Next Article in Journal
Improved Tunicate Swarm Optimization Based Hybrid Convolutional Neural Network for Classification of Leaf Diseases and Nutrient Deficiencies in Rice (Oryza)
Previous Article in Journal
Comparative Physiological and Gene Expression Analyses Provide Insights into Ion Transports and Osmotic Adjustment of Sweet Sorghum under Salt Stress
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 14
Issue 8
10.3390/agronomy14081850
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Exogenous Hemin Increases the Yield, Phenolic Compound Content, and Antioxidant Enzyme Activity of Dragon Fruit during the High-Temperature Period

by
Minmin Sun
1,
Aaqil Khan
1,
Jiahui Wang
1,
Linchong Ding
1,
Xiaohui Yang
1,
Jian Xiong
1,
Zhiyuan Sun
1,
Naijie Feng
1,2,* and
Dianfeng Zheng
1,2,*
1
College of Coastal Agriculture Sciences, Guangdong Ocean University, Zhanjiang 524088, China
2
South China Center of National Saline-Tolerant Rice Technology Innovation, Zhanjiang 524088, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(8), 1850; https://doi.org/10.3390/agronomy14081850 (registering DOI)
Submission received: 2 August 2024 / Revised: 18 August 2024 / Accepted: 20 August 2024 / Published: 21 August 2024
(This article belongs to the Section Horticultural and Floricultural Crops)
Browse Figures
Versions Notes

Abstract

:
Dragon fruits have abundant nutritional and antioxidant properties. High temperatures limit the growth and production of dragon fruits. Hemin can effectively alleviate abiotic stress in plants. However, the regulatory effect of Hemin on dragon fruit under heat stress remains unclear. In this study, we explored the impacts of foliar application of Hemin on dragon fruit size, yield and quality during the high temperatures of the summer season. In this experiment, dragon fruit variety ‘Jindu No. 1’ was used as material and treated with three Hemin concentrations, i.e., H1: 1 μmol.L−1, H2: 10 μmol.L−1, H3: 100 μmol.L−1, compared with CK: control. The results show that exogenous Hemin increased the single fruit weight, yield, fruit shape index and edible rate. It also improved pericarp L* value, a* value, C* and decreased ho, improving the peel colour; exogenous Hemin enhanced soluble solids content and phenolic compounds content and antioxidant enzyme activities in the pulp of dragon fruit. In addition, exogenous Hemin increased the content of chlorophyll content in dragon fruit stems. Differential metabolites determined by metabolomic assay also indicated that Hemin significantly increased the content of active substances such as selagin. Additionally, the Hemin treatment H2 also activated the activity of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX), which helps to mitigate the effects of high temperatures on dragon fruit. The current findings strongly advocate that H2 treatment may effectively counteract the adverse effects of heat stress by regulating the morph-physiological and antioxidant traits.

1. Introduction

Dragon fruit (Hylocereus polyrhizus), commonly known as dragon fruit or pitahaya, belongs to the cactus family (Cactaceae), native to the tropical regions of Mexico, Central and South America [1]. Dragon fruit is one of the vital sources of antioxidants. Regular consumption of dragon fruit prevents anemia [2], reduces blood glucose [3], prevents cancer and has anti-aging [4], anti-inflammatory and antibacterial properties [5]. As a result of the above-mentioned values of dragon fruit species as crop plants and the rich nutritional characteristics of the fruit, interest in these varieties is increasing all over the world [6]. The nutritional and food value increased demand for dragon fruit, and its cultivation area in China rapidly expanded, but there is less information about the dragon fruit pulp composition [7]. The high temperatures in the Guangdong region during August had a great impact on agriculture production [8]. A high temperature leads to yellowing of stalks, unfavorable pistil and fruit formation, and finally affects the yield and quality of dragon fruit [9]. In order to improve the economic returns and nutritional value of dragon fruit, it is important to perform research to identify the mechanism of enhancing crop yield and nutritional quality during the high temperatures of the summer season.
Dragon fruit is rich in antioxidant and phenolic substances [10]. It is the product of secondary metabolic processes and has the common structure of aromatic rings with one or more hydroxyl substituents [11], which directly affects the quality of plants [12]. Natural antioxidants include flavonoids, phenols and anthocyanins [13]. The dragon fruit is mainly associated with the presence of flavonoid and phenol compounds [14]. The human body itself cannot synthesis polyphenols and needs to consume them from other external sources [15]. Phenolic substances are the major secondary metabolites found in fruits and largely contribute to the fruit’s antioxidant capabilities [16,17].
The antioxidant system is composed of enzymatic and non-enzymatic activities [18]. The enzymatic antioxidant system consists of a series of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX), which is an important enzyme system that scavenges reactive oxygen species and inhibits oxidative reactions in tissues [19]. Under various abiotic stress conditions, heme seed can increase SOD, POD, CAT and APX activities in wheat [20].
Plant growth regulators are widely used to improve plant stress tolerance, regulate plant nutrient growth and improve fruit quality [21].
Hemin is also known as methemoglobin chloride, iron chloride porphyrin and methemoglobin. Hemin is widespread in nature and is an important component of hemoglobin [22]. Hemin consists of a ferrous ion and a large central heterocyclic ring called a porphyrin, which connects the four porphyrin rings through a hypomethyl bond [23,24]. Hemin can be isolated and purified from animal blood or synthesised artificially [25]. In plants, Hemin acts as a bioregulator with multiple biological functions [26]. In recent years, researchers have begun to focus on exploring the role of Hemin in horticultural and field crops [27]. Hemin treatment enhanced photosynthesis and increased yield in maize [28]. Hemin treatment increased anthocyanin content and nutritional value of strawberries [29]. In addition, Hemin treatment can promote soybeans’ lateral roots [30] and cucumber adventitious roots [25]. Hemin treatment increased SOD, POD, CAT and APX activities in rice under salt stress [20]. However, there are few studies on the application of plant growth regulators in dragon fruit production, and even fewer studies on Hemin in dragon fruit.
The objective of this study was to investigate the effects of different concentrations of Hemin on the yield, phenolic compounds and antioxidant enzyme activities of dragon fruit during the high temperatures of the summer season in Guangdong Province, and to find the appropriate concentrations for improving the yield, quality and antioxidant activities of dragon fruit. This is also the first time that Hemin, a novel plant growth regulator, has been applied to dragon fruit.

2. Materials and Methods

2.1. Plant Material

The dragon fruits were obtained from the dragon fruit experimental base in Bu Chao Village, Suixi, Zhanjiang City (located at longitude 110°46′ E, latitude 21°10′ N), and the plants were 5-year-old “Jindu No. 1”, which were planted in rows, with a spacing of 0.4 m × 2.5 m, and were about 1000 plants per mu of land. Except for the spraying of different treatments of regulators, all experimental plants were subjected to uniform cultivation measures, including fertiliser application, plant protection and irrigation.

2.2. Design of the Experiment

This experiment was carried out on 4 August 2023, with dragon fruit plants on the third day of stamen appearance as the test material, and the plant growth regulator Hemin (supplied by Shanghai Changdeto Agricultural Science and Technology Co., Ltd., Shanghai, China) was designed in three concentrations: H1 (1 μmol.L−1), H2 (10 μmol.L−1), and H3 (100 μmol.L−1). CK (clear water) was used as the control. The whole plant was sprayed on the front and back until the plant dripped. Twelve plants were treated for each concentration, and three replications were set up. In total, there were four treatments and 144 plants. The fruits were harvested (18 September 2023) after all the peel colours had turned red and quickly transported back to the laboratory for analysis and determination.

