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Article

Effects of Digested Pig Slurry on Photosynthesis, Carbohydrate Metabolism and Yield of Tomato (Solanum lycopersicum L.)

by
Yunfei Teng
1,
Bin Shang
1 and
Xiuping Tao
2,*
1
Key Laboratory of Energy Conservation and Waste Management in Agricultural Structures, Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Science, Beijing 100081, China
2
Institute of Urban Agriculture, Chinese Academy of Agricultural Science, Chengdu 610000, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(9), 2042; https://doi.org/10.3390/agronomy12092042
Submission received: 4 July 2022 / Revised: 18 August 2022 / Accepted: 23 August 2022 / Published: 27 August 2022
(This article belongs to the Section Horticultural and Floricultural Crops)
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Abstract

:
Soilless cultivation of vegetables is widely used in production. It is also well accepted that digested slurry is frequently applied as a fertilizer in agricultural production. However, the effect of digested pig slurry on yield and quality of tomato soilless cultivation, as well as the yield and quality influenced by plant carbohydrate metabolism, remain unexplored. Here, the dual inputs of fertilizers (digested pig slurry (D) and mineral fertilizer (M)) and soilless substrates (peat substrate (P) and cinder substrate(C)) consisted of four treatments. The dry biomass and fruit yields, photosynthetic parameters, carbohydrate contents and metabolism enzymes in leaves and fruits were recorded during the experimental period. The highest fruit yields were obtained in DP and MP treatments. Although DP treatment significantly increased the fresh weight of single fruits by 18.0% compared to MP treatment, it reduced the number of ripe fruits. The photosynthetic efficiency and carbohydrate contents (sucrose, glucose and fructose) in leaves were generally higher in DP treatment compared to other treatments, as well as the activities of sucrose phosphate synthase and AGPase in leaves. The soluble sugar contents of fruits in DP and DC treatments were enhanced by 12.3% and 37.0%, respectively, compared to MP and MC treatments. Moreover, the current results showed that DP treatment significantly increased the activity of acid invertase in fruit by 36.3%, 31.3%, and 42.2%, respectively, compared to MP, DC, and MC treatments, and decreased the activity of AGPase by 24.2%, 16.0%, and 36.4%, respectively. The current results have demonstrated that DP treatment had better yield and quality, owing to digested pig slurry increasing the photosynthetic efficiency and source strength, and regulated the activities of carbohydrate metabolism enzymes.

1. Introduction

Digested slurry is a by-product of anaerobic digestion of manure, which has the potential to be used as fertilizer in crop management [1]. Digested slurry may contain substantial amounts of mineral elements such as nitrogen, phosphorus, potassium, and other trace elements [2]. Currently, the use of digested slurry as a fertilizer has drastically increased, not only due to the considerable increases in the cost of chemical fertilizer, but also to sustainably utilize the high nutrient level in digested slurry [3,4]. Plants can directly absorb the available nitrogen in digested slurry, including inorganic nitrate (NO3), ammonium (NH4), and as a simply structured organic, partly from the degradation of organic matter [5]. Therefore, digested slurry was conducive to the yields and qualities of crops or fruits as reported by many previous studies [6,7,8,9,10].
Tomato is one of the most important horticulture crops, with the largest production volume globally [11]. The functional value of tomato was primarily embodied in the contents of sugar, lycopene, vitamin C, and polyphenols [12]. Many previous studies have focused on the effect of application of digested slurry on the quality of tomato fruit [9,13,14]. There are also studies available regarding the impacts of digested slurry on tomato yields [15,16,17]. Of those studies, the main focus has been the evaluation of yield depending on the dose, method of fertilization and the nutrient characteristic of digested slurry. However, those studies were mainly performed in soil cultivation. Plant production in soilless culture is rapidly expanding. Soilless cultivation of vegetables with digested slurry was a promising method for integrating food production and organic waste management. Furthermore, digested slurry was considered a suitable fertilizer source for tomato due to the high levels of N and K normally found in digested slurry [18]. However, the combined effect of digested slurry and soilless substrates on the yield and quality of tomato fruit is limited, and especially the combined effects on carbohydrate metabolism in tomato remain uninvestigated.
Carbohydrates are essential to yield and quality of crops since they are not only the raw materials for fruit growth but also the major determinants of fruit quality [19]. Plant growth and carbohydrate metabolism are closely associated since carbohydrate generated by photosynthesis provides the primary source of building blocks and energy for production [20]. Digested slurry with suitable concentration could increase the photosynthetic efficiency of plants [21,22]. Xu et al. [23] reported that digested slurry can improve the photosynthetic efficiency, metabolic level and promote the growth of Perilla frutescens seedlings. External factors such as nutrients regulate the activities of enzymes [24]. The activity of various enzymes in metabolic processes alters the content and overall composition of sugars in the sink organ. Furthermore, source loading and leaf metabolism, as well as carbohydrates transport, are closely related to enzyme activities in the source (leaves) and sink tissues (fruit) [25]. However, there is limited research on the variation of carbohydrate metabolism of tomato plants when digested pig slurry is used as fertilizer.
The objectives of this study were to: (1) investigate the effects of digested pig slurry on the yield and quality of tomato fruits when adding them to two types of substrates. (2) explore the variation of leaf and fruit carbohydrates metabolism when tomato plants were fed with digested pig slurry on soilless substrates.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

