Effect of Enhanced Ultraviolet-B Radiation on Fruit Maturity and Quality and Leaf Photosynthesis in ‘Guifei’ Mango

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Xiaokai LinCollege of Horticulture, Hainan University, Haikou 570228, China; and Engineering Research Center for the Selection and Breeding of New Tropical Crop Varieties, Ministry of Education, Haikou 570228, China

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Feng LiuSouth Subtropical Crop Research Institute, China Academy of Tropical Agricultural Sciences, Zhanjiang 524000, China

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Haizhi LiaoCollege of Horticulture, Hainan University, Haikou 570228, China; and Engineering Research Center for the Selection and Breeding of New Tropical Crop Varieties, Ministry of Education, Haikou 570228, China

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Jingjia DuCollege of Horticulture, Hainan University, Haikou 570228, China; and Engineering Research Center for the Selection and Breeding of New Tropical Crop Varieties, Ministry of Education, Haikou 570228, China

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Junjie PengCollege of Horticulture, Hainan University, Haikou 570228, China; and Engineering Research Center for the Selection and Breeding of New Tropical Crop Varieties, Ministry of Education, Haikou 570228, China

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Kaibing ZhouCollege of Horticulture, Hainan University, Haikou 570228, China; and Engineering Research Center for the Selection and Breeding of New Tropical Crop Varieties, Ministry of Education, Haikou 570228, China

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To investigate the characteristics of photosynthetic physiological changes in leaves of Mangifera indica L. cv. Guifei under enhanced ultraviolet (UV)-B radiation, natural light-exposed trees were used as controls and 96 kJ·m−2·d−1 enhanced UV-B radiation was artificially simulated in the field. The changes in fruit maturity and quality, the leaf net photosynthetic rate (Pn), photosynthetic pigment contents, photochemical reactions, the activities of photosynthetic enzymes and related gene expression levels were determined. Compared with the control, the percentage of mature fruits under the treatment significantly increased, and fruit quality improved. The net photosynthetic rate (Pn), photosynthetic pigment content, Hill reaction activity, and photochemical quenching coefficient (qP) of the treated leaves showed significantly higher values than those of the control leaves. The activities of Rubisco and Rubisco activating enzyme (RCA) and the expression levels of the Rubisco large subunit and Rubisco small subunit were significantly increased. Treatment with 96 kJ·m−2·d−1 enhanced ultraviolet-B radiation improved Rubisco activity by increasing the expression of the Rubisco large and small subunit genes, thereby enhancing the CO2-fixing capacity and dark reaction capacity of leaves. Thus, the net photosynthetic rate of leaves increased, which promoted the early maturity of ‘Guifei’ mango by the rapid accumulation of photosynthetic products.

Abstract

To investigate the characteristics of photosynthetic physiological changes in leaves of Mangifera indica L. cv. Guifei under enhanced ultraviolet (UV)-B radiation, natural light-exposed trees were used as controls and 96 kJ·m−2·d−1 enhanced UV-B radiation was artificially simulated in the field. The changes in fruit maturity and quality, the leaf net photosynthetic rate (Pn), photosynthetic pigment contents, photochemical reactions, the activities of photosynthetic enzymes and related gene expression levels were determined. Compared with the control, the percentage of mature fruits under the treatment significantly increased, and fruit quality improved. The net photosynthetic rate (Pn), photosynthetic pigment content, Hill reaction activity, and photochemical quenching coefficient (qP) of the treated leaves showed significantly higher values than those of the control leaves. The activities of Rubisco and Rubisco activating enzyme (RCA) and the expression levels of the Rubisco large subunit and Rubisco small subunit were significantly increased. Treatment with 96 kJ·m−2·d−1 enhanced ultraviolet-B radiation improved Rubisco activity by increasing the expression of the Rubisco large and small subunit genes, thereby enhancing the CO2-fixing capacity and dark reaction capacity of leaves. Thus, the net photosynthetic rate of leaves increased, which promoted the early maturity of ‘Guifei’ mango by the rapid accumulation of photosynthetic products.

The ultraviolet radiation B region (UV-B, 280–315 nm) is critical for plant growth and development, morphogenesis, adaptive orientation, photosynthesis, and secondary metabolism (Krizek, 2004; Rozema et al., 1997; Teramura, 1983). In recent years, atmospheric thinning of the ozone layer has led to more UV-B radiation reaching the biosphere, which is called “enhanced UV-B radiation” (Neale et al., 2021). Therefore, there has been great concern about increased UV-B radiation and its consequences on the biosphere throughout the 21st century, although the ozone layer has recovered in recent years due to the implementation of the Montreal Protocol.

