yield of rice is the focus of current research.
Previous studies have shown that 2-acetyl-1-pyrroline (2-AP) is not only considered to be the main characteristic of the aroma quality of rice but also the key flavor compound that distinguishes aromatic rice from non-aromatic rice [3,4]. In one study, researchers found that 2-AP was present in all parts of fragrant rice except the root system [5]. There are two main methods of synthesizing 2-AP, one of which is proline (PRO), which is a precursor substance. The metabolite 1-pyrrole-5-carboxylic acid (P5C) is produced under the regulation of proline dehydrogenase (PDH), 1-pyrrole-5-carboxylic acid synthetase (P5CS), and ornithine aminotransferase (OAT). P5C generates Δ1-pyrroline through the regulation of P5CS and finally transforms it into 2-AP [6]. Another pathway is non-functional betaine aldehyde dehydrogenase (BADH2), which leads to the formation of Δ1-pyrroline from GABald in fragrant rice and the final synthesis of 2-AP with an acetyl group [7,8]. Previous studies revealed that the application of silicon fertilizer could increase the 2-AP content due to the improved PRO and net photosynthetic rates [9]. Du et al. [10] showed that silicon and selenium fertilizer management regulated soil, increased photosynthesis, and promoted dry matter accumulation, which is beneficial for promoting the grain yield and 2-AP content of fragrant rice. Meanwhile, the application of nitrogen fertilizer could increase the 2-AP content through an increase in the PRO content [11]. However, there has been limited research on biochar, as biochar can alter the physical and chemical properties of soil, potentially affecting the production of 2-AP.
Biochar is a material produced through the high-temperature pyrolysis of agricultural biomass waste (wood residues, crop straw, animal manure, organic waste, and so on) in a low-oxygen environment [12,13]. The long-term use of chemical fertilizers has caused a series of problems in agricultural production, including environmental pollution, soil hardening, and a decreased fertilizer efficiency and crop yield. Consequently, researchers have been exploring new materials that are highly efficient and environmentally friendly [14]. Biochar is one such novel material, known for its high stability, strong adsorption capacity, and well-developed pore structure [15]. Additionally, its physicochemical properties have positive impacts on the environment and agriculture. The application of biochar can improve soil conditions, enhance fertilizer utilization, provide mineral nutrients, and promote nutrient cycling between soil and plants [16,17]. This, in turn, facilitates plant growth and productivity [18,19]. Studies by the authors of [20] have shown that biochar optimization can improve the root morphology and physiological characteristics of rice, leading to enhanced nutrient absorption. Moreover, the application of biochar also affects the photosynthetic characteristics [21,22] and dry matter accumulation of crops [23]. Gong et al. and Yin et al. [24,25] demonstrated that biochar can improve crop quality and increase crop yield.
To date, numerous studies have been conducted on the regulation of aromatic rice fragrance and yield using chemical fertilizers and organic fertilizers. However, the effects of the application of biochar on the grain yield, quality, and 2-AP content of fragrant rice remain unclear. In this study, we conducted a two-year field experiment to investigate the effects of biochar application (0, 0.375, 0.75, 1.50 t ha−1) on the grain yield, 2-AP content, and grain quality of fragrant rice. As the application of biochar can improve the physical and chemical structure of the soil and enhance the absorption of nutrients by roots, we hypothesized that biochar fertilizer could potentially enhance the rice yield and aroma. The objective of this study was to determine whether, under the application of biochar, (I) the effect of grain yield increase was regulated by yield components, biomass accumulation, and photosynthetic characteristics; (II) the aroma-enhancing effect was regulated by the activities of PDH and P5CS and the contents of PRO, P5C, ∆1-pyrroline and methylglyoxal; (III) and the yield and yield-related properties, as well as the relationship of 2-AP to substances associated with its synthetic pathway, which we investigated through regression analyses and heatmaps.

2. Materials and Methods

2.1. Site Description

Field experiments were conducted at the Experimental Farm of the College, South China Agricultural University (113°81′ E, 23°13′ N), in the early seasons of 2022 and 2023. The experimental site has a subtropical monsoon climate. The monthly average, maximum, and minimum temperatures and the precipitation during the rice-growing period are shown in Table 1. The experimental soil type is sandy loam soil. The soil pH was 6.03; the SOC and TN were 18.13 and 1.65 g kg−1; and the alkali-hydrolyzed nitrogen, available phosphorus, and potassium were 124.03, 16.59, and 332.48 mg kg−1, respectively, before transplanting in the early season of 2022.