Tomato seeds (Solanum Lycopersicum. L. cv. Ruifen 882, Rijk Zwaan Agricultural Technology Co., LTD, De Lier, the Netherlands) were sown into 50-cell plug trays, and seedlings were transplanted to a Chinese Solar Greenhouse (CSG) when the fifth leaf expanded. The CSG had an area of 600 m2 (60 m×10 m) and was located in Shunyi district, Beijing, China (40°26′ N, 116°52′ E). The entire experimental duration was between November 2020 and June 2021, during which the daytime average air temperature and relative humidity (RH) in the greenhouse were 23.9 ± 2. °C and 44.8 ± 9.4%, respectively, and at night-time were 12.7 ± 2.3 °C and 88.0 ± 4.5%, respectively. The greenhouse was covered with a thermal insulation quilt at night (from 6:00 PM to 8:00 AM). The average photosynthetic active radiation at solar noon was 563.5 ± 213.7 µmol·m−2·s−1.

2.2. Fertilizer and Substrate Treatments

Two types of fertilizers (i.e., digested pig slurry and chemical fertilizer) and two soilless substrates (i.e., peat substrates and cinder substrates) were used in this study based on four treatments (Completely randomized block design), i.e., digested pig slurry applied on peat substrate (DP), mineral fertilizer applied on peat substrate (MP), digested pig slurry applied on cinder substrate (DC), and mineral fertilizer applied on cinder substrate (MC). The digested pig slurry was obtained from a large-scale anaerobic digestor with a capacity of 2.52 × 104 m3 located in Tangshan city, Hebei province, China. The hydraulic retention time of anaerobic digestion was 30 days. After digestates collection from the anaerobic digestor, they were stored at 4 °C for analysis, and the characteristics of digestates are shown in Table 1.
Two growth media based on mixtures of peat and cinder were prepared. Cinder substrate lacks nutrients with low water-holding capacity, which often constrains plant growth and depends on the treatment application [26], whereas peat substrate was the one obtained with a richer nutrient compared to cinder substrate. Peat substrates are formulated by blending 60% peat (Pindstrup Horticulture Co., Ltd., Ryomgaard, Denmark), 20% vermiculite, and 20% perlite by volume, and cinder substrates are formulated by blending 50% cinder and 50% vermiculite by volume. These soilless mediums were purchased from Green life Agricultural Technology Co., Ltd., Shijiazhuang city, China. The contents of total nitrogen, available phosphorus, available potassium and total carbon were 3.06 ± 0.11 g/kg, 0.26 ± 0.001 g/kg, 0.82 ± 0.001 g/kg, and 26.58 ± 0.40% for peat substrate, respectively, and 0.21 ± 0.05 g/kg, 0.02 ± 0.001 g/kg, 0.04 ± 0.001 g/kg, and 2.93 ± 0.35% in cinder substrates, respectively.
Fifteen tomato plants were grown in each treatment. Plants were grown in plastic pots with a volume of 12 L, each. The pots were arranged at a density of three plants per m−2. The fertilizer rates were determined according to the nutrients balance method [27]. The target yield is 90,000 kg/ha, the amounts of N, P2O5, and K2O were 347.4 kg/ha, 104.0 kg/ha, and 399.6 kg/ha, respectively. The amount of digested pig slurry (calculated according to N content) or chemical fertilizer applied in different treatments is shown in Table 2. All watering was done manually on the surface of the substrate. Each plant was irrigated with 1 L tap water in March and April 2021 and 2 L in May and June 2021 every two days, which was sufficient to avoid water stress.