Currently, studies on the effects of enhanced UV-B radiation and its causes have been conducted in China and abroad and has mainly on food crops (Duarte-Sierra et al., 2020; Erram et al., 2017; He et al., 2015; Liu et al., 2013; Mao et al., 2017) and algae (Saber et al., 2020). One of the effects of enhanced UV-B radiation on plants is on photosynthesis, and in general, a high dose of UV-B radiation leads to a decrease in chloroplast content, the destruction of photosynthetic system reaction centers, and reductions in Hill reaction activity, photosynthetic system II (PSII) light use efficiency, and the net photosynthetic rate (Albert et al., 2010; Ballaré et al., 2011). UV-B radiation also greatly reduces the yield and quality of cotton (Kakani et al., 2003).

Some studies have also shown that enhanced UV-B radiation can have beneficial effects on plants, with appropriate enhanced UV-B radiation increasing the photosynthetic pigment contents of tobacco leaves and chrysanthemum (Liu et al., 2007; Ma et al., 2016). Moreover, appropriately enhanced UV-B radiation is beneficial to the growth of Luffa cylindrical (Luo et al., 2003). The results showed that enhanced UV-B radiation increased the chlorophyll and iron contents in the roots and leaves of maize (Zlatev et al., 2012).

Mango (Mangifera indica L.) is an evergreen tree belonging to the family Anacardiaceae and is known as the “king of tropical fruits” in China. Hainan is one of the most important mango production areas. This tree is generally distributed in tropical areas with low latitudes and strong UV radiation, so mango can adapt well to this environment. With the possibility of stronger UV-B radiation in the future, it is necessary to study the effect of enhanced UV-B radiation on fruit development and leaf photosynthesis in mango. Our previous study on the cultivation performance and photosynthetic performance of mango under different levels of enhanced UV-B radiation showed that 24 kJ·m−2·d−1 enhanced UV-B radiation had no effect on adult mango trees, and 48 kJ·m−2·d−1 and 96 kJ·m−2·d−1 enhanced UV-B radiation treatments reduced the tree yield and fruit quality of ‘Tainong 1’ and ‘Jinhuang’ mangoes. Additionally, the mesophyll tissue structure was damaged, resulting in a decrease in photosynthetic performance. Among the treatments, 96 kJ·m−2·d−1 enhanced UV-B radiation had a serious adverse effect on adult mango trees (Wang et al., 2020a, 2020b; Yue et al., 2019; Yuan et al., 2019; Zhou et al., 2019). At present, there are no reports on the effects of enhanced UV-B radiation on fruit development and leaf photosynthesis in Guifei mango, another major cultivar in Hainan Province.

In this article, ‘Guifei’ mango was used as the experimental material, and an enhanced UV-B radiation treatment of 96 kJ·m−2·d−1 was simulated in the field. The mature fruit ratio, fruit quality indexes, including soluble sugar, titratable acid, total soluble solid, and vitamin C contents, and leaf photosynthetic parameters were measured to study the effect of enhanced UV-B radiation on fruit maturity and quality and leaf photosynthetic capacity in ‘Guifei’ mango. Our results reveal the response of ‘Guifei’ mango to enhanced UV-B radiation, which will be helpful for improving tolerance to UV-B stress in mango in the future.

Materials and Methods

Plant material and growth conditions

The trial was conducted in a collectively owned mango orchard in Liaoci Village, Yingzhou Town, Lingshui Li Autonomous County, Hainan Province, with a tropical and monsoon climate. The annual precipitation is 1500 to 2500 mm, and the annual average temperature is 25.2 °C. We selected ten 16-year-old ‘Guifei’ mango trees that were robust and uniform in growth and free from diseases and pests, with a spacing of 3 m × 5 m. A yield regulation technique was implemented, with the Qingming Festival as the expected harvest period, the flowering period being late December to early January, the first physiological fruiting period being mid-January, the second physiological fruiting period being late January, the fruiting period being early February, the fruit expansion period being early to mid-April, and the ripening period being late April to early May.