2.3. Determination of Morphological Indicators of Fruit

Ten fruits were taken from each treatment for the following indices (except yield) [31]. The fruit pulp weight and single fruit weight were determined by weighing with an electronic balance. Edible rate (%) = the fruit pulp weight/fruit weight × 100%, and yield in this paper refers to the total single fruit weight of 12 plants in one treatment; vernier callipers were used to determine the maximum distance of the transverse direction of the fruit for the transverse diameter, the maximum distance of the longitudinal direction of the fruit for the longitudinal diameter of the fruit; and the fruit shape index = the longitudinal diameter of fruit/the transverse diameter of fruit.

2.4. Determination of Peel Colour Index

In this study, the skin colour of dragon fruit was identified using a Konica Minolta CR-400 colorimeter (Konica Minolta Sensing, Inc., Osaka, Japan). Ten fruits were measured for each treatment, five points were taken along the equator of the fruits, and the average value was taken and recorded [32]. The illuminance and viewing angle were previously calibrated at D65 and 10°, respectively. L*, a* and b* parameters were calculated according to the CIELab colour scale. Red saturation/green saturation (a*/b*), hue (h°) and chroma (C*) angles defining hue and intensity were also calculated. C* = (a*2 + b*2)0.5; h° = arctan (b*/a*).

2.5. Determination of Fruit Nutritional Indicators

Soluble solids content was determined by a digital refractometer (PAL-1, ATAGO, Osaka, Japan); soluble proteins were determined with the Thomas Brilliant Blue G-250 staining method by Campion et al. [33]. The starch and sucrose contents were determined by the method of Kuai et al. [34,35] and Nayyar Du et al. [36,37]. Total phenols, total flavonoids and total anthocyanins were determined by the method of Pirie and Zeraik et al. [38,39], with slight modifications, using 1% HCl-methanol ice bath extraction, for each gram of fresh weight of the sample. The total phenolics and flavonoids were expressed as the absorbance values at 280 nm and 325 nm, respectively, and the anthocyanins were expressed as the difference between the absorbance values at 530 nm and 650 nm in units of ΔOD280/g, ΔOD325/g, and U/g FW.

2.6. Determination of Enzyme Activities Related to the Antioxidant System of the Fruit Pulp

Enzyme liquid extraction was carried out as follows: fruit pulp (0.5 g) was ground with liquid nitrogen, and 10 mL of pre-cooled phosphate buffer (50 mmol L−1; PH 7.8) was added in three portions, ground well, poured into a centrifuge tube and centrifuged for 20 min at 4 °C and 10,000× g. The supernatant was collected to determine the activity of catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), and ascorbate peroxidase (APX). Enzyme activity assay: the SOD activity was determined according to Giannopolities and Bewley et al. [40,41]. The POD activity was determined according to the method of Klapheck [42]. CAT activity was determined according to Gupta et al. [43] and Li et al. [44]. APX activity was determined according to the method of Nakano et al. [45].

2.7. Determination of Chlorophyll Content of Dragon Fruit Stems

After two weeks of treatment, stalks of the same height from the ground and of the same year were collected with a 0.86 cm diameter perforator (Tingshi Yi E-commerce Co., Ltd., Suqian, China)to test for chlorophyll content. A total of 0.5 g of stalks was weighed into a 15 mL test tube and 10 mL of anhydrous ethanol was added for extraction. The tubes were placed in a dark environment for about 48 h until the stalks turned white and Chl was completely leached out. The absorbance of the extracted solution at 470, 649 and 665 nm was measured using an enzyme marker (Epoch, BioTek Instruments, Winooski, Vermont, United States), and the chlorophyll a (Chla), chlorophyll b (Chlb), total chlorophyll (Chl), and carotenoid (Carotenoids) contents were calculated [46].
Chla (mg.g−1) = 13.95A665 − 6.88A669
Chlb (mg.g−1) = 24.96A665 − 7.32A669
Chl (mg.g−1) = Chla + Chlb
Carotenoids (mg.g−1) = (1000A470 − 2.05 Chla − 114.8 Chlb)/245

2.8. Metabolomic Measurements

The metabolomic assay was carried out by Wuhan Metaviral Biotechnology Company, according to the previous analysis method [47]. Sample preparation: The pulp was freeze-dried, ground, added to the pre-cooled extraction solution (50% methanol containing 0.1% HCl) and centrifuged at 12,000 rpm for 3 min. The supernatant was collected for ultra-performance liquid chromatography tandem mass spectrometry (UPLC—MS/MS) analysis. Phenolic compounds were qualitatively and quantitatively analysed by mass spectrometry based on a software database (MWDB) (V4.4). Hierarchical Cluster Analysis (HCA) was performed to analyse the accumulation pattern of metabolites among different samples by plotting heat maps with the R software (2.9.4) ComplexHeatmap package. Pearson’s Correlation Coefficient r (Pearson’s Correlation Coefficient) was used as an assessment index for biological repeat correlation. Metabolites with a fold change ≥1.5 and a fold change ≤ 0.8 were selected as candidate differential metabolites, and the differential metabolites were annotated using the KEGG database.

2.9. Data Analysis

Three replicates were set for each treatment, expressed as mean ± standard error. Experimental data were processed using SPSS 26.0 software; Student’s t-test and Duncan’s multiple comparison test were used for statistical comparison and significant analysis [48]; graphing was performed using Origin 2021; and correlation analysis was performed using Pearson’s method. The results were expressed as three replicates of data.

3. Results

3.1. Effects of Hemin on Morphological Traits of Dragon Fruits

Dragon fruit illustrated different responses against the three concentration of Hemin. Hemin markedly influenced the morphological traits of dragon fruits (Table 1). The fruit weight and edible rate were improved by 12.99% and 7.16% in H1, 21.07% and 11.30% in H2, and 12.89% and 10.45% in H3, respectively, compared to CK.
The dragon fruit yield was significantly enhanced by 13.81% and 11.63%, respectively, for H2 and H3 treatments, compared to CK. Similarly, the fruit shape index was markedly increased by 3.92%, 4.96% and 7.05%, respectively, in H1, H2 and H3 treatments, compared to CK. H1, H2 and H3 treatments increased the transverse and longitudinal diameters of fruits, compared to CK.

3.2. Effects of Hemin Treatment on the Peel Colour Index

The effects on the peel colour index were explored by exogenously spraying three concentrations of Hemin. It was found that there was a positive effect on peel colour indices under certain concentration of Hemin treatments, especially H2 treatment, which significantly affected the L*, C* and h° of the peel (Figure 1A,E,F). The peel L* value, a* value, a*/b* and C* were, respectively, increased by 1.06%, 1.60%, 5.36% and 2.99% in H1 treatment, compared to CK (Figure 1A,B,D,E); the values of L*, a*, b*, a*/b* and C* were increased by 2.24%, 2.41%, 10.53%, 1.58% and 3.23%, while h° significantly was decreased by 4.72% for H2 treatment, respectively, compared to CK (Figure 1A–F); L* value and h° were increased by 1.15% and 1.47%, respectively, for H3 treatment (Figure 1A,F), while a* value, b* value, a*/b*, and C* were decreased by 1.5%, 1.68%, 3.62%, and 0.93%, respectively (Figure 1B–E), compared to CK.