2.2. Experimental Materials and Design

Two fragrant rice cultivars, i.e., ‘Meixiangzhang2’ (Lemont (American variety) × Fengaozhan) and ‘Xiangyaxiangzhang’ (Xiangsimiao126 × Xiangyaruanzhan), were used in this study. Seeds of these cultivars were obtained from the Rice Research Institute of the College of Agriculture, South China Agricultural University. The biochar (N: P2O5: K2O > 5%) was provided by Dongguan Foota Biotechnology Co., Ltd. The raw materials of biochar production include activated carbon, active organic matter, seaweed extract, and viable bacteria, among which the activated carbon was made of crop straw after carbonization at 300 °C for one hour and activation at 600 °C for four hours. Field experiments were conducted using a randomized complete block design with four management treatments, i.e., T1: no biochar treatment; T2: biochar with 0.375 t ha−1; T3: biochar with 0.75 t ha−1; and T4: biochar with 1.50 t ha−1. All treatments were applied in a ratio of 60% base fertilizer and 40% tiller fertilizer. The base fertilizer was spread artificially two days before transplantation. The tiller fertilizer was applied evenly in the tilling layer, and the tillering fertilizer was applied 10 days after transplantation.
The plot area was 25.5 m2, and three replicates were performed for each treatment. Before sowing, the seeds were soaked for 12 h and then transferred to an incubator at 36 °C for 12 h. The germinated seeds were then sown in a PVC seedling tray, and after 15 days, the seedlings were transplanted into the rice field. For the 2022 field experiments, the seeds were sown on March 10, transplanted on March 28, and harvested on July 10; for the 2023 experiments, the seeds were sown on March 11, transplanted on April 1, and harvested on July 8. The Changzhou Yameike 2BD-300 (LSP-40AM) rice pot seedling seeder and matching pot seedling tray were used for seedling cultivation; the Changzhou Yameike 2ZB-6AK pot seedling ride-type high-speed transplanter was used for transplantation. The row spacing of the plants was 30 cm × 16 cm. Irrigation and pest management were carried out in accordance with the local provincial general management method.

2.3. Determination of 2-AP Content in Fragrant Rice

The 2-AP content was determined according to the methods reported in [26], with modification. Fresh grains in the maturity stage were collected and ground into powder with liquid nitrogen. Then, we weighed 2.0 g into a bottle, immediately added 10 mL of dichloromethane, and performed extraction in an ultrasonic cleaning machine at 40 °C for four hours. Next, we added an appropriate amount of anhydrous sodium sulfite to the extract to absorb the water, and then the supernatant was used to measure the 2-AP content on a gas chromatograph‒mass spectrometer (Japan GCMS QP 2010 Plus, Shimadzu Corporation, Kyoto, Japan). The 2-AP contents were expressed as µg kg−1.

2.4. Determination of Grain Yield, Yield Components, and Grain Quality

In the maturity stage, the effective panicle number of 1 m2 was counted at six different locations for each treatment, and the harvested panicle grains were dried until the water content was 12.5–14.5% for the threshing treatment, which was used to determine the grain yield, grain number per panicle, and seed setting rate. Then, 1000 fulled grains were randomly selected for each treatment to determine the 1000-grain weight. The dried grains were stored at room temperature for three months, and fulled grains were then selected. The grain quality was determined referring to [27]. The chalkiness degree and chalky rice rate were determined using a rice appearance quality analyzer (SC-E, Hangzhou Wanshen Corporation, Hangzhou, China).

2.5. Determination of Dry Matter Accumulation and Photosynthetic Characteristics

In the maximum tillering stage (MTS), booting stage (BS), full heading stage (FHS), and maturity stage (MS), six representative plants were randomly selected from each treatment group, the straw and panicles of the fragrant rice were separated in the FHS and MS, and the green was killed in an oven at 105 °C for 30 min, baked at 80 °C until dry, and finally weighed. In the heading stage, a portable photosynthetic system (LI-6800, LI-COR, New York, NY, USA) was used to determine the photosynthetic characteristics of the fragrant rice at 9:00–11:00 in sunny weather.

2.6. Determination of the Physiological Indices Related to 2-AP Accumulation in the Fragrant Rice Grains

The PRO, P5C, and Δ1-pyrroline contents, as well as the PDH and P5SC activity, were determined referring to [28]. The methylglyoxal content was estimated according to the methods reported in [29]. The PRO contents were expressed as µg g−1 FW; the PDH activities were expressed as U g−1 min−1 FW; and the P5CS activities and the P5C, Δ1-pyrroline, and methylglyoxal contents were expressed as µmol g−1 FW.

2.7. Statistical Analysis

Microsoft Excel 2010 and SPSS 26 software were used to collect and analyze the data. Graphs were drawn using Origin 2023 software. The least significant difference (LSD) test was used for multiple comparisons, with a significance level p < 0.05.