UV-B radiation experiments

Natural light (including visible and UV light) was used as the control, and 96 kJ·m−2·d−1 artificially simulated enhanced UV-B radiation was set up in the field as the treatment. The field experiment was designed with a single tree plot and five replications. The average local UV-B radiation intensity was 83.47 kJ·m−2·d−1. Treatment was carried out from the full flowering period (late December) to the fruit ripening period (mid-May). A trellis was set up in the test garden along with four UV lamps (KAZHI, LH26R36R, Nanjing, China). The power of each UV lamp was 40 W, the peak wavelength was 313 nm, the radiation dose was 24 kJ·m−2·d−1, and the lamp light source was wrapped with a 0.08-mm cellulose acetate membrane to filter UV-C. The UV lamps were cross-suspended at 30 cm from the top of the trees, and the lamps were turned on daily from 0800 to 1700 HR (treatment was stopped on cloudy and rainy days) for 5 months of continuous treatment.

Sampling for biochemical assays

Five mango leaves from each tree were collected every 7 d from 27 Dec 2019, to 22 May 2020 for biochemical analysis. The second sampling was carried out on 17 Jan 2020 and was stopped for a period due to the coronavirus epidemic. The positions of leaf and fruit samples collected in the experiment were at the top of 30 cm under the light source, and the intensity of UV-B was 179.47 kJ·m−2·d−1. The yield per plant was investigated during fruit harvesting, and 10 fruit samples were randomly selected from the periphery of the middle crown for quality analysis. Leaf and fruit samples were collected and frozen in liquid nitrogen and stored at −80 °C until use.

Indicators and methods

Determination of the ripe mango fruit ratio.

The yield per tree was investigated in the field 134, 141, and 150 d after flowering, and the fruit maturation rate was investigated according to the standard of complete fruit maturation based on the skin color change from yellow to red.

Determination of the mango quality index.

The soluble sugar and vitamin C contents of pulp were measured according to the method described by Li (2000). The soluble solids and titratable acid contents of pulp were measured by a sugar acid meter (PAL-BXIACID15; ATAGO, Tokyo, Japan). Soluble solids are solid substances soluble in the water of fruit juice and include sugars, organic acids, mineral salts, soluble proteins, pectin, pigments, and vitamins. The soluble solid content is one indicator of fruit flavor quality and maturity. Soluble solids are mainly soluble sugars. The sugar-acid ratio of fruit is the ratio of soluble sugar to titratable acid, and the solid-acid ratio of fruit is the ratio of soluble solids to titratable acid.

Measurement of the leaf net photosynthetic rate.

The net photosynthetic rate (Pn) of leaves was measured by a photosynthesis analyzer (Yaxin-1101; YAXIN LIYI, Beijing, China). The top well-developed leaves of mango trees were selected for measurement. At 10:00 AM, the leaves were placed in a leaf chamber under natural light. The photosynthetic (respiration) rate of the leaves could be calculated automatically after parameters such as the CO2 concentration, humidity, temperature, leaf temperature, and gas flow in the gas path were measured by the instrument. Measurements were taken every other week.

Determination of the chlorophyll fluorescence quenching coefficient and physiological and biochemical indicators of leaves.

Leaf photosynthetic pigment contents were determined by the Arnon method (Arnon, 1949), and the chlorophyll a+b contents and a/b values were calculated. Determination of chlorophyll fluorescence quenching coefficients was performed using a dual-channel modulated chlorophyll fluorometer (DUAL-PAM-100; Zealquest Scientific Technology, Shanghai, China). The Hill reaction activity was determined using a method from the literature (Yu and Zheng, 1980).

Determination of carbon assimilation-related enzyme activities and gene expression in leaves.

The enzyme activities of Rubisco activating enzyme (RCA) and ribulose-1,5-diphosphate carboxylase/oxygenase (Rubisco) were determined by an enzyme-linked immunoassay kit (Sangon Biotech, Shanghai, China). Total RNA was extracted by a UNlQ-10 column TRIzol total RNA extraction kit (B511321, Sangon Biotech). Maxima Reverse Transcriptase (EP0307; Vazyme, Nanjing, China) was used for reverse transcription, and 2X SG Fast qPCR Master Mix (B639273, Vazyme) was used for real-time quantitative PCR (Q-PCR). The relative quantitative calculation was performed by the 2-ΔΔCt method. Primers for amplifying Rubisco large (rbcL) and small (rbcS) subunits were designed using the Primer3 (https://primer3.ut.ee/) online tool, and the reference gene was Actin (Zhang et al., 2017). The primers designed in his study were as follows: rbcL (F-ACGCCGGTACAGTAGTAGGT, R-GAATCCAGTCCAACCACG) and rbcS (F-CCTCTCCTACCTCCCTCCTC, R-GCACATGTCCCACCTCATCA).