2.3. Sampling and Measurements

2.3.1. Growth Measurements

During the experiment ripe fruits were harvested four times on 5 May, 20 May, 1 June and 16 June 2021, respectively. The accumulated fresh weight of ripe fruits was considered as the fruit yield. Destructive harvest measurements were taken at the end of the experiment. Four plants were randomly selected from each treatment. Fresh weight of roots, stems, leaves and fruits were determined, and dry weight of roots, stems and leaves were determined after being placed in a ventilated oven (DHG-9620-A; Bluepard, Shanghai, China) at 80 °C for at least 3 days, while dry weights of fruits were determined at 105 °C for 5 days. Plant total biomass was the sum of the dry weight of plant organs produced during the experiment.

2.3.2. Leaf Photosynthesis Measurements

Net leaf photosynthetic rate (Pn), stomatal conductance (Cond), CO2 concentration in substomatal cavity (Ci) and Transpiration rate (Tr) were taken 60 days after seedling transplanting, i.e., 30-day fruit age. Four plants from each treatment were randomly selected, and measurements were performed on the upper-most fully expanded leaves, between 8:30 and 15:30. The measurements were performed with the LI-6400XT photosynthesis system (Li-COR Biosciences, Lincoln, NE, USA) equipped with a leaf chamber fluorometer (LI-COR part no. 6400-40, enclosed leaf area: 2 cm2). During measurements, photosynthetic photon flux density (PPFD) was 600 µmol·m−2·s−1, CO2 partial pressure was 400 µmol·mol−1, leaf temperature was 25 °C, leaf-to-air vapor pressure deficit (VPDleaf-air) was maintained at 0.7–1.0 kPa, and the flow rate of air through the system was 500 µmol·s−1. Irradiance was provided by a mixture of red (90%) and blue (10%) LEDs in the fluorometer. Peak intensities of red and blue LEDs were at wavelengths of 635 nm and 465 nm, respectively.

2.3.3. Leaf Carbohydrate Contents and Metabolism Enzymes Measurements

To determine leaf carbohydrate contents, leaf samples were collected after photosynthesis measurements for each treatment. Samples were covered by aluminum foil and immediately plunged into liquid nitrogen and stored at −80 °C until analysis. The carbohydrates contents of leaves (sucrose, fructose, glucose and starch) were determined using ELISA kits (Beijing Solarbio Science & Technology Co., Ltd., Beijing, China). The sugar metabolism enzymes of leaves (sucrose phosphate synthase, sucrose synthase, and adenosine glucose pyrophosphorylase) were assayed according to the method of Liao et al. [28].

2.3.4. Fruit Carbohydrate Contents and Metabolism Enzymes Measurements

Fruit sampling was taken at 20 days after anthesis (anthesis started from March 15), six tomato fruits were sampled at each sampling time, and a total of four samplings were performed at fruit ages of 20 days, 30 days, 40 days and 50 days in the first truss. Three fruits were used for dry weight determination using the gravimetric method, and the other fruits were frozen immediately in liquid nitrogen, then stored at −80 °C for the analysis of sugars concentration and enzymes activities. The carbohydrates contents (soluble sugar and starch) and the metabolism enzymes (acid invertase, sucrose synthase, sucrose phosphate synthase, and adenosine glucose pyrophosphorylase) activities in tomato fruits were determined similarly as in leaf samples.
The carbon supply flux (Csupply, g/d) was calculated using the following equation:
C supply = c D W d D W d t + d C r e p d t
where cDW was the carbon amount in 1 g of dry mass (g C/g DW) with the value of 0.44 for tomato fruit; dDW/dt was the variation rate of fruit dry weight; dCrep/dt was the carbon efflux by respiration.

2.4. Statistical Analysis

All results were subjected to two-way analysis of variance (ANOVA) for two main experimental factors—‘fertilizer source’ and ‘substrate type’—and their interaction and followed by Fisher’s protected least significant test (LSD) at 95% confidence. All analyses were performed using the software of Statistical Package for the Social Sciences (SPSS Inc. Release 25, Chicago, IL, USA). Correlation analysis was implemented for carbohydrate contents and the activities of metabolism enzymes of fruits in all treatments via Pearson’s correlations and two-sided tests.

3. Results

3.1. Tomato Growth and Yield

DP and MP treatments significantly increased the plant dry biomass and fruit yields by 29.2%, 43.5%, and 53.5%, 62.3%, respectively, compared to DC and MC treatments (Table 3 and Table 4). Although DP treatment significantly increased the fresh weight of single fruit, it did not increase the number of ripe fruits (Table 4). Moreover, DC treatment significantly increased the fruit yields by 34.4% compared to MC treatment. This mainly resulted from a significantly higher fruit number per plant (Table 4). Only fertilizer source was not significant on fruit number, and the other components of the yield were all influenced by fertilizer, substrate, and their interaction.