3.3. Effects of Hemin Treatment on Fruit Nutritional Indices

3.3.1. Effect of Hemin Treatment on Soluble Solids, Soluble Protein, Starch and Sucrose

Three concentrations of Hemin treatments increased the soluble solids content of dragon fruit; especially H2 had a significant effect (Figure 2A). The soluble solids content was increased by 6.61%, 9.53% and 6.23%, respectively, in H1, H2 and H3, compared to CK.
The soluble protein of dragon fruit increased and then decreased with increasing Hemin treatment concentration (Figure 2B). It was significantly increased by 7.24%, 11.77% and −15.34% for H1, H2 and H3 treatments, respectively, compared to CK.
The different concentrations of treatments had significant effects on starch and sucrose content of dragon fruit pulp (Figure 2C,D). The starch content was significantly increased by 12.07% in H2 treatment and was significantly decreased by 7.06% and 8.17% in H1 and H3 treatments, respectively, compared with CK. The sucrose content was significantly increased by 11.50% and 30.58% in H1 and H2 treatments, respectively, while it was significantly decreased by 1.90% in H3 treatment, compared to CK.

3.3.2. Effects of Hemin Treatment on the Phenolic Content of Dragon Fruit

The total phenolic content of dragon fruit pulp was increased by 24.82% in H2 treatment, while it was decreased by 39.46% and 21.36%, respectively, for H1 and H3 treatments, compared to CK (Figure 3A).
As the concentration of Hemin treatment increased, the flavonoid content of dragon fruit was increased by 12.56% and 86.64% in H1 and H2 treatments, respectively, compared to CK (Figure 3B). The effect was significant and maximum in H2 treatment, and the flavonoid content was decreased by 2.17% in H3 treatment, compared to CK (Figure 3B).
The anthocyanin content of dragon fruit was increased by 1.26% and 13.44% in H1 and H2 treatments, respectively, while it was decreased by 23.61% in H3 treatment, compared to CK (Figure 3C).

3.4. Effects of Hemin Treatment on Antioxidant Enzyme Activities of the Pulp of Fruit

The effects on antioxidant enzyme activities of dragon fruit pulp were investigated by exogenously spraying different concentrations of Hemin. Compared with CK, the activities of POD, SOD, APX and CAT enzymes of dragon fruit pulp were first increased and then decreased with the increasing concentration of Hemin treatment (Figure 4). The activities of antioxidant enzymes (POD, SOD, APX, CAT) (except for the insignificant increase in APX in H1) were significantly enhanced in H1 and H2 treatments, while there was no significant effect on the activities of these four enzymes in H3 treatment. The results show that Hemin markedly influenced the antioxidant system of dragon fruit pulp. They were all enhanced in H2 treatment especially.

3.5. Effect of Hemin Treatment on Chlorophyll Content of Dragon Fruit Stems

In order to further investigate the effect of Hemin treatment on the chlorophyll content of dragon fruit stems, we selected H2 and CK treatments for the determination of chlorophyll content. The results show that the chlorophyll a, chlorophyll b, total chlorophyll and carotenoid content were significantly increased by 18.98%, 30.60%, 21.85% and 24.89% for H2 treatment, respectively, compared to CK (Figure 5A–D).

3.6. Analysis of Metabolomic Differences

In order to have a clearer understanding of the changing pattern of polyphenols in different treatments, 407 metabolites were determined in this study by the UPLC-MS/MS platform, all of which included 191 phenolic acids, 166 flavonoids, 44 lignans and coumarins, 2 stilbenes, and 4 tannins, and the 407 metabolites were detected in all the samples. Flavonoids and phenolic acids were the main phenolics in dragon fruit pulp, and flavonols and flavones were the main flavonoids (Figure 6A).
In order to show more intuitively the relationship between CK and H2 and the differences in the expression of metabolites among different samples, we performed a hierarchical cluster analysis of the expression levels of all significantly different metabolites (Figure 6B). The results of the cluster heatmap analysis show that there were significant differences in the substances in different groups, which were divided into two clusters in total. The metabolites in cluster 1 were high in group H2, of which 11 were flavonoids, ac-counting for 61.1%; 4 were phenolic acids, accounting for 22.2%, and 3 were lignans and coumarin, accounting for 16.6%. Metabolites in cluster 2 were high in CK group, in which 29 were flavonoids, accounting for 69.0% as the highest; 9 were lignans and coumarins, accounting for 21.4%, medium; 3 were phenolic acids, accounting for 7.1%, and 1 was a stilbene, accounting for 2.3% as the lowest. Overall, both cluster and statistical analyses showed that the metabolites in CK and H2 produced significant differences. Eighteen up-regulated differential metabolites contained 11 flavonoids, 4 phenolic acids, and 3 lignans and coumarins. The different biological replicates clustered equally among themselves, indicating good homogeneity among biological replicates and high reliability of the data. The top six differential metabolites screened from differential metabolites in the up- and down-regulation of Log2 FC values were as follows: selagin, apigenin-7-O-(6″-malonyl) glucoside, kaempferol-3-O-(6″-O-acetyl)- glucoside,saccharin-3′-O-glucoside, phenylpropionic acid-O-β-D-glucopyranoside, dihydroneplanocarpine and 5,2′-dihydroxy-7,8-dimethoxyflavone-glucoside, ruderaldehyde-guaiacylglycerol-β-O-4′-dihydropinosyl ether glucoside, eucalyptol A, 2,3,5, 4′-tetrahydroxystilbene-2-O-glucoside, rhamnolimonene-3-O-(4″-O-glucosyl)glucoside-4′-O-gluco-side, and 6-hydroxy-7-methoxycoumarin. The top six up-regulated were five flavonoids and one phenolic acid, and the top six down-regulated were two flavonoids, three lignans and coumarins, and one astragalus. The results show that the content of phenolic metabolites in the pulp changed more significantly under H2 treatment, and the accumulation of selagin, apigenin-7-O-(6″-malonyl) glucoside, kaempferol-3-O-(6″-O-acetyl) glucoside, saccharin-3′-O-glucoside, phenylpropanoic acid-O-β-D-glucopyranoside, and dihydroneplanocarpene also increased significantly. H2 treatment was favourable to increase the accumulation of these phenolics in dragon fruit pulp.
OPLS-DA analysis is a multivariate statistical analysis method with supervised pattern recognition, which is able to effectively exclude effects that are not relevant to the study, thereby screening out differential metabolites. As shown in Figure 7A,B, in this model, R2 X and R2 Y denote the explanatory rate of the constructed model for the X and Y matrices, which were 29.5% and 27.1%, respectively. Q2 denotes the predictive power of the model, and the Q2 of this figure was greater than 0.5, indicating the appropriateness of the constructed model. The results show that a significant separation between H2 and CK occurred and the data were reproducible and reliable.

3.7. Correlation Analysis

In order to reveal the correlation between dragon fruit yield, quality and photosynthetic pigments under Hemin treatment, the analysis was carried out by using ChiPlot (https://www.chiplot.online/correlation_heatmap.html), as shown in Figure 8, which shows that all indicators were positively correlated. Based on the degree of strength, the correlations can be categorised as low (0.31–0.50), medium (0.51–0.70), strong (0.71–0.90) and very strong (0.91–1.0) [49]. Of these, 20.3% were moderate and 45.3% were very strong correlations, which ensures the reliability of the analysis.