Statistical analysis

SAS software was used for statistical analysis. Analysis of variance was used to determine the dynamic changes in each indicator, and the least significant difference method was used for multiple comparative analysis (P < 0.05). A t test was used to test the significance of the differences between the treatment and the control for each indicator.

Results

Effect of enhanced UV-B radiation on the mature fruit ratio

As seen in Figs. 1 and 2, the mature fruit ratio was significantly higher in all treatments than in the control during the study period. The mature fruit ratio of the control was almost 0 and was 6.77% higher in the treatment than in the control 134 d after flowering. The ratio in the treatment was 37.83% higher than that in the control 141 d after flowering, showing the maximum difference. At 150 d after flowering, the ratio in the treatment was 23% higher than that in the control. The enhanced UV-B radiation treatment of 96 kJ·m−2·d−1 promoted fruit ripening of ‘Guifei’ mango.

Fig. 1.
Fig. 1.

The mangoes were harvested 134 d after flowering.

Citation: HortScience 57, 9; 10.21273/HORTSCI16738-22

Fig. 2.
Fig. 2.

The effects of enhanced ultraviolet-B radiation on the mature fruit ratio. *Indicates a significant difference between the treatment and the control (P < 0.05), and the same as below.

Citation: HortScience 57, 9; 10.21273/HORTSCI16738-22

Effects of enhanced UV-B radiation on fruit quality

Tables 1 and 2 show that the soluble sugar content, soluble solid content, sugar-acid ratio, and solid-acid ratio of the flesh of treated fruits at 134 d after flowering were significantly higher than those of the control, while the titratable acid content under the treatment was significantly lower than that under the control; there was no significant difference at other times. There was no significant difference in the vitamin C content between the treatment and the control at 134 and 141 d after flowering, and the vitamin C content in the treated fruit flesh was significantly higher than that in the control at 150 d after flowering. Therefore, there was no significant difference between the treatment and the control regarding fruit quality at 141 d and 150 d after flowering. The fruit quality under the treatment at 134 d after flowering was significantly better than that under the control, which might have been due to its early maturity.

Table 1.

Comparison of soluble sugar, titratable acid, and soluble solid contents between the treatment and the control.

Table 1.
Table 2.

Comparison of the sugar-acid ratio, solid-acid ratio, and vitamin C content between the treatment and the control.

Table 2.

Effects of enhanced UV-B radiation on the leaf photosynthetic rate

As seen in Fig. 3A, the Pn of both the treatment and the control showed a similar “M”-shaped trend, with no significant change from 27 Dec to 17 Jan, a significant decrease until 22 Apr, and then a significant increase until 7 May 7, followed by a significant decrease until 22 May. At the same time, the Pn of the treatment was significantly higher on 22 Apr, 29 Apr, and 7 May than that of the control. Visibly, the 96 kJ·m−2·d−1 enhanced UV-B radiation treatment showed a trend of promoting photosynthesis in the leaves of ‘Guifei’ mango.

Fig. 3.
Fig. 3.

The effects of enhanced ultraviolet-B radiation on the net photosynthetic rate (Pn), Hill reaction activity, photochemical quenching coefficient, Rubisco activating enzyme, Rubisco, and relative expression of Rubisco large subunit and Rubisco small subunit genes in leaves. Note: The letters of the line chart indicate significant differences in the dynamic changes on different dates; different letters indicate significant differences, and the same letter indicates nonsignificant (P < 0.05).

Citation: HortScience 57, 9; 10.21273/HORTSCI16738-22

Effects of enhanced UV-B radiation on the photosynthetic pigment content in leaves

The effects of enhanced UV-B radiation treatment on the photosynthetic pigment content in leaves are shown in Table 3. There were significant differences between the treatment and the control in the dynamic changes at a given time.

Table 3.

The effects of enhanced ultraviolet-B radiation on the photosynthetic pigment contents in mango leaves.

Table 3.