3. Results

3.1. Grain Yield and Yield Components

The application of biochar had significant effects on the grain yield and components of fragrant rice. In 2022 and 2023, the yield of two varieties of fragrant rice showed the following trend: T4 > T3 > T2 > T1. For MXZ2, compared with the T1 treatment, the T2, T3 and T4 treatments significantly increased the yield, number of effective panicles, seed setting rate, and 1000-grain weight in 2022 and 2023. In 2022 and 2023, the yield and number of effective panicles were the highest under the T4 treatment, the yield ranged from 4.62 to 6.33 t ha−1, and the seed setting rate was the highest in 2022, being 2.05% higher than that of the T1 treatment. Under the T3 treatment, the seed setting rate and 1000-grain weight were the highest in 2022, increased by 10.82% and 3.29% compared with the T1 treatment, respectively, and the grain number per panicle was the highest in 2023, increased by 12.00% compared with the T1 treatment. Similarly, for XYXZ, compared with the T1 treatment, the T2, T3 and T4 treatments significantly increased the yield, number of effective panicles, seed setting rate, and 1000-grain weight in 2022 and 2023. Under the T4 treatment, the seed setting rate was the highest in 2022, increased by 4.44% compared with the T1 treatment. The yield, number of effective panicles, and 1000-grain weight were the highest in 2022 and 2023, and the yields were 4.90 and 6.14 t ha−1, respectively. Under the T3 treatment, the seed setting rate was the highest in 2023, increased by 1.88% compared with the T1 treatment. Under the T2 treatment, the grain number per panicle was the highest in both 2022 and 2023 (Table 2).

3.2. Biomass Accumulation and Photosynthetic Characteristics

With the extension of the growth period, the application gradually increased the biomass accumulation of fragrant rice. During the tillering and booting stages, the biomass accumulation of both cultivars in 2022 and 2023 showed an increasing trend under the T2, T3, and T4 treatments compared to the T1 treatment. In the heading stage, the biomass accumulation of MXZ2 and XYXZ had a significant effect and showed an increasing trend in the stem leaf and panicle numbers under the T2, T3, and T4 treatments, compared with the T1 treatment, in 2022 and 2023. In the maturity stage, for MXZ2, both the stem leaf and panicle numbers showed an upward trend in 2022 and 2023; for XYXZ, the stem leaf and panicle numbers were highest under the T3 treatment in 2023 (Figure 1). During the heading and maturity stages, the total biomass accumulation of the two fragrant rice varieties was significantly affected by the application of biochar, and the total biomass accumulation was higher in the maturity stage than in the heading stage. In the heading stage, in 2022 and 2023, the total biomass accumulation of the two varieties showed the following trend: T4 > T3 > T2 > T1. Meanwhile, in the maturity stage, in 2022, the total biomass accumulation of the two varieties showed the following trend: T4 > T3 > T2 > T1. The total biomass accumulation of XYXZ was highest under the T3 treatment in 2023 (Figure 2). The application of biochar substantially affected the photosynthetic characteristics of fragrant rice in the heading stage. For MXZ2, compared with the T1 treatment, the T2, T3 and T4 treatments all increased the net photosynthetic rate and intercellular CO2 concentration by 6.22–29.90% and 2.18–11.20%, respectively, but decreased the transpiration rate and stomatal conductance in 2022 and 2023. The same results were also observed for XYXZ; compared with the T1 treatment, the T2, T3 and T4 treatments increased the net photosynthetic rate and intercellular CO2 concentration by 4.58–22.23% and 2.49–19.80%, respectively, and also decreased the transpiration rate and stomatal conductance (Figure 3).

3.3. 2-AP Content

The application of biochar had a significant effect on the content of 2-AP. In 2022 and 2023, the 2-AP content in the grains of MXZ2 and XYXZ in the maturity stage increased with the application of biochar. For MXZ2, the 2-AP content ranged from 96.36 to 163.93 µg kg−1. In 2022, compared to the T1, T2, and T3 treatments, the T4 treatment increased the 2-AP content by 59.34, 40.30, and 8.74%, respectively. Meanwhile, in 2023, increases of 53.09, 13.79, and 2.71% in the 2AP contents of the grains were detected following the T4 treatment compared with the T1, T2, and T3 treatments, respectively. For XYXZ, the 2-AP content ranged from 117.46 to 180.28 µg kg−1. In 2022, compared to the T1, T2, and T3 treatments, the T4 treatment increased the 2-AP content by 51.81, 36.03, and 7.69%, respectively. Meanwhile, increases of 30.60, 13.66, and 6.58% in the 2-AP contents of the grains were detected following the T4 treatment compared with the T1, T2, and T3 treatments, respectively, in 2023. Overall, the yields and 2-AP contents of MXZ2 and XYXZ showed an increasing trend with the application of biochar in 2022 and 2023 (Figure 4).