4. Discussion

Hemin is both a substrate and promoter of HO-1 and induces HO-l expression [50]. Application of Hemin treatments increased the single fruit weight, yield, palatability, transverse diameter, longitudinal diameter and fruit shape index of dragon fruit, probably due to the activation of heme oxygenase (HO) to enhance the accumulation of dragon fruit biomass by protecting the light-sensitive pigments and thus increasing the chlorophyll content and enhancing the photosynthetic capacity. Similar results were found in maize [51], mung bean [52], rice [22,53] and oilseed rape [54]. The trends of changes in peel colour and pulp anthocyanin content in this study are consistent with previous studies in which spraying plant growth regulators improved peel colour by increasing anthocyanin accumulation in fruits [55]. It is possible that Hemin treatment increased the anthocyanin content of dragon fruit pulp, which in turn increased the peel L* value, a* value, b* value, a*/b*, C* and decreased ho, thus making the peel show a redder and brighter colour, whereas too high a concentration of H3 may not be conducive to the accumulation of anthocyanins and thus impact the peel colour [29]. Elevated L* values, a* values and reduced ho imply a higher value of dragon fruit, which is consistent with the results of Shattir et al. [56].
Total soluble solids are the main edible quality of fruit, and an increase in soluble solids content is a good indicator of fruit ripeness and flavour [57]. Previous studies have shown that red-fleshed dragon fruit is softer and sweeter when the soluble solids content is less than 15% and above 12% in the pulp of the fruit [58]. In the study, the soluble solids content in dragon fruit was increased (Figure 2A), and the content was above 16%, which may be caused by the different dragon fruit varieties and planting areas. The increase in total sugar content during fruit ripening was also dependent on sucrose accumulation [59]. Zhao et al. [51] found that Hemin treatment promoted sucrose accumulation in maize, which is consistent with the result that sucrose content of dragon fruit pulp was significantly higher in Hemin-treated fruit than in CK in this study (Figure 2D).
Phenolic compounds are among the endogenous free radical scavenging antioxidants in fruits [60], which can attenuate oxidative stress and protect cellular structures from damage under the influence of external stresses and elicitors [61], contributing to antioxidant capacity enhancement [62], which plays an important role in plant development and stress defence. It has been suggested that phenolic compounds may be the major antioxidants in papaya [63]. Usually, extracts with high phenolic content have higher antioxidant and cytotoxic activities [64,65]. In the present study, the contents of total phenols, flavonoids and anthocyanins were increased by Hemin treatments (Figure 3A–C), which is consistent with the results of previous studies in maize [66] and strawberry [29]. Phenolics during fruit ripening varied among fruits, and these variations could be due to a number of different factors such as variety, stage of ripening, soil and climatic conditions, management practices, and extraction conditions [67]. The higher content of phenolic compounds in the pulp of dragon fruit results in its exhibiting higher antioxidant activity [68].
SOD is capable of scavenging superoxide radicals (O2−) to form H2O2, which acts in synergy with enzymes such as CAT and POD to defend against damage to the cell membrane system by reactive oxygen species and other peroxide radicals, and APX is involved in regulating H2O2 as a signalling molecule that reduces H2O2 [69]. That the application of Hemin in Chinese cabbage increased the activities of SOD, POD, CAT and APX and repaired the damage caused by reactive oxygen species to the cells under cadmium stress was found by the study of Zhu et al. [70]; exogenous hematin increased the activities of SOD and POD in alfalfa roots [71]; exogenous hemin treatment increased the activities of APX, SOD, and POD in mung bean seedlings [52]; and Hemin seed can increase SOD, POD, CAT, and APX activities in wheat [17]. In this study, the SOD, POD, CAT and APX activities of dragon fruit pulp treated with Hemin (except H3) were significantly higher than those of the control (Figure 4), which laterally proved that Hemin treatment improved the tolerance of dragon fruit to stress and could delay senescence. It may be that the enzymatic antioxidant system can effectively inhibit the accumulation of ROS in fruits and reduce oxidative damage, thus playing a key role in the inhibition of fruit senescence [72].
Selagin belongs to a group of flavonoids with significant antioxidant activity, thymus growth stimulation, and antimicrobial properties [73]. Ren et al. [74] showed that flavonoids are the main active constituents of cypress and have anticancer effects. Bailly et al. [75] found that the flavonoids in cypress have medical and cosmetic applications. The presence of compounds with antioxidant, anti-inflammatory and immunomodulatory properties in cypress extracts has also been demonstrated [76]. In the study, significant changes in the content of selagin were found in Hemin treatments, with the greatest rate of increase. The mechanism by which Hemin treatment increases the synthesis of coniferin can be analysed in conjunction with the transcriptome in the future.
Some studies have shown that high chlorophyll content favours light absorption, thus increasing photosynthesis [77]. Heme oxygenase-1 (HO-1) protects phytochrome and promotes chlorophyll synthesis, and Hemin induces the expression of heme oxygenase-1 (HO-1), thus increasing plant chlorophyll content and biomass [78]. The correlation analysis in this study showed that photosynthetic pigments were promoted with yield, phenolic content, antioxidant enzyme activity and the fruit nutritional index content of dragon fruit, and it also showed a very strong correlation with yield and flavonoid content (Figure 8). This indicates that Hemin treatment protects phytochrome, increases the chlorophyll content in the stems, promotes photosynthesis, and ultimately enhances the yield and quality of dragon fruit.

5. Conclusions

In this study, we investigated the effects of Hemin, a novel plant growth regulator, on dragon fruit in high summer temperatures in Guangdong. It confirmed that Hemin treatment could improve the morphological index of dragon fruit and, especially, increase the yield, edible rate and fruit shape index of dragon fruit; it could also improve the nutritional quality of dragon fruit, and especially and significantly increase the content of sucrose, starch, and flavonoids. The Hemin treatment also significantly increased the activities of antioxidant enzymes (SOD, POD, CAT and APX) in the pulp of dragon fruits, which is conducive to the improvement of stress tolerance. As analysed by UPLC-MS/MS, Hemin treatment increased the content of selagin in the pulp of dragon fruit, which is beneficial for improving photosynthesis in the plant and enhancing fruit quality. In conclusion, the effect of Hemin application on dragon fruit is positive, especially the H2 concentration treatment. Future studies will further optimize its application strategy and explore its intrinsic deeper mechanism of action through joint analysis with transcriptome, so as to provide a scientific basis for agricultural production.

Author Contributions

Conceptualization, D.Z. and N.F.; methodology, D.Z., N.F. and M.S.; software, M.S., X.Y., J.X., L.D. and Z.S.; validation, M.S., Z.S. and X.Y.; formal analysis, M.S. and L.D.; investigation, M.S., L.D., X.Y., J.W. and A.K.; writing—original draft preparation, M.S.; writing—review and editing, Z.S., A.K. and J.W.; supervision, D.Z.; funding acquisition, D.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by Research and development of meteorological disaster prevention and control technology and Product creation of major economic crops (300702A20059).