The chlorophyll a, b, and a + b contents in the control had no significant change before 15 May and then increased significantly. The chlorophyll a, b and a + b contents in the control had no significant change from 27 Dec to 22 Apr and increased significantly after 22 Apr. The chlorophyll a/b of the control had no significant change before 17 Jan and then showed a downward trend; the values of the treatment showed no significant change until 7 May with a decreasing trend afterward. The carotenoid content of the control did not change significantly from 27 Dec to 15 May but increased significantly after 15 May. The content in the treatment showed no significant change before 22 Apr and then increased significantly. The chlorophyll a content of the treatment was significantly higher than that of the control on 7 and 15 May, with no significant differences on the other days. There was no significant difference in chlorophyll b content between the treatment and the control before 22 Apr, and the treatment value was significantly higher than that of the control. The chlorophyll a+b and a/b of the treatment were significantly higher than those of the control on 22 Apr and 15 May, and there was no significant difference at the other times. The carotenoid content of the treatment was significantly higher than that of the control on 22 Apr and 15 May, and there was no significant difference at the other times.

Effect of enhanced UV-B radiation on the Hill reaction of leaves

As seen in Fig. 3B, the trends of the Hill reaction activity were different between the treatment and control, with the control showing essentially no significant change and the treatment showing an increasing and then decreasing trend.

The treatments were not significantly different from the control until 7 Jan; the treatment values were significantly higher than the control values on 22 Apr, 7 May, and 15 May. Therefore, the treatment promoted the photolysis of water, which might further promote the photoreaction.

Effect of enhanced UV-B radiation on the photochemical quenching coefficient (qP) of leaves

Figure 3C shows that the qP of both the treatment and control showed a trend of increasing, then decreasing and then increasing again. The treatments showed significantly higher values than the control on 22 Apr and 7 and 22 May, with no significant differences on the other days. Thus, the treatment showed a trend of promoting electron transfer in the photosynthetic chain, which may further promote the light reaction.

Effect of enhanced UV-B radiation on the leaf dark response

RCA and Rubisco activities.

As shown in Fig. 3D, the activity of RCA increased significantly from 17 Jan to 22 Apr and then tended to stabilize. The activity in the control was stable at first, decreased significantly on 7 May, and then tended to stabilize. The RCA activity of the treatment was significantly higher than that of the control on 22 Apr and 7, 15, and 22 May.

Figure 3E shows that the activity of 1,5-diphosphate carboxylase (Rubisco) in the treatment and the control showed a similar trend of decreasing, then increasing, then decreasing and then increasing. On 7, 15, and 22 May, the Rubisco activity of the treatment was significantly higher than that of the control. The enhanced UV-B radiation treatment showed a tendency to significantly increase leaf RCA and Rubisco activities, which promoted the assimilation of CO2.

Relative expression levels of rbcL and rbcS.

Figure 3F shows that the relative expression level of the gene coding rbcL in the control increased significantly from 22 Apr to 15 May and then decreased significantly. The relative expression levels under the treatment first showed a stable trend; after 17 Jan, they began to increase significantly until 15 May and then decreased significantly. The expression level of rbcL under the treatment was significantly higher than that under the control on 22 Apr and 15 and 22 May.

Figure 3G shows that the relative expression level of the gene encoding rbcS under the control showed stability and then significantly increased after 15 May. The relative expression level showed a consistent and significant increase after 17 Jan. At the same time, the expression level of rbcS in the treatment was significantly higher than that in the control on 22 Apr and 15 May.

UV-B radiation at 96 kJ·m−2·d−1 enhanced the expression of rbcL and rbcS genes.

Discussion

Effects of enhanced UV-B radiation on the photosynthetic physiology of leaves, mature fruit ratio, and fruit quality.

As an indicator of the intensity of photosynthesis, photosynthetic pigment contents can reflect the changes in organs and tissues and the physiological photosynthetic ability of plants under environmental stress (Cutraro, 2005). Depending on the crop species and variety, the photosynthetic pigment content increases or decreases with increasing UV-B radiation intensity (Choi and Roh, 2003). The photosynthetic pigment content of ‘Guifei’ mango under 96 kJ·m−2·d−1 enhanced UV-B radiation changed significantly, and chlorophyll a, b, carotenoid, chlorophyll a+b, and a/b values increased significantly, which indicated an increased photosynthetic capacity (Mauzerall, 1976). It may be that the intensity of UV-B radiation did not reach the inhibition threshold of ‘Guifei’ mango but was beneficial to the enhancement of its photosynthetic capacity, which was consistent with the results of Yang et al. (2021). The chlorophyll a/b value was positively correlated with the degree of thylakoid stacking, reflecting that enhanced UV-B radiation treatment was beneficial to chloroplast thylakoid structure. Therefore, it is speculated that enhanced UV-B radiation may facilitate the accumulation of more assimilates by optimizing the stacking structure of chloroplast thylakoids, increasing the content of photosynthetic pigments and optimizing the composition ratio. Carotenoids, photoprotective pigments, dissipate absorbed UV-B radiation and scavenge free radicals (Liu et al., 2012). An elevated carotenoid content may be a protective mechanism initiated by the leaves after enhanced UV-B radiation treatment while enhancing the ability of the leaves to capture light energy.