3.2. Photosynthetic Parameters and Carbohydrate Metabolism of Tomato Leaves

The greatest leaf photosynthetic rate was observed in DP treatment, and this mainly resulted from a higher value of Cond and Ci in DP treatment (Figure 1). Similarly, transpiration rates in DP treatment significantly increased by 30.2%, 45.0%, and 40.8%, respectively, compared to MP, DC, and MC treatments. Fertilizer source and the interaction Fertilizer × Substrate were not significant on Pn, and the other photosynthetic parameters were all influenced by fertilizer, substrate, and their interaction.
The two digested pig slurry treatments significantly increased the sucrose, fructose, and glucose contents in leaves by 30%, 29.9%, 33.3% and 50%, 47.2%, 66.7%, respectively, compared to the two of mineral fertilizer treatments. This mainly resulted from the higher activities of sucrose phosphate synthase in leaves of two digested pig slurry treatments (Table 5 and Table 6). On the contrary, the starch content of MC treatment was significantly higher than DP, MP, and MC treatments by 27.3%, 9.1%, and 36.4%, respectively. Moreover, the activities of AGPase in leaves for digested pig slurry treatments were 16.2% and 9.8% higher than the two of mineral fertilizer treatments, respectively (Table 6). Fertilizer source significantly influenced the carbohydrates contents and the activities of carbohydrate metabolism enzymes in leaves. Likewise, substrate type significantly influenced sucrose, glucose, sucrose synthase and AGPase, and the interaction Fertilizer × Substrate significantly influenced glucose, starch, sucrose phosphate synthase and sucrose synthase.

3.3. Carbon Supply Flux and Carbohydrate Contents of Tomato Fruits

Carbon supply flux (Csupply) directly reflects the carbon flows into the fruit. Csupply increased with time in DP and MC treatments but decreased with time in DC treatment. The Csupply in DP treatment was significantly higher than MP, DC, and MC treatments by 66.7%, 71.8%, and 59.0%, respectively, after 40 days of fruit age (Table 7).
The two digested pig slurry treatments significantly increased the soluble sugar content of fruit by 12.3% and 37.0%, respectively, compared to the two of mineral fertilizer treatments at 50 days of fruit age (Figure 2). As for the starch content, significantly higher fruit starch contents were detected in DC and MP treatments (0.89 ± 0.01 and 0.82 ± 0.04, respectively) when fruit age was less than 40 days (Figure 2). Fertilizer, substrate, and their interaction all significantly influence the soluble sugar and starch contents of fruit.

3.4. The Variation of Carbohydrate Metabolism Enzymes of Tomato Fruit and Correlation Analysis of Carbohydrate Metabolism

Acid invertase (AI) activity was positively correlated with the fruit dry weight and soluble sugar content of tomato fruits, with correlation coefficients (r) of 0.874 and 0.882, respectively (Table 8). At a fruit age of 50 days, DP treatment significantly increased the activity of AI by 36.3%, 31.3%, and 42.2%, respectively, compared to MP, DC, and MC treatments (Figure 3a). The activity of sucrose synthase (Susy) decreased with time, and positively correlated with starch content (r = 0.635) (Figure 3b and Table 8). Meanwhile, the activities of sucrose phosphate synthase (SPS) in DP and DC treatments were 50.8% and 31.0% higher than MP and MC treatments, respectively. SPS activity fluctuated during entire experimental periods, with the lower values appearing at 40 days of fruit age (Figure 3c and Table 8). AGPase activity correlated with the starch concentration (r = 0.548), As the fruit grew, the AGPase activity decreased with time. The lowest AGPase activity was achieved in DP treatment at 50 days of fruit age, whereas MC treatment showed the highest AGpase activity (Figure 3d and Table 8). Only substrate type was not significant on the activity of SPS of fruit, and the other carbohydrate enzymes of fruit were significantly influenced by fertilizer, substrate, and their interaction.