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Acknowledgments

We thank the local landowners and Yang Chengkun for the overall support.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Shah, K.; Chen, J.; Chen, J.; Qin, Y. Pitaya nutrition, biology, and biotechnology: A review. Int. J. Mol. Sci. 2023, 24, 13986. [Google Scholar] [CrossRef]
  2. Widyaningsih, A.; Setiyani, O.; Umaroh, U.; Sofro, M.A.U.; Amri, F. Effect of consuming red dragon fruit (hylocereus costaricensis) juice on the levels of hemoglobin and erythrocyte among pregnant women. Belitung Nurs. J. 2017, 3, 255–264. [Google Scholar]
  3. Holanda, M.O.; Lira, S.M.; Silva, J.Y.G.D.; Marques, C.G.; Coelho, L.C.; Lima, C.L.S.; Costa, J.T.G.; Silva, G.S.D.; Santos, G.B.M.; Zocolo, G.J.; et al. Intake of pitaya (Hylocereus polyrhizus (f.a.c. Weber) britton & rose) beneficially affects the cholesterolemic profile of dyslipidemic c57bl/6 mice. Food Biosci. 2021, 42, 101181. [Google Scholar]
  4. Luo, H.; Cai, Y.; Peng, Z.; Liu, T.; Yang, S. Chemical composition and in vitroevaluation of the cytotoxic and antioxidant activities of supercritical carbon dioxide extracts of pitaya (dragon fruit) peel. Chem. Cent. J. 2014, 8, 1. [Google Scholar] [PubMed]
  5. Tischer, B.; Pangloli, P.; Nieto-Veloza, A.; Reeder, M.; Dia, V.P.; Sarker, U. Bioactive compounds, antioxidant capacity and anti-inflammatory activity of native fruits from brazil. PLoS ONE 2023, 18, e285625. [Google Scholar]
  6. Carrillo Salazar, J.A.; Ortiz Hernández, Y.D. Pitahaya (Hylocereus spp.): A short review. Comun. Sci. 2012, 3, 220–237. [Google Scholar]
  7. Angonese, M.; Motta, G.E.; de Farias, N.S.; Molognoni, L.; Daguer, H.; Brugnerotto, P.; de Oliveira Costa, A.C.; Olivera Muller, C.M. Organic dragon fruits (Hylocereus undatus and Hylocereus polyrhizus) grown at the same edaphoclimatic conditions: Comparison of phenolic and organic acids profiles and antioxidant activities. LWT-Food Sci. Technol. 2021, 149, 111924. [Google Scholar]
  8. Yaodong, D.; Ruijun, H.; Hongyu, W. Characteristics and Impact of Weather and Climate in Guangdong Province from July to August 2023. Guangdong Meteorol. 2023, 5, 45. [Google Scholar]
  9. Chu, Y.; Chang, J. High temperature suppresses fruit/seed set and weight, and cladode regreening in red-fleshed ‘da hong’ pitaya (Hylocereus polyrhizus) under controlled conditions. Hortscience 2020, 55, 1259–1264. [Google Scholar]
  10. Paśko, P.; Galanty, A.; Zagrodzki, P.; Ku, Y.G.; Luksirikul, P.; Weisz, M.; Gorinstein, S. Bioactivity and cytotoxicity of different species of pitaya fruits—A comparative study with advanced chemometric analysis. Food Biosci. 2021, 40, 100888. [Google Scholar]
  11. Valcarcel, J.; Reilly, K.; Gaffney, M.; O Brien, N.M. Antioxidant activity, total phenolic and total flavonoid content in sixty varieties of potato (Solanum tuberosum L.) Grown in ireland. Potato Res. 2015, 58, 221–244. [Google Scholar]
  12. Rytel, E.; Tajner-Czopek, A.; Kita, A.; Aniołowska, M.; Kucharska, A.Z.; Sokół-Bętowska, A.; Hamouz, K. Content of polyphenols in coloured and yellow fleshed potatoes during dices processing. Food Chem. 2014, 161, 224–229. [Google Scholar] [PubMed]
  13. Eghbaliferiz, S.; Iranshahi, M. Prooxidant activity of polyphenols, flavonoids, anthocyanins and carotenoids: Updated review of mechanisms and catalyzing metals. Phytother. Res. 2016, 30, 1379–1391. [Google Scholar]
  14. Chen, Z.; Zhong, B.; Barrow, C.J.; Dunshea, F.R.; Suleria, H.A.R. Identification of phenolic compounds in australian grown dragon fruits by lc-esi-qtof-ms/ms and determination of their antioxidant potential. Arab. J. Chem. 2021, 14, 103151. [Google Scholar]
  15. Guan, H.; Zhang, W.; Sun-Waterhouse, D.; Jiang, Y.; Li, F.; Waterhouse, G.I.N.; Li, D. Phenolic-protein interactions in foods and post ingestion: Switches empowering health outcomes. Trends Food Sci. Technol. 2021, 118, 71–86. [Google Scholar]
  16. Tao, X.; Wu, Q.; Li, J.; Huang, S.; Cai, L.; Mao, L.; Luo, Z.; Li, L.; Ying, T. Exogenous methyl jasmonate regulates phenolic compounds biosynthesis during postharvest tomato ripening. Postharvest Biol. Technol. 2022, 184, 111760. [Google Scholar]
  17. Bovy, A.G.; Schijlen, E.G.W.M.; Hall, R.D. Metabolic engineering of flavonoids in tomato (Solanum lycopersicum): The potential for metabolomics. Metabolomics 2007, 3, 399–412. [Google Scholar]
  18. Ren, R.; Li, Z.; Zhang, L.; Zhou, H.; Jiang, X.; Liu, Y. Enzymatic and nonenzymatic antioxidant systems impact the viability of cryopreserved paeonia suffruticosa pollen. Plant Cell Tissue Organ Cult. 2021, 144, 233–246. [Google Scholar]
  19. Munné-Bosch, S.; Queval, G.; Foyer, C.H. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol. 2013, 161, 5–19. [Google Scholar] [PubMed]
  20. Xu, S.; Lou, T.; Zhao, N.; Gao, Y.; Dong, L.; Jiang, D.; Shen, W.; Huang, L.; Wang, R. Presoaking with hemin improves salinity tolerance during wheat seed germination. Acta Physiol. Plant. 2011, 33, 1173–1183. [Google Scholar]
  21. Zhao, M.; Li, J.; Shi, X.; Sanaullah Malik, M.; Quan, Y.; Guo, D.; Wang, L.; Wang, S. Effects of exogenous plant regulators on growth and development of “kyoho” grape under salt alkali stress. Front. Plant Sci. 2023, 14, 1274684. [Google Scholar]
  22. Meng, F.; Guo, J.; Feng, N.; Zheng, D.; Chen, X.; Chen, Z.; Jiang, H.; Jiang, X. Beneficial effects of hemin on antioxidative capacity and anatomical characters of nacl-stressed rice plants. J. Plant Growth Regul. 2024. [Google Scholar] [CrossRef]
  23. Keum, H.; Yoo, D.; Jon, S. Photomedicine based on heme-derived compounds. Adv. Drug Deliv. Rev. 2022, 182, 114134. [Google Scholar]
  24. Li, Q.; Li, C.; Baryshnikov, G.; Ding, Y.; Zhao, C.; Gu, T.; Sha, F.; Liang, X.; Zhu, W.; Wu, X.; et al. Twisted-planar-twisted expanded porphyrinoid dimer as a rudimentary reaction-based methanol indicator. Nat. Commun. 2020, 11, 5289. [Google Scholar]
  25. Lin, Y.; Li, M.; Huang, L.; Shen, W.; Ren, Y. Involvement of heme oxygenase-1 in β-cyclodextrin–hemin complex-induced cucumber adventitious rooting process. Plant Cell Rep. 2012, 31, 1563–1572. [Google Scholar]