Photosynthesis produces the materials and energy needed for plant growth and development and is sensitive to environmental changes (Chao et al., 2009). Numerous studies have shown that enhanced UV-B radiation adversely affects plants, leading to a decrease in the photosynthetic rate (Surabhi et al., 2009; Teramura et al., 2010). A study found that C3, C4, and CAM plants showed different performances under enhanced UV-B radiation (Basiouny et al., 2010), indicating that different species of plants had different responses to enhanced UV-B radiation. The photosynthetic rate of ‘Guifei’ mango treated with enhanced UV-B radiation was higher than that of ‘Guifei’ mango without UV-B radiation treatment. Previous studies on ‘Tainong No. 1’ and ‘Jinhuang’ mango have found that enhanced UV-B radiation inhibits photosynthesis, resulting in a decrease in the photosynthetic rate (Wang et al., 2020a, 2020b), but the results in this study were the opposite, which may have been caused by the differences in UV-B radiation resistance among different mango cultivars.

Li found that UV-B radiation promotes the ripening of highbush blueberries (Li et al., 2021). Some studies also found that under UV-B radiation at 150 μW/cm2, the fruit quality of grape berries was significantly improved, which was consistent with the results of our study (Fang and Wang, 2017). Our results showed that 96 kJ·m−2·d−1 enhanced UV-B radiation treatment could promote early ripening and improve the fruit quality of ‘Guifei’ mango. It is possible that enhanced UV-B radiation can enhance the photosynthetic function of leaves, thereby promoting fruit growth and early ripening.

Photoreaction changes.

When most plants are subjected to enhanced UV-B radiation stress, the activity of the PSII reaction center is decreased (Mishra et al., 2008), the PSII electron transport system is damaged, the primary photosynthetic reaction is hindered (Gonzalez-Mendoza et al., 2007; Zavafer et al., 2017), and the Hill reaction activity and photochemical quenching coefficient (qP) are decreased, resulting in reduced assimilation and a decreased net photosynthetic rate. However, the results showed that in ‘Guifei’ mango leaves under the 96 kJ·m−2·d−1 enhanced UV-B radiation treatment, the Hill reaction activity and qP showed an upward trend, contrary to previous studies. Hill reaction activity is positively correlated with photosynthetic capacity (Liang et al., 2006). Therefore, it is speculated that enhanced UV-B radiation may enhance the photoreaction activity of leaves, thus creating energy conditions for dark reactions to fix more CO2 and further enhancing the photosynthetic capacity.

Dark reaction changes.

Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) is a key enzyme in photosynthetic carbon assimilation that catalyzes both carbon reduction in photosynthesis and carbon oxidation in photorespiration (Miziorko and Lorimer, 1983). Among them, the Rubisco enzyme is composed of eight 56-kDa large subunits (rbcL) and eight 14-kDa small subunits (rbcS), which are encoded by chloroplast genes and nuclear genes. Although rbcL contains the active site of the Rubisco enzyme, recent studies have shown that rbcS has an important effect on the regulation of Rubisco enzyme activity and protein content (Cai et al., 2014). Abiotic stress leads to a decrease in Rubisco enzyme activity and large and small subunit protein contents, which in turn inhibits photosynthetic efficiency (Vassileva et al., 2011). It has been shown that enhanced UV-B radiation causes a decline in Rubisco large subunit gene expression and Rubisco enzyme carboxylation activity in ‘Tainong 1’ mango, but little has been reported about small subunit and Rubisco activating enzymes in mango. In its passive state, Rubisco must be activated by RCA to catalyze its activity (Portis, 1995); that is, the activity of Rubisco in plants depends on the degree of RCA activation. The activation of Rubisco is a key factor determining the carbon assimilation efficiency of leaves. In this article, the Rubisco and RCA enzyme activities in the leaves of ‘Guifei’ fruit trees treated with enhanced UV-B radiation at 96 kJ·m−2·d−1 were significantly increased, which was beneficial for improving the CO2 assimilation efficiency and photosynthetic electron transfer efficiency. The significantly increased RCA activity also ensured that Rubisco was active in the plant. Under this treatment, the genes encoding the key carbon assimilation enzymes rbcL and rbcS were significantly increased at the transcriptional level, increasing the amount of CO2 fixed by RuBP and thereby improving the carboxylation efficiency of Rubisco and the transport efficiency of photosynthates. Therefore, enhanced UV-B radiation treatment can upregulate the expression of key enzyme genes of photosynthetic carbon assimilation in ‘Guifei’ mango, promote the utilization rate of light energy, accelerate the Calvin cycle, and ultimately promote photosynthetic efficiency, which may be an important mechanism for the growth and development of ‘Guifei’ mango under 96 kJ·m−2·d−1 enhanced UV-B radiation treatment.