4. Discussion

4.1. Yield and Total Biomass Production

Fertilization is essential to determine the growth of crops [14]. In this study, the two digested pig slurry treatments increased the plant dry biomass and fruit yields compared to the two mineral fertilizer treatments (Table 3 and Table 4). This could be caused by two factors: first, the digested pig slurry was a quick-released nitrogen fertilizer [16,29], and second, the digested pig slurry had higher organic matter mineralization rates [18]. Moreover, the treatments in peat substrate significantly increased the fruit yields and plant dry biomass compared to the treatments in cinder substrate. This mainly resulted from the high pH in cinder substrate, causing nutrient nitrogen loss [16]. However, peat substrate is rich in organic matter, and has a high water-holding capacity and air space [26]. In addition, although DP treatment resulted in a significantly higher fresh weight of single fruit compared to MP treatment, there was no significant difference in the number of ripe fruits and fruit yields between the two treatments (Table 4). This indicated that DP treatment only stimulated fruit growth and did not increase the number of ripe fruits. On the contrary, DC treatment significantly increased the number of ripe fruits, while it did not increase the fresh weight of single fruit. A possible explanation for this might be that the higher amount of urea in MC treatment caused tomato seedling root damage and inhibited plant growth [30].

4.2. Photosynthesis and Carbohydrate Metabolism in Tomato Leaves

Photosynthesis provides carbohydrate for plant growth [20]. The current results showed that DP treatment had higher Pn compared to other treatments, which resulted from the significantly increased Cond and Ci of DP treatment (Figure 1). Stomatal opening degree affects plant photosynthetic efficiency [31]. Likewise, DP treatment significantly increased the transpiration rate compared to the other treatments. These findings were also acknowledged by Zhang et al. [21] and Xu et al. [23], who reported that digested slurry increased the supply of N and P elements and improved plant photosynthesis. Source-sink balance regulates carbon status in plants [20]. The current results showed that DP treatment significantly increased the sucrose, fructose, and glucose contents and the activities of AGPase and SPS in leaves compared to other treatments (Table 5 and Table 6). The overexpression of AGPase activity can increase transient starch accumulation in leaves and alleviate feedback inhibition of photosynthesis [32]. Likewise, the increase of SPS activity can enhance sucrose and hexose levels in leaves [32]. These results are likely to be related to the content of bioavailable potassium in DP treatment (possibly the microbial composition and activities in digested pig slurry facilitated the bioavailable potassium released), which regulated stomatal opening and enhanced the cellular osmotic regulation [33]. Therefore, DP treatment increased the photosynthetic efficiency and source strength, and consequently resulted in a higher carbohydrates content in plants.

4.3. Carbohydrate Contents of Tomato Fruits

In tomato fruit, photosynthesis affects source-sink partition, and contributes to final quality and yield [32]. Here, the Csupply of tomato fruit in DP treatment was significantly higher than the other treatments (Table 7). This result indicated that DP treatment significantly improved fruit growth. A possible explanation for this might be that potassium in DP treatment promoted the photoassimilates transport efficiency in phloem and improved the dry matter accumulation in fruits [34]. Furthermore, tomato plants grown with digested slurry often exhibit an enhancement in soluble sugar in fruits [9,13,14]. In this study, the soluble sugar content in DP treatment was significantly higher than MP treatment (Figure 2). This probably occurred because more bioavailable potassium in DP treatment causes sugar accumulation, and the latter is closely related to the potassium content [35]. Similarly, the soluble sugar content in DC treatment was significantly higher than MC treatment, which probably occurred because the relatively high electrical conductivity (EC) in digested pig slurry caused moderate salinity stress and increased soluble sugar contents of these tomatoes [36]. It is well known that salinity stress increases starch contents of tomato fruit [37,38], while starch degradation is an important source of sugar and energy at the beginning of fruit ripening [39]. In the current study, DC treatment had the highest starch content compared to other treatments when fruit age was less than 40 days (Figure 2), which can explain the reason why DC treatment had higher soluble sugar content in fruit ripening.