  26. Zhang, J.; Yang, X.; Ren, Y.; Yang, B.; Liu, Z.; You, B.; Zhang, H.; Shen, W.; Chen, X. Β-cyclodextrin–hemin enhances tolerance against salinity in tobacco seedlings by reestablishment of ion and redox homeostasis. Plant Growth Regul. 2017, 81, 533–542. [Google Scholar]
  27. Xie, Y.J.; Xu, S.; Han, B.; Wu, M.Z.; Yuan, X.X.; Han, Y.; Gu, Q.; Xu, D.K.; Yang, Q.; Shen, W.B. Evidence of arabidopsis salt acclimation induced by up-regulation of hy1 and the regulatory role of rbohd-derived reactive oxygen species synthesis. Plant J. Cell Mol. Biol. 2011, 66, 280–292. [Google Scholar]
  28. Sun, G.; Meng, Y.; Wang, Y.; Zhao, M.; Wei, S.; Gu, W. Exogenous hemin optimized maize leaf photosynthesis, root development, grain filling, and resource utilization on alleviating cadmium stress under field condition. J. Soil Sci. Plant Nut. 2022, 22, 631–646. [Google Scholar]
  29. Li, Y.; Li, H.; Wang, F.; Li, J.; Zhang, Y.; Wang, L.; Gao, J.; Sheng, Q. Comparative transcriptome analysis reveals effects of exogenous hematin on anthocyanin biosynthesis during strawberry fruit ripening. Int. J. Genom. 2016, 2016, 6762731. [Google Scholar]
  30. Balestrasse, K.B.; Zilli, C.G.; Tomaro, M.L. Signal transduction pathways and haem oxygenase induction in soybean leaves subjected to salt stress. Redox Rep. 2008, 13, 255–262. [Google Scholar]
  31. Chu, Y.; Chang, J. Heat stress leads to poor fruiting mainly due to inferior pollen viability and reduces shoot photosystem ii efficiency in “da hong” pitaya. Agronomy 2022, 12, 225. [Google Scholar] [CrossRef]
  32. Diop, A.; Meot, J.M.; Lechaudel, M.; Chiroleu, F.; Ndiaye, N.D.; Mertz, C.; Cisse, M.; Chillet, M. Impact of preharvest and postharvest on color changes during convective drying of mangoes. Foods 2021, 10, 490. [Google Scholar] [CrossRef] [PubMed]
  33. Campion, E.M.; Loughran, S.T.; Walls, D. Protein Quantitation and Analysis of Purity; Humana Press: Totowa, NJ, USA, 2011; Volume 681, pp. 229–258. [Google Scholar]
  34. Kuai, J.; Liu, Z.; Wang, Y.; Meng, Y.; Chen, B.; Zhao, W.; Zhou, Z.; Oosterhuis, D.M. Waterlogging during flowering and boll forming stages affects sucrose metabolism in the leaves subtending the cotton boll and its relationship with boll weight. Plant Sci. 2014, 223, 79–98. [Google Scholar] [PubMed]
  35. Kanto, U.; Jutamanee, K.; Osotsapar, Y.; Jattupornpong, S. Effect of swine manure extract on leaf nitrogen concentration, chlorophyll content, total potassium in plant parts and starch content in fresh tuber yield of cassava. J. Plant Nutr. 2012, 35, 688–703. [Google Scholar]
  36. Nayyar, H.; Bains, T.; Kumar, S. Low temperature induced floral abortion in chickpea: Relationship to abscisic acid and cryoprotectants in reproductive organs. Environ. Exp. Bot. 2005, 53, 39–47. [Google Scholar]
  37. Du, Y.; Zhao, Q.; Chen, L.; Yao, X.; Zhang, W.; Zhang, B.; Xie, F. Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings. Plant Physiol. Biochem. 2020, 146, 1–12. [Google Scholar] [PubMed]
  38. Zeraik, M.L.; Yariwake, J.H. Quantification of isoorientin and total flavonoids in passiflora edulis fruit pulp by hplc-uv/dad. Microchem. J. 2010, 96, 86–91. [Google Scholar]
  39. Pirie, A.; Mullins, M.G. Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrose, nitrate, and abscisic acid. Plant Physiol. 1976, 58, 468–472. [Google Scholar] [PubMed]
  40. Giannopolitis, C.N.; Ries, S.K. Superoxide dismutases, 1: Occurrence in higher plants [corn, oats, peas]. Plant Physiol. 1977, 59, 309–314. [Google Scholar] [PubMed]
  41. Stewart, R.R.C.; Bewley, J.D. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol. 1980, 65, 245–248. [Google Scholar] [PubMed]
  42. Klapheck, S.; Zimmer, I.; Cosse, H. Scavenging of hydrogen peroxide in the endosperm of ricinus communis by ascorbate peroxidase. Plant Cell Physiol. 1990, 31, 1005–1013. [Google Scholar]
  43. Gupta, D.K.; Huang, H.G.; Yang, X.E.; Razafindrabe, B.H.N.; Inouhe, M. The detoxification of lead in sedum alfredii h. Is not related to phytochelatins but the glutathione. J. Hazard. Mater. 2010, 177, 437–444. [Google Scholar]
  44. Li, X.; Zhang, L.; Li, Y.; Ma, L.; Bu, N.; Ma, C. Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to uv-b radiation and/or cd. Plant Soil 2012, 352, 377–387. [Google Scholar]
  45. Nakano, Y.; Asada, K.K.U.U. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22, 867–880. [Google Scholar]
  46. Xiao, Q.; Tang, W.; Zhang, C.; Zhou, L.; Feng, L.; Shen, J.; Yan, T.; Gao, P.; He, Y.; Wu, N. Spectral preprocessing combined with deep transfer learning to evaluate chlorophyll content in cotton leaves. Plant Phenomics 2022, 2022, 9813841. [Google Scholar]
  47. Qian, G.; Li, X.; Zhang, H.; Zhang, H.; Zhou, J.; Ma, X.; Sun, W.; Yang, W.; He, R.; Wahab, A.; et al. Metabolomics analysis reveals the accumulation patterns of flavonoids and phenolic acids in quinoa (Chenopodium quinoa willd.) Grains of different colors. Food Chem. X 2023, 17, 100594. [Google Scholar] [PubMed]
  48. Liu, Y.; Pan, Y.; Li, J.; Chen, J.; Yang, S.; Zhao, M.; Xue, Y. Transcriptome sequencing analysis of root in soybean responding to mn poisoning. Int. J. Mol. Sci. 2023, 24, 12727. [Google Scholar] [CrossRef]
  49. Magalhães, D.S.; Ramos, J.D.; Pio, L.A.S.; Vilas Boas, E.V.D.B.; Pasqual, M.; Rodrigues, F.A.; Rufini, J.C.M.; Santos, V.A.D. Physical and physicochemical modifications of white-fleshed pitaya throughout its development. Sci. Hortic. 2019, 243, 537–543. [Google Scholar]
  50. Abdel-Hamid, H.A.; Marey, H.; Ibrahim, M. Hemin protects against cell stress induced by estrogen and progesterone in rat mammary glands via modulation of nrf2/ho-1 and nf-kappab pathways. Cell Stress Chaperones 2023, 28, 289–301. [Google Scholar]
  51. Zhao, M.; Meng, Y.; Wang, Y.; Sun, G.; Liu, X.; Li, J.; Wei, S.; Gu, W. Exogenous hemin alleviates cadmium stress in maize by enhancing sucrose and nitrogen metabolism and regulating endogenous hormones. Int. J. Phytoremediat. 2023, 25, 368–380. [Google Scholar]
  52. Mahawar, L.; Popek, R.; Shekhawat, G.S.; Alyemeni, M.N.; Ahmad, P. Exogenous hemin improves Cd2+ tolerance and remediation potential in Vigna radiata by intensifying the ho-1 mediated antioxidant defence system. Sci. Rep. 2021, 11, 2811. [Google Scholar]