3.4. 2-AP Biosynthesis Related Physiological Indexes

The PDH and P5CS activities and the contents of PRO, P5C, ∆1-pyrroline, and methylglyoxal in the grains of both fragrant rice cultivars increased to a certain extent in the maturity stage under the T2, T3 and T4 treatments, compared with the T1 treatment. For MXZ2, the contents of P5C, methylglyoxal, PRO, and ∆1-pyrroline significantly increased following the T2, T3, and T4 treatments in 2022 and 2023, as compared with the T1 treatment, for which the contents of PRO and ∆1-pyrroline showed no significant difference in 2022. For XYXZ, the contents of PRO, ∆1-pyrroline, and methylglyoxal significantly increased using the T2, T3, and T4 treatments in 2022 and 2023, as compared with the T1 treatment, where the P5C content showed no significant difference in 2023. Additionally, in 2022, the T4 treatment led to the highest contents of P5C and methylglyoxal, with increases of 4.82 and 8.47%, respectively. The application of biochar also regulated the enzyme activities related to 2-AP biosynthesis. In 2022 and 2023, both aromatic rice varieties showed a significant increase in PDH activity with the T2, T3, and T4 treatments, compared with the T1 treatment. The P5CS activity of XYXZ showed no significant difference, while the P5CS activity of MXZ2 significantly increased with the T3 and T4 treatments, with increases of 6.06, 6.49, 3.23, and 5.20%, respectively, in 2022 and 2023 (Figure 5).

3.5. Grain Quality

The application of biochar had a significant effect on the grain quality of fragrant rice. In terms of milling quality, for MXZ2, the brown rice rate, milled rice rate, and head rice rate were the highest using the T4 treatment, increasing by 1.11, 2.61 and 5.55%, respectively, compared with the T1 treatment in 2022. In 2023, the brown rice rate was the highest under the T3 treatment, and the milled rice rate was the highest under the T4 treatment, increasing by 1.24 and 2.26%, respectively, compared with the T1 treatment. For XYXZ, in 2022 and 2023, there was no significant difference between the brown rice rate and the milled rice rate, and the head rice rate was reduced in the T3 and T4 treatments compared with the T2 treatment. In terms of appearance quality, compared with the T1 treatment, the chalkiness degree and chalk rice rate under the T2, T3, and T4 treatments showed a decreased trend for the two fragrant cultivars in 2022 and 2023 (Table 3).

3.6. Regression Analysis and Heatmaps for Various Indexes

To further evaluate possible differences between the investigated parameters of the treatments, a regression analysis was performed in 2022 and 2023. The correlation analysis showed that the 2-AP content was positively correlated with the PDH and P5CS activity, as well as the PRO, P5C, ∆1-pyrroline, and methylglyoxal contents (Figure 6).
The grain yield was positively correlated with the PDH activity, the methylglyoxal content, the total biomass accumulation in the full heading stage, total biomass accumulation in the maturity stage, intercellular CO2 concentration, net photosynthetic rate, grain number per panicle, seed setting rate, and milled rice rate. The content of 2-AP was positively correlated with the PDH and P5CS activities, as well as the PRO, P5C, and methylglyoxal contents, the total biomass accumulation in the full heading stage, total biomass accumulation in the maturity stage, net photosynthetic rate, number of effective panicles, and 1000-grain weight (Figure 7).

4. Discussion

Biochar application can effectively promote nutrient circulation between soil and plants, thereby improving yield, grain quality, biomass accumulation, and related physiological characteristics [30]. In the present study, we explored the effects of different biochar fertilizer application rates on the yield components, grain quality, 2-AP content, biomass accumulation, and photosynthetic characteristics of two fragrant rice cultivars. We found that the grain yield significantly increased with the increase in the biochar fertilizer application rate for both fragrant rice cultivars, which could be attributed to the increase in the yield components (number of effective panicles, seed setting rate, and 1000-grain weight) (Table 1). The results of our study are consistent with those in [31], where it was demonstrated that biochar increased the rice grain yield, number of effective panicles, and seed setting rate. Similarly, the authors of [32] proved that the application of biochar could increase the total biomass accumulation and the number of grains per panicle, thereby increasing the yield of rice.
The accumulation and transport of dry matter are the key factors affecting grain yield. Studies have shown that fertilization application can increase dry matter accumulation in each part of the plant, promote dry matter transport from the stem and leaves to the panicles, and significantly increase the contribution rate of material assimilation in the late heading stage. An et al. [33] revealed that fertilization application could increase rice dry matter. In the present study, we found that the application of biochar could increase the accumulation of dry matter in the above-ground part of rice (Figure 1 and Figure 2) and reached its maximum in the maturity stage. This is consistent with the findings of a study [34] which demonstrated that the application of biochar could increase the accumulation of dry matter in rice to a certain extent. Meanwhile, we found that the application of biochar could increase the net photosynthetic rate and intercellular CO2 concentration (Figure 3). Ullah et al. and Sainju et al. [35,36] revealed that the application of biochar fertilizer can promote photosynthetic capacity and [37] dry matter accumulation. Therefore, it can be concluded that biochar can promote the biomass accumulation of fragrant rice by improving its photosynthetic characteristics and enables the dry matter of stems and leaves to be transported to the grain, ultimately increasing the grain yield.
The demand for rice grains with certain aroma characteristics is increasing. 2-AP is a key compound in rice with a fragrant aroma [38]. PRO, P5C, and ∆1-pyrroline can be regulated through PDH and PSCS to eventually generate 2-AP. The present study showed that the content of 2-AP increased with increased rates of biochar application (Figure 4). This was attributed to the enzyme activity of PDH and PSCS and the increase in the PRO, P5C, ∆1-pyrroline, and methylglyoxal contents (Figure 5). The regression analysis results showed that the content of 2-AP was positively correlated with related precursor substances (PRO, P5C, ∆1-pyrroline, methylglyoxal) and related enzymes (PDH, P5CS) (Figure 6). Our results are consistent with those reported in [39], which showed that 2-AP was positively correlated with PRO, P5C, PDH, and PSCS. A similar discovery was reported in [40], which demonstrated that application of fertilizers increased the 2-AP content, and 2-AP was positively correlated with PRO, P5C, PDH, and PSCS. Therefore, it can be inferred that biochar increases the 2-AP content by enhancing the precursor substances of the 2-AP synthesis pathway.
In addition to yield, the grain quality is also a determinant in farmers’ economic returns, usually including rice milling, appearance, cooking, and nutrient quality. The difference in rice quality is related to environmental conditions and rice varieties [41]. Moreover, excessive use of chemical fertilizer will also have adverse effects on rice quality [42]. Biochar, as an environmentally friendly material, has received a lot of attention in recent years. The results showed that MXZ2 and XYXZ increased the milling rice rate and head rice rate, but both decreased the chalkiness degree and chalk rice rate. In terms of appearance quality, there were significant differences between C, Y × B, C × B and Y × C × B (Table 3). Our results were consistent with those reported in [43], which showed that the application of biochar increased the brown rice rate, milling rice rate, and head rice rate but decreased the chalkiness degree and chalk rice rate of rice.

5. Conclusions

Our two-year field experiment showed that the application of biochar at increasing rates improved the grain yield by increasing the number of effective panicles, seed setting rate, 1000-grain weight, total biomass accumulation, and photosynthetic characteristics. The application of biochar increased the 2-acetyl-1-pyrroline (2-AP) content by increasing the activities of proline dehydrogenase (PDH) and 1-pyrrole-5-carboxylic acid synthetase (P5CS) and the contents of proline (PRO), 1-pyrrole-5-carboxylic acid (P5C), and methylglyoxal. In terms of rice quality, the application of biochar increased the percentage of brown rice, milled rice rate, and head rice rate but reduced the chalkiness degree and chalk rice rate. In summary, the application of biochar increased the grain yield and 2-AP content of fragrant rice.

Author Contributions

Conceptualization, X.T. and Z.M.; methodology, J.Q. and M.D.; analysis, X.Z.; investigation, X.Z., X.Q., X.Y., J.W. and S.T.; data curation, X.Z.; writing—original draft preparation, X.Z.; supervision, X.Z.; writing—review and editing, Z.M. and J.Q.; visualization, X.T. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (31971843), the Technology System of Modern Agricultural Industry in Guangdong (2020KJ105), Guangzhou Science and Technology Project (202103000075), and the Special Rural Revitalization Funds of Guangdong Province (2021KJ382).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to the authors will use these data for writing their graduation thesis.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effects of biochar application on dry matter accumulation in the stem–leaf and panicle in four stages of fragrant rice (tillering stage, booting stage, full heading stage, and maturity stage) in 2022–2023. Different lowercase letters above the line indicate significant differences between treatments in the same part (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; MTS: maximum tillering stage; BS: booting stage; FHS: full heading stage; MS: maturity stage. (A–D) indicates 2022 MXZ2; (E–H) indicates 2022 XYXZ; (I–L) indicates 2023 MXZ2; (M–P) indicates 2023 XYXZ.
Figure 1. Effects of biochar application on dry matter accumulation in the stem–leaf and panicle in four stages of fragrant rice (tillering stage, booting stage, full heading stage, and maturity stage) in 2022–2023. Different lowercase letters above the line indicate significant differences between treatments in the same part (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; MTS: maximum tillering stage; BS: booting stage; FHS: full heading stage; MS: maturity stage. (A–D) indicates 2022 MXZ2; (E–H) indicates 2022 XYXZ; (I–L) indicates 2023 MXZ2; (M–P) indicates 2023 XYXZ.
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Figure 2. Effects of applications of biochar on total biomass accumulation in fragrant rice at full heading stage (A) and maturity stage (B) of 2022–2023. Different lowercase letters above the column indicated a significant difference among treatments in the same period (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; FHS: full heading stage; MS: maturity stage.
Figure 2. Effects of applications of biochar on total biomass accumulation in fragrant rice at full heading stage (A) and maturity stage (B) of 2022–2023. Different lowercase letters above the column indicated a significant difference among treatments in the same period (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; FHS: full heading stage; MS: maturity stage.
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Figure 3. Effects of applications of biochar on transpiration rate (A), stomatal conductance (B), intercellular CO2 concentration (C), net photosynthetic rate (D) in fragrant rice at full heading stage of 2022–2023. Different lowercase letters above the column indicated a significant difference among treatments in the same period (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan.
Figure 3. Effects of applications of biochar on transpiration rate (A), stomatal conductance (B), intercellular CO2 concentration (C), net photosynthetic rate (D) in fragrant rice at full heading stage of 2022–2023. Different lowercase letters above the column indicated a significant difference among treatments in the same period (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan.
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Figure 4. Effects of biochar fertilizer applications on the 2-AP content of fragrant rice in the maturity stage in 2022–2023. MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; 2-AP: 2-acetyl-1-pyrroline. Different lowercase letters above the column indicate significant differences between treatments in the same year (p < 0.05).
Figure 4. Effects of biochar fertilizer applications on the 2-AP content of fragrant rice in the maturity stage in 2022–2023. MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; 2-AP: 2-acetyl-1-pyrroline. Different lowercase letters above the column indicate significant differences between treatments in the same year (p < 0.05).
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Figure 5. Effects of applications of biochar on PRO (A), PDH (B), P5C (C), P5CS (D), ∆1-pyrroline (E), and methylglyoxal (F) in the grains of fragrant rice at the maturity stage (2022–2023). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase; different lowercase letters above the column indicate a significant difference among treatments in the same years (p < 0.05).
Figure 5. Effects of applications of biochar on PRO (A), PDH (B), P5C (C), P5CS (D), ∆1-pyrroline (E), and methylglyoxal (F) in the grains of fragrant rice at the maturity stage (2022–2023). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase; different lowercase letters above the column indicate a significant difference among treatments in the same years (p < 0.05).
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Figure 6. Regression analysis between 2-AP content and enzymes involved in 2-AP biosynthesis in MXZ2 (A,C,E,G,I,K) and XYXZ (B,D,F,H,J,L) under different treatments (2022–2023). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; 2-acetyl-1-pyrroline; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase. * and ** represent a significant difference at p < 0.05 and p < 0.01, respectively.
Figure 6. Regression analysis between 2-AP content and enzymes involved in 2-AP biosynthesis in MXZ2 (A,C,E,G,I,K) and XYXZ (B,D,F,H,J,L) under different treatments (2022–2023). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; 2-acetyl-1-pyrroline; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase. * and ** represent a significant difference at p < 0.05 and p < 0.01, respectively.
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Figure 7. Correlation analysis of the indicators. Data from 2022 and 2023 were used for the analysis. Red indicates a positive correlation between the two parameters. Blue indicates a negative correlation between the two parameters. * represents a significant difference at p < 0.05. 2-AP: 2-acetyl-1-pyrroline; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase; TBA-FHS: total biomass accumulation in the fulling heading stage; TBA-MS: total biomass accumulation in the maturity stage; Tr: transpiration rate; Gs: stomatal conductance; Ci: intercellular CO2 concentration; Pn: net photosynthetic rate; EP: number of effective panicles; GPP: grain number per panicle; SET: seed setting rate; TGW: 1000-grain weight; BR: brown rice rate; MR: milled rice rate; HR: head rice rate; CD: chalkiness degree; CR: chalk rice rate.
Figure 7. Correlation analysis of the indicators. Data from 2022 and 2023 were used for the analysis. Red indicates a positive correlation between the two parameters. Blue indicates a negative correlation between the two parameters. * represents a significant difference at p < 0.05. 2-AP: 2-acetyl-1-pyrroline; PRO: proline; P5C: 1-pyrrolin-5-carboxylic acid; PDH: proline dehydrogenase; P5CS: 1-pyrrolin-5-carboxylate acid synthetase; TBA-FHS: total biomass accumulation in the fulling heading stage; TBA-MS: total biomass accumulation in the maturity stage; Tr: transpiration rate; Gs: stomatal conductance; Ci: intercellular CO2 concentration; Pn: net photosynthetic rate; EP: number of effective panicles; GPP: grain number per panicle; SET: seed setting rate; TGW: 1000-grain weight; BR: brown rice rate; MR: milled rice rate; HR: head rice rate; CD: chalkiness degree; CR: chalk rice rate.
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Table 1. Mean monthly temperatures and precipitation during the rice-planting seasons.
Table 1. Mean monthly temperatures and precipitation during the rice-planting seasons.
MonthAverage Temperature
(°C) 		Maximum Temperature (°C)Minimum Temperature (°C)Precipitation
(mm)
20222023202220232022202320222023
March22.0321.0727.8725.615.4414.75182.63161.29
April23.6123.6329.1628.1917.1618.76165.3577.72
May25.0327.3929.6731.8220.5222.27367.03221.49
June28.6729.3233.1534.4624.7425.16385.83354.33
July31.2431.1236.2236.1725.6625.73206.76193.04
Table 2. Effects of biochar application on the grain yield and yield components of fragrant rice in 2022 and 2023.
Table 2. Effects of biochar application on the grain yield and yield components of fragrant rice in 2022 and 2023.
YearCultivarTreatmentNumber of Effective Panicles
(×104 ha−1)		Grains Number per PanicleSeed Setting Rate (%)1000-Grain Weight (g)Yield
(t ha−1)
2022MXZ2T1212.67 ± 14.67 b159.05 ± 1.46 a77.45 ± 1.06 b17.95 ± 0.03 b4.62 ± 0.19 b
T2264.00 ± 12.70 a155.03 ± 6.82 a84.73 ± 1.74 a17.96 ± 0.14 b5.87 ± 0.06 a
T3300.67 ± 19.40 a152.05 ± 3.94 a85.83 ± 1.44 a18.54 ± 0.13 a5.97 ± 0.16 a
T4308.00 ± 12.70 a158.02 ± 12.03 a84.99 ± 1.10 a18.50 ± 0.09 a6.18 ± 0.22 a
XYXZT1234.67 ± 7.33 c128.73 ± 8.29 a75.21 ± 0.71 a19.10 ± 0.15 a4.03 ± 0.23 b
T2278.67 ± 7.33 b140.35 ± 5.01 a77.19 ± 0.94 a19.03 ± 0.13 a4.45 ± 0.14 ab
T3330.00 ± 12.70 a138.71 ± 6.67 a77.89 ± 2.04 a19.38 ± 0.25 a4.51 ± 0.09 ab