4.4. Carbohydrate Metabolism Enzymes Affect Fruit Yield and Quality

Carbohydrate metabolism is regulated by the related key enzymes [33]. The activity of various enzymes in metabolic processes alters the content and overall composition of sugars in the sink organ (fruits). Acid invertase (AI) is important in sucrose metabolism, which promotes sucrose conversion and hexose accumulation [40]. In the current study, a rapid increase of AI activity of DP treatment was observed at 50 days of fruit age (Figure 3a). This presence of acid invertase in cell walls provides possible machinery to degrade sucrose unloaded from phloem to fruit apoplast. The elevated soluble sugar levels in the apoplasmic space of fruits may be favorable to the maintenance of these turgor pressure gradients through an osmo-regulatory mechanism [41,42]. Meanwhile, water also flows into fruit with the water potential gradient between phloem and fruit [43]. The accumulation of water modifies fruit hydrostatic pressure, which drives the expansion of fruit volume and promotes fruit growth [44]. This explained the higher soluble sugar content and fruit dry weight of DP treatment (Figure 2 and Table 4). Susy and AGPase activities of fruits are key enzymes in regulating starch biosynthesis [32]. The current study showed that DC treatment significantly increased the Susy and AGPase activities at 20 days of fruit age (Figure 3b,d), which resulted in the accumulation of starch during the middle stage of fruit development [45]. Similarly, DC treatment showed the highest starch content at 20 days of fruit age (Figure 2). In accordance with the present results, previous studies have demonstrated that the activity of AGPase increased and AGPase-encoding genes were up-regulated under salt stress conditions [37]. Likewise, the fruit weight of tomato was inhibited by salinity stress due to the reduction of osmotic pressure and water potential [46]. Additionally, DP and DC treatments exhibited the highest SPS activities at 20 days of fruit age (Figure 3c). The SPS activity was correlated with maintaining the balance of sucrose concentration in the early fruit development stage [47]. However, the SPS activity at a fruit age of 50 days was increased again because sucrose resynthesis is necessary for its storage or its further intercellular transport [48].

5. Conclusions

The application of digested pig slurry clearly highlighted beneficial effects on the yields, photosynthetic parameters and carbohydrate contents of tomato plants, especially when cultivated on peat substrate. The results of the current study demonstrated that digested pig slurry is a suitable fertilizer for tomato soilless production. Digested pig slurry in peat substrate (DP) showed similar fruit yield and higher soluble sugar content compared to the mineral fertilizer treatment (MP), indicating that digested pig slurry can substitute mineral fertilizer and satisfy the nutrient requirements of tomato production. However, digested pig slurry in cinder substrate treatment (DC) also showed higher fruit yield and quality than the mineral fertilizer treatment (MC), indicating that digested slurry could be a valuable alternative to mineral fertilizers to boost fertility in poor soilless substrates. Moreover, fruit quality was also improved by digested pig slurry treatments (DP and DC), as indicated by the higher soluble sugar contents in fruits. Mineral fertilizer in cinder substrate (decreased the yield and quality) ought to be avoided during soilless cultivation. Digested pig slurry applied on peat substrate is preferable (higher yield and quality) in tomato soilless production. Future work should be carried out on a deeper analysis of the mechanism that digested slurry affects the source-sink carbon partition. The long-term effects of digested slurry application on substrate microbiota, nutrient and salt accumulation also need to be explored.

Author Contributions

Conceptualization, X.T., B.S.; formal analysis, Y.T.; investigation, Y.T.; data curation, Y.T.; supervision, X.T.; writing—original draft preparation, Y.T.; writing—review and editing, Y.T., B.S. and X.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Key Research and Development Program (2016YFD0501400), Chinese Academy of Agricultural Sciences-Agricultural Science and Technology Innovation Program (CAAS-ASTIP-IUA), and The CAAS Special Support Program for Distinguished Talents (NKYCLJ-C-2021-029).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data associated with this manuscript are included in the main manuscript.

Acknowledgments

The authors gratefully acknowledge the laboratory staff for their contributions, continued diligence, and dedication to their craft. The valuable comments of the editor and four anonymous reviewers are greatly appreciated.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02042 g001 550
Figure 1. The photosynthetic parameters of tomato leaves at 30 days of fruit age. Different superscripts in each treatment indicated significant differences at p < 0.05.
Figure 1. The photosynthetic parameters of tomato leaves at 30 days of fruit age. Different superscripts in each treatment indicated significant differences at p < 0.05.
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Agronomy 12 02042 g002 550
Figure 2. The soluble sugar and starch concentrations of tomato fruits during experimental periods (Different superscripts in each treatment or among treatments indicated significant differences at p < 0.05).
Figure 2. The soluble sugar and starch concentrations of tomato fruits during experimental periods (Different superscripts in each treatment or among treatments indicated significant differences at p < 0.05).
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Agronomy 12 02042 g003 550
Figure 3. The profiles of acid invertase (a), Sucrose synthase (b), Sucrose phosphate synthase (c), and Adenosine glucose pyrophosphorylase (AGpase) activities (d) in tomato fruit (Different superscripts in each treatment indicated significant differences at p < 0.05).
Figure 3. The profiles of acid invertase (a), Sucrose synthase (b), Sucrose phosphate synthase (c), and Adenosine glucose pyrophosphorylase (AGpase) activities (d) in tomato fruit (Different superscripts in each treatment indicated significant differences at p < 0.05).
Agronomy 12 02042 g003
Table
Table 1. Characteristics of digested pig slurry.
Table 1. Characteristics of digested pig slurry.
pHElectrical Conductivity
(ms/cm)		Total Organic Carbon
(mg/L)		N-Tot
(mg/L)		NH4+-N
(mg/L)		P-Tot
(mg/L)		K-Tot
(mg/L)
8.01 ± 0.016.88 ± 0.20213.03 ± 3.011000 ± 40813.33 ± 6.43232.5 ± 0.71697 ± 2.83
Table
Table 2. The amount of digested pig slurry and chemical fertilizer applied in the four treatments.
Table 2. The amount of digested pig slurry and chemical fertilizer applied in the four treatments.
TreatmentBase Fertilizer
(67%)		Topdressing Fertilizer 1
(33%)
DP
(Digested pig slurry +Peat substrate)		2.06 L0.35 L time−1 × 10 times
MP
(Mineral fertilizer + Peat substrate)		N: 2.06 g; P2O5: 1.91 g; K2O: 6.24 gN: 0.35 g; P2O5: 0.12 g; K2O: 0.44 g
DC
(Digested pig slurry + Cinder substrate)		5.91 L0.35 L time−1 × 10 times
MC
(Mineral fertilizer + Cinder substrate)		N: 5.91 g; P2O5: 2.60 g; K2O: 7.05 gN: 0.35 g; P2O5: 0.12 g; K2O: 0.44 g
1 Topdressing at interval of 10 days.
Table
Table 3. Effect of digested pig slurry on plant dry biomass.
Table 3. Effect of digested pig slurry on plant dry biomass.
TreatmentDry Biomass (g per Plant)
Roots Stems LeavesFruitsTotal
DP8.1 ± 3.0 ab50.2 ± 13.4 a49.7 ± 9.5 a154.1 ± 9.7 a262.1 ± 27.4 a
MP6.4 ± 2.4 b40.1 ± 2.7 a48.7 ± 5.5 a137.5 ± 4.3 a233.2 ± 7.8 a
DC11.2 ± 3.3 a38.3 ± 5.0 a40.4 ± 5.4 a95.0 ± 15.2 b185.5 ± 25.6 b
MC5.4 ± 0.8 b23.0 ± 4.6 b28.9 ± 5.1 b51.1 ± 3.2 c108.5 ± 10.0 c
Different superscripts in each row indicate significant differences at p < 0.05.
Table
Table 4. Effects of digested pig slurry on fruit yield, ripe fruit number of per plant and single fruit fresh weight.
Table 4. Effects of digested pig slurry on fruit yield, ripe fruit number of per plant and single fruit fresh weight.
TreatmentYield
(kg·m−2)		Fruit Number
(no. per Plant)		Fruit Fresh Weight
(g per Fruit)
DP6.004 ± 0.38 a11.3 ± 1.2 ab177.1 ± 8.4 a
MP5.811 ± 0.18 a13.3 ± 0.6 a145.3 ± 3.4 b
DC3.391 ± 0.54 b10.0 ± 2.0 b103.6 ± 14.3 c
MC2.223 ± 0.14 c7.7 ± 0.6 c96.7 ± 3.3 c
Significance
Fertilizer*ns*
Substrate***
Fertilizer×Substrate***
ns: not significant difference; * significant differences to Fisher’s Test at p < 0.05; Different superscripts in each row indicate significant differences at p < 0.05.
Table
Table 5. Effect of digested pig slurry on carbohydrate contents in leaves at 30-d fruit age.
Table 5. Effect of digested pig slurry on carbohydrate contents in leaves at 30-d fruit age.
TreatmentSucrose
(mg·g−1 FW)		Fructose
(mg·g−1 FW)		Glucose
(mg·g−1 FW)		Starch
(mg·g−1 FW)
DP1.0 ± 0.08 a16.4 ± 2.3 a0.3 ± 0.02 a0.8 ± 0.07 b
MP0.7 ± 0.12 b11.5 ± 2.0 b0.2 ± 0.01 b1.0 ± 0.08 ab
DC1.0 ± 0.12 a16.3 ± 1.7 a0.3 ± 0.02 a0.7 ± 0.03 b
MC0.5 ± 0.08 c8.6 ± 1.6 b0.1 ± 0.003 c1.1 ± 0.04 a
Significance
Fertilizer****
Substrate*ns*ns
Fertilizer×Substratensns**
ns: not significant difference; * significant differences to Fisher’s Test at p < 0.05; Different superscripts in each row indicate significant differences at p < 0.05.
Table
Table 6. Effect of digested pig slurry on the activities of carbohydrate metabolism enzymes in tomato leaves at 30-d fruit age.
Table 6. Effect of digested pig slurry on the activities of carbohydrate metabolism enzymes in tomato leaves at 30-d fruit age.
TreatmentSucrose Phosphate Synthase Activity
(µg·min−1·g−1 FW)		Sucrose Synthase Activity
(µmol·min−1·g−1 FW)		AGPase Activity 1
(nmol·min−1·g−1 FW)
DP348.8 ± 19.5 a241.5 ± 11.6 b77.8 ± 2.2 a
MP205.2 ± 18.3 c259.1 ± 9.4 ab65.2 ± 1.6 c
DC281.7 ± 10.2 b269.9 ± 11.6 a70.2 ± 0.2 b
MC262.7 ± 38.4 b182.1 ± 14.6 c63.3 ± 1.8 c
Significance
Fertilizer***
Substratens**
Fertilizer×Substrate**ns
ns: not significant difference; * significant differences to Fisher’s Test at p < 0.05; Different superscripts in each row indicate significant differences at p < 0.05. 1: adenosine glucose pyrophosphorylase.
Table
Table 7. Effect of digested pig slurry on carbon supply flux of fruits.
Table 7. Effect of digested pig slurry on carbon supply flux of fruits.
TreatmentCarbon Supply Flux (g C/day)
0–20 days20–30 days30–40 days40–50 days
DP0.04 ± 0.005 e0.18 ± 0.02 c0.26 ± 0.01 b0.39 ± 0.10 a
MP0.03 ± 0.004 e0.16 ± 0.01 cd0.23 ± 0.03 bc0.13 ± 0.06 bcd
DC0.03 ± 0.006 e0.16 ± 0.02 cd0.14 ± 0.02 bcd0.11 ± 0.03 d
MC0.02 ± 0.003 e0.09 ± 0.03 de0.15 ± 0.01 bcd0.16 ± 0.03 cd
Different superscripts in each treatment or among treatments indicated significant differences at p < 0.05.
Table
Table 8. Pearson’s correlation coefficients among the carbohydrate contents and the activities of carbohydrate enzymes in tomato fruit during experimental periods.
Table 8. Pearson’s correlation coefficients among the carbohydrate contents and the activities of carbohydrate enzymes in tomato fruit during experimental periods.
TreatmentFruit Dry
Weight		Soluble Sugar
Content		Starch
Content		AISPSSusyAGPase
Fruit dry weight1
Soluble sugar content0.876 **1
Starch content−0.560 *−0.516 *1
AI0.874 **0.882 **−0.596 *1
SPS−0.326−0.1800.0170.0151
Susy−0.685 **−0.632 **0.635 **−0.579 *0.4001
AGPase−0.666 **−0.613 *0.548 *−0.562 *0.4500.870 **1
Correlation was significant at * p < 0.05; ** p < 0.01. AI: acid invertase activity; SPS: Sucrose phosphate synthase activity; Susy: Sucrose synthase activity; AGPase: adenosine glucose pyrophosphorylase.
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Teng, Y.; Shang, B.; Tao, X. Effects of Digested Pig Slurry on Photosynthesis, Carbohydrate Metabolism and Yield of Tomato (Solanum lycopersicum L.). Agronomy 2022, 12, 2042. https://doi.org/10.3390/agronomy12092042

AMA Style

Teng Y, Shang B, Tao X. Effects of Digested Pig Slurry on Photosynthesis, Carbohydrate Metabolism and Yield of Tomato (Solanum lycopersicum L.). Agronomy. 2022; 12(9):2042. https://doi.org/10.3390/agronomy12092042

Chicago/Turabian Style

Teng, Yunfei, Bin Shang, and Xiuping Tao. 2022. "Effects of Digested Pig Slurry on Photosynthesis, Carbohydrate Metabolism and Yield of Tomato (Solanum lycopersicum L.)" Agronomy 12, no. 9: 2042. https://doi.org/10.3390/agronomy12092042

APA Style

Teng, Y., Shang, B., & Tao, X. (2022). Effects of Digested Pig Slurry on Photosynthesis, Carbohydrate Metabolism and Yield of Tomato (Solanum lycopersicum L.). Agronomy, 12(9), 2042. https://doi.org/10.3390/agronomy12092042

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