  53. Chen, Q.; Zhang, X.; Liu, Y.; Wei, J.; Shen, W.; Shen, Z.; Cui, J. Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; Suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul. 2017, 81, 253–264. [Google Scholar]
  54. Zhao, H.; Zheng, D.; Feng, N.; Zhou, G.; Khan, A.; Lu, X.; Deng, P.; Zhou, H.; Du, Y. Regulatory effects of hemin on prevention and rescue of salt stress in rapeseed (Brassica napus L.) Seedlings. BMC Plant Biol. 2023, 23, 558. [Google Scholar]
  55. Shafiq, M.; Singh, Z.; Khan, A.S. Time of methyl jasmonate application influences the development of ‘cripps pink’ apple fruit colour. J. Sci. Food Agric. 2013, 93, 611–618. [Google Scholar]
  56. Shattir, A.; Abu-Goukh, A. Physico-chemical changes during growth and development of papaya fruit. Ι: Physical changes. Agric. Biol. J. N. Am. 2010, 1, 866–870. [Google Scholar]
  57. de Lima, C.A.; Fábio, G.F.; Nilton, T.V.J.; Graciele, B. Avaliação de características físico-químicas de frutos de duas espécies de pitaya1. Ceres Mag. 2014, 3, 377–383. [Google Scholar]
  58. Cordeiro, M.H.M.; Silva, J.M.D.; Mizobutsi, G.P.; Mizobutsi, E.H.; Mota, W.F.D. Caracterização física, química e nutricional da pitaia-rosa de polpa vermelha. Rev. Bras. Frutic. 2015, 37, 20–26. [Google Scholar]
  59. Burger, Y.; Schaffer, A.A. Contribution of sucrose metabolism enzymes to sucrose accumulation in cucumis melo. J. Am. Soc. Hortic. Sci. 2007, 132, 704–712. [Google Scholar]
  60. Wang, Y.; Ji, D.; Chen, T.; Li, B.; Zhang, Z.; Qin, G.; Tian, S. Production, signaling, and scavenging mechanisms of reactive oxygen species in fruit-pathogen interactions. Int. J. Mol. Sci. 2019, 20, 2994. [Google Scholar] [CrossRef]
  61. Kerch, G. Chitosan films and coatings prevent losses of fresh fruit nutritional quality: A review. Trends Food Sci. Technol. 2015, 46, 159–166. [Google Scholar]
  62. Li, X.; Li, M.; Wang, J.; Wang, L.; Han, C.; Jin, P.; Zheng, Y. Methyl jasmonate enhances wound-induced phenolic accumulation in pitaya fruit by regulating sugar content and energy status. Postharvest Biol. Technol. 2018, 137, 106–112. [Google Scholar]
  63. Ali, A.; Ong, M.K.; Forney, C.F. Effect of ozone pre-conditioning on quality and antioxidant capacity of papaya fruit during ambient storage. Food Chem. 2014, 142, 19–26. [Google Scholar]
  64. Roleira, F.M.; Tavares-Da-Silva, E.J.; Varela, C.L.; Costa, S.C.; Silva, T.; Garrido, J.; Borges, F. Plant derived and dietary phenolic antioxidants: Anticancer properties. Food Chem. 2015, 183, 235–258. [Google Scholar] [PubMed]
  65. Akyol, H.; Riciputi, Y.; Capanoglu, E.; Caboni, M.F.; Verardo, V. Phenolic compounds in the potato and its byproducts: An overview. Int. J. Mol. Sci. 2016, 17, 835. [Google Scholar] [CrossRef]
  66. Liu, X.; Meng, Y.; Wei, S.; Gu, W. Exogenous hemin confers cadmium tolerance by decreasing cadmium accumulation and modulating water status and matter accumulation in maize seedlings. Agronomy 2021, 11, 739. [Google Scholar] [CrossRef]
  67. Alañón, M.E.; Pimentel-Moral, S.; Arráez-Román, D.; Segura-Carretero, A. Hplc-dad-q-tof-ms profiling of phenolic compounds from mango (Mangifera indica L.) Seed kernel of different cultivars and maturation stages as a preliminary approach to determine functional and nutraceutical value. Food Chem. 2021, 337, 127764. [Google Scholar]
  68. Trivellini, A.; Lucchesini, M.; Ferrante, A.; Massa, D.; Orlando, M.; Incrocci, L.; Mensuali-Sodi, A. Pitaya, an attractive alternative crop for mediterranean region. Agronomy 2020, 10, 1065. [Google Scholar] [CrossRef]
  69. Zhao, H.; Fan, Z.; Wu, J.; Zhu, S. Effects of pre-treatment with s-nitrosoglutathione-chitosan nanoparticles on quality and antioxidant systems of fresh-cut apple slices. Food Sci. Technol. 2021, 139, 110565. [Google Scholar]
  70. Zhu, Z.; Huang, Y.; Wu, X.; Liu, Z.; Zou, J.; Chen, Y.; Su, N.; Cui, J. Increased antioxidative capacity and decreased cadmium uptake contribute to hemin-induced alleviation of cadmium toxicity in chinese cabbage seedlings. Ecotoxicol. Environ. Saf. 2019, 177, 47–57. [Google Scholar] [PubMed]
  71. Han, Y.; Xuan, W.; Yu, T.; Fang, W.B.; Lou, T.L.; Gao, Y.; Chen, X.Y.; Xiao, X.; Shen, W.B. Exogenous hematin alleviates mercury-induced oxidative damage in the roots ofmedicago sativa. J. Integr. Plant Biol. 2007, 49, 1703–1713. [Google Scholar]
  72. Xia, Y.; Chen, T.; Qin, G.; Li, B.; Tian, S. Synergistic action of antioxidative systems contributes to the alleviation of senescence in kiwifruit. Postharvest Biol. Technol. 2016, 111, 15–24. [Google Scholar]
  73. Gayathri, V.; Asha, V.V.; John, J.A.; Subramoniam, A. Protection of immunocompromised mice from fungal infection with a thymus growth-stimulatory component from selaginella involvens, a fern. Immunopharm. Immunot. 2011, 33, 351–359. [Google Scholar]
  74. Ren, M.; Li, S.; Gao, Q.; Qiao, L.; Cao, Q.; Yang, Z.; Chen, C.; Jiang, Y.; Wang, G.; Fu, S. Advances in the anti-tumor activity of biflavonoids in iselaginella/i. Int. J. Mol. Sci. 2023, 24, 7731. [Google Scholar] [PubMed]
  75. Bailly, C. The traditional and modern uses of Selaginella tamariscina (p.beauv.) Spring, in medicine and cosmetic: Applications and bioactive ingredients. J. Ethnopharmacol. 2021, 280, 114444. [Google Scholar] [PubMed]
  76. Křížkovská, B.; Kumar, R.; Yehořová, K.; Sýkora, D.; Dobiasová, S.; Kučerová, D.; Tan, M.C.; Linis, V.; Oyong, G.; Ruml, T.; et al. Comparison of chemical composition and biological activities of eight selaginella species. Pharmaceuticals 2021, 14, 16. [Google Scholar]
  77. Gao, F.; Khan, R.; Yang, L.; Chi, Y.X.; Wang, Y.; Zhou, X.B. Uncovering the potentials of long-term straw return and nitrogen supply on subtropical maize (Zea mays L.) Photosynthesis and grain yield. Field Crops Res. 2023, 302, 109062. [Google Scholar]
  78. Liu, Y.; Xu, S.; Ling, T.; Xu, L.; Shen, W. Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J. Plant Physiol. 2010, 167, 1371–1379. [Google Scholar] [PubMed]
Agronomy 14 01850 g001aAgronomy 14 01850 g001b