T4337.34 ± 7.33 a122.10 ± 1.01 a78.55 ± 1.46 a19.52 ± 0.35 a4.90 ± 0.21 a
2023MXZ2T1212.67 ± 19.40 b149.20 ± 11.06 a83.25 ± 0.98 a18.72 ± 0.51 a5.02 ± 0.12 b
T2293.33 ± 19.40 a161.90 ± 4.77 a84.16 ± 0.63 a18.86 ± 0.32 a5.45 ± 0.12 b
T3300.67 ± 14.67 a167.10 ± 7.62 a82.74 ± 1.05 a18.56 ± 0.61 a6.16 ± 0.32 a
T4300.67 ± 7.33 a153.41 ± 5.84 a84.96 ± 0.18 a18.75 ± 0.13 a6.33 ± 0.07 a
XYXZT1198.00 ± 12.70 d136.07 ± 11.43 b83.49 ± 0.46 a17.75 ± 0.07 c5.50 ± 0.24 a
T2249.33 ± 7.33 c163.98 ± 3.46 a82.40 ± 1.55 a18.65 ± 0.09 b5.83 ± 0.44 a
T3293.33 ± 7.33 b141.49 ± 1.89 ab85.06 ± 0.15 a18.60 ± 0.19 b5.94 ± 0.04 a
T4322.67 ± 7.33 a139.65 ± 10.33 ab84.44 ± 1.03 a19.17 ± 0.14 a6.14 ± 0.28 a
ANOVAY nsns**ns**
C ns******
B **nsnsns**
Y × C **ns******
Y × B nsnsnsnsns
C × B nsnsnsnsns
Y × C × B nsnsnsnsns
Within the same variety, different lowercase letters in the same column indicate significant differences between treatments (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; Y: year; C: cultivar; B: biochar treatment; Y × C: interaction between year and cultivar; Y × B: interaction between year and biochar treatment; C × B: interaction between cultivar and biochar treatment; Y × C × B: interaction between year, cultivar, and biochar treatment; * and ** represent a significant difference at p < 0.05 and p < 0.01, respectively; ns represents a non-significant difference.
Table 3. Effects of biochar applications on the grain quality of fragrant rice in 2022 and 2023.
Table 3. Effects of biochar applications on the grain quality of fragrant rice in 2022 and 2023.
YearCultivarTreatmentBrown Rice Rate (%)Milled Rice Rate (%)Head Rice Rate (%)Chalkiness Degree (%)Chalk Rice Rate (%)
2022MXZ2T180.35 ± 0.11 b70.2 ± 0.20 b60.03 ± 0.53 b15.25 ± 0.25 a5.53 ± 0.22 a
T280.82 ± 0.14 ab70.75 ± 0.42 b59.02 ± 0.26 bc10.81 ± 0.14 b5.30 ± 0.10 a
T380.69 ± 0.14 b70.72 ± 0.34 b58.08 ± 0.16 c11.68 ± 0.55 b3.56 ± 0.17 b
T481.24 ± 0.17 a72.03 ± 0.34 a63.36 ± 0.28 a10.4 ± 1.18 b2.84 ± 0.15 c
XYXZT179.48 ± 0.20 a65.43 ± 0.30 a56.02 ± 0.48 c10.04 ± 0.41 a4.41 ± 0.24 d
T279.32 ± 0.13 a64.92 ± 0.28 a58.29 ± 0.29 a7.16 ± 0.71 b2.41 ± 0.19 b
T379.66 ± 0.20 a64.35 ± 0.32 a57.17 ± 0.17 b5.48 ± 0.69 c1.54 ± 0.13 c
T479.78 ± 0.21 a65.58 ± 0.57 a56.37 ± 0.26 bc4.41 ± 0.24 d2.29 ± 0.13 b
2023MXZ2T179.21 ± 0.34 b67.60 ± 0.75 b58.57 ± 0.56 b11.51 ± 0.87 a4.35 ± 0.08 a
T279.76 ± 0.04 ab68.90 ± 0.2 ab60.22 ± 0.17 a10.04 ± 0.41 a4.19 ± 0.06 ab
T380.19 ± 0.05 a68.67 ± 0.2 ab60.81 ± 0.21 a8.25 ± 0.32 c3.04 ± 0.11 c
T480.15 ± 0.12 a69.13 ± 0.09 a60.87 ± 0.31 a10.17 ± 0.37 b3.94 ± 0.11 b
XYXZT179.33 ± 0.08 a67.85 ± 0.31 a54.86 ± 0.65 b5.58 ± 0.23 a2.10 ± 0.06 a
T279.41 ± 0.28 a66.89 ± 0.05 a58.64 ± 0.48 a4.46 ± 0.09 c1.20 ± 0.06 c
T379.44 ± 0.04 a67.66 ± 0.74 a56.16 ± 0.84 b4.81 ± 0.14 b1.66 ± 0.08 b
T479.69 ± 0.30 a67.98 ± 0.55 a56.83 ± 0.24 ab3.92 ± 0.12 d1.69 ± 0.04 b
ANOVAY **nsns*ns
C **********
B nsnsns*ns
Y × C ****nsns**
Y × B nsns******
C × B ns*******
Y × C × B nsns*****
Within the same variety, different lowercase letters in the same column indicate significant differences between treatments (p < 0.05). MXZ2: Meixiangzhan2; XYXZ: Xiangyaxiangzhan; Y: year; C: cultivar; B: biochar treatment; Y × C: interaction between year and cultivar; Y × B: interaction between year and biochar treatment; C × B: interaction between cultivar and biochar treatment; Y × C × B: interaction among year, cultivar, and biochar treatment; * and ** represent a significant difference at p < 0.05 and p < 0.01, respectively; ns represents a non-significant difference.
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Zhang, X.; Qiu, X.; Yao, X.; Wei, J.; Tong, S.; Mo, Z.; Qi, J.; Duan, M.; Tang, X. Biochar Regulates 2-Acetyl-1-Pyrroline, Grain Yield and Quality in Fragrant Rice Cropping Systems in Southern China. Agronomy 2023, 13, 2860. https://doi.org/10.3390/agronomy13122860

AMA Style

Zhang X, Qiu X, Yao X, Wei J, Tong S, Mo Z, Qi J, Duan M, Tang X. Biochar Regulates 2-Acetyl-1-Pyrroline, Grain Yield and Quality in Fragrant Rice Cropping Systems in Southern China. Agronomy. 2023; 13(12):2860. https://doi.org/10.3390/agronomy13122860

Chicago/Turabian Style

Zhang, Xuechan, Xinfeng Qiu, Xiangbin Yao, Jianjiao Wei, Shaojie Tong, Zhaowen Mo, Jianying Qi, Meiyang Duan, and Xiangru Tang. 2023. "Biochar Regulates 2-Acetyl-1-Pyrroline, Grain Yield and Quality in Fragrant Rice Cropping Systems in Southern China" Agronomy 13, no. 12: 2860. https://doi.org/10.3390/agronomy13122860

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