Conclusions

Artificially simulated enhanced UV-B radiation treatment at 96 kJ·m−2·d−1 can improve the photosynthetic pigment contents and chloroplast thylakoid stacking structure of adult leaves of ‘Guifei’ mango, as well as improve the light energy capture, water photolysis, electron transfer, and light energy conversion abilities; enhance the light reaction; and allow stronger assimilation. Treatment also increases key photosynthetic enzyme activities by increasing the expression of key genes, such as rbcL and rbcS, which enhances the CO2 fixation ability of leaves. On the basis of these two aspects, the enhanced UV-B radiation treatment increases the net photosynthetic rate of leaves and promotes the rapid accumulation of photosynthetic products, ultimately accelerating ‘Guifei’ mango ripening and improving fruit quality. This study advances our knowledge of the photosynthetic mechanism regulated by 96 kJ·m−2·d−1 enhanced UV-B radiation in ‘Guifei’ mango and lays an early foundation for understanding the related physiological processes. These results will aid in the development of new technologies for regulating ripening, which is challenging in ‘Guifei’ mango.

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  • He, Y., Zhan, F., Zu, Y., Xu, W. & Li, Y. 2015 Effects of enhanced UV-B radiation on culm charateristics and lodging index of two local rice varieties in Yuanvang terraces under field condition J. Appl. Ecol. 26 1 39 45 https://doi.org/10.13287/j.1001-9332.20141208.002. (In Chinese)

    • Search Google Scholar
    • Export Citation
  • Kakani, V.G., Reddy, K.R., Zhao, D. & Mohammed, A.R. 2003 Effects of ultraviolet-B radiation on cotton (Gossypium hirsutum L.) morphology and anatomy Ann. Bot. 91 7 817 826 https://doi.org/10.1093/aob/mcg086

    • Search Google Scholar
    • Export Citation
  • Krizek, D.T 2004 Influence of PAR and UV-A in determining plant sensitivity and photomorphogenic responses to UV-B radiation Photochem. Photobiol. 9 4 307 315 https://doi.org/10.1111/j.1751-1097.2004.tb00013.x

    • Search Google Scholar
    • Export Citation
  • Li, H 2000 Principles and techniques of plant physiological and biochemical experiments 134 138 Beijing Higher Education Press https://xueshu.baidu.com/usercenter/paper/show?paperid=9451ba3beb65814b9b02a7667177c1b5&site=xueshu_se

    • Search Google Scholar
    • Export Citation
  • Li, T., Yamane, H. & Tao, R. 2021 Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry Hort. Res. 8 1 67 https://doi.org/10.1038/s41438-021-00503-4

    • Search Google Scholar
    • Export Citation
  • Liang, C.J., Huang, X.H. & Zhou, Q. 2006 Effect of cerium on photosynthetic characteristics of soybean seedling exposed to supplementary ultraviolet-B radiation J. Environ. Sci. (China) 18 6 1147 1151 https://doi.org/10.1016/S1001-0742(06)60053-3

    • Search Google Scholar
    • Export Citation
  • Liu, B., Liu, X.B., Li, Y.S. & Herbert, S.J. 2013 Effects of enhanced UV-B radiation on seed growth characteristics and yield components in soybean Field Crops Res. 154 3 158 163 https://doi.org/10.1016/j.fcr.2013.08.006

    • Search Google Scholar
    • Export Citation
  • Liu, M., Bo, C., Zhou, S. & Liu, Y. 2012 Responses of the flavonoid pathway to UV-B radiation stress and the correlation with