Figure 1. Changes in L* (A); a* (B); b* (C); pericarp a*/b* (D); saturation (E); and hue angle (F) of the pericarp under different treatments. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Figure 1. Changes in L* (A); a* (B); b* (C); pericarp a*/b* (D); saturation (E); and hue angle (F) of the pericarp under different treatments. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Agronomy 14 01850 g001aAgronomy 14 01850 g001b
Agronomy 14 01850 g002
Figure 2. Changes in soluble solids content (A), soluble protein content (B), starch content (C), and sucrose content (D) of dragon fruit pulp under different treatments. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Figure 2. Changes in soluble solids content (A), soluble protein content (B), starch content (C), and sucrose content (D) of dragon fruit pulp under different treatments. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Agronomy 14 01850 g002
Agronomy 14 01850 g003
Figure 3. Changes of total phenol (A), flavonoid (B) and anthocyanin content of dragon fruit pulp under different treatments (C). CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Figure 3. Changes of total phenol (A), flavonoid (B) and anthocyanin content of dragon fruit pulp under different treatments (C). CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Agronomy 14 01850 g003
Agronomy 14 01850 g004
Figure 4. Effect of different treatments on superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX), and catalase (CAT) of dragon fruit pulp. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean ± standard error of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Figure 4. Effect of different treatments on superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX), and catalase (CAT) of dragon fruit pulp. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean ± standard error of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Agronomy 14 01850 g004
Agronomy 14 01850 g005
Figure 5. Effect of different Hemin treatments on chlorophyll a (Chla) (A), chlorophyll b (Chlb) (B), total chlorophyll (Chl) (C) and carotenoid (D) content of dragon fruit stems. CK: control; H2: 10 μmol.L−1. Mean ± standard error of three replicates. The significance test of difference between normal group and H2 treatment group was implemented with Student’s t-test. ** indicates highly significant difference (p < 0.01).
Figure 5. Effect of different Hemin treatments on chlorophyll a (Chla) (A), chlorophyll b (Chlb) (B), total chlorophyll (Chl) (C) and carotenoid (D) content of dragon fruit stems. CK: control; H2: 10 μmol.L−1. Mean ± standard error of three replicates. The significance test of difference between normal group and H2 treatment group was implemented with Student’s t-test. ** indicates highly significant difference (p < 0.01).
Agronomy 14 01850 g005
Agronomy 14 01850 g006aAgronomy 14 01850 g006b
Figure 6. Metabolite classification plot (A), phenolic content thermogram (B) under Hemin treatment vs. control. CK-1, CK-2, CK-3, and H2-1, H2-2, and H2-3 represent three sample replicates in control and 10 μmol.L−1 Hemin treatments.
Figure 6. Metabolite classification plot (A), phenolic content thermogram (B) under Hemin treatment vs. control. CK-1, CK-2, CK-3, and H2-1, H2-2, and H2-3 represent three sample replicates in control and 10 μmol.L−1 Hemin treatments.
Agronomy 14 01850 g006aAgronomy 14 01850 g006b
Agronomy 14 01850 g007
Figure 7. OPLS-DA plots of Hemin treatment versus control (A), OPLS-DA validation plots (B). CK-1, CK-2, CK-3, and H2-1, H2-2, and H2-3 represent three sample replicates of the control and 10 μmol. L−1 Hemin treatments.
Figure 7. OPLS-DA plots of Hemin treatment versus control (A), OPLS-DA validation plots (B). CK-1, CK-2, CK-3, and H2-1, H2-2, and H2-3 represent three sample replicates of the control and 10 μmol. L−1 Hemin treatments.
Agronomy 14 01850 g007
Agronomy 14 01850 g008
Figure 8. Correlation between antioxidant enzyme activity, phenolic content, nutritional quality, photosynthetic pigment content and yield of dragon fruit by different Hemin treatments.
Figure 8. Correlation between antioxidant enzyme activity, phenolic content, nutritional quality, photosynthetic pigment content and yield of dragon fruit by different Hemin treatments.
Agronomy 14 01850 g008
Table 1. Changes of different treatments on morphological indices of dragon fruit. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
Table 1. Changes of different treatments on morphological indices of dragon fruit. CK: control; H1: 1 μmol.L−1; H2: 10 μmol.L−1; H3: 100 μmol.L−1. Mean  ±  SE of three replicates. Duncan’s multiple comparison test was adopted for significance analysis of the differences between the normal group and the treatment group. Different letters indicate significant differences (p < 0.05).
TreatmentSingle Fruit Weight (g)Edible Rate (%)Yield (g)Transverse
Diameter (mm)		Longitudinal
Diameter (mm)		Fruit Shape
Index
CK219.16 ± 8.61 b61.49%± 0.02 b6110.09 ± 206.15 b66.20 ± 2.72 a84.67 ± 3.28 b1.2767 ± 0.00 c
H1247.62 ± 1.99 ab65.89%± 0.01 a6195.23 ± 69.88 b68.07 ± 1.15 a90.13 ± 1.91 ab1.3267 ± 0.01 b
H2265.34 ± 14.04 a68.44% ± 0.01 a6954.10 ± 87.77 a67.63 ± 3.75 a90.67 ± 5.34 ab1.34 ± 0.01 ab
H3247.42 ± 9.44 ab67.92%± 0.00 a6820.99 ± 230.08 a71.83 ± 0.66 a98.50 ± 1.82 a1.3667 ± 0.01 a
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sun, M.; Khan, A.; Wang, J.; Ding, L.; Yang, X.; Xiong, J.; Sun, Z.; Feng, N.; Zheng, D. Exogenous Hemin Increases the Yield, Phenolic Compound Content, and Antioxidant Enzyme Activity of Dragon Fruit during the High-Temperature Period. Agronomy 2024, 14, 1850. https://doi.org/10.3390/agronomy14081850

AMA Style

Sun M, Khan A, Wang J, Ding L, Yang X, Xiong J, Sun Z, Feng N, Zheng D. Exogenous Hemin Increases the Yield, Phenolic Compound Content, and Antioxidant Enzyme Activity of Dragon Fruit during the High-Temperature Period. Agronomy. 2024; 14(8):1850. https://doi.org/10.3390/agronomy14081850

Chicago/Turabian Style

Sun, Minmin, Aaqil Khan, Jiahui Wang, Linchong Ding, Xiaohui Yang, Jian Xiong, Zhiyuan Sun, Naijie Feng, and Dianfeng Zheng. 2024. "Exogenous Hemin Increases the Yield, Phenolic Compound Content, and Antioxidant Enzyme Activity of Dragon Fruit during the High-Temperature Period" Agronomy 14, no. 8: 1850. https://doi.org/10.3390/agronomy14081850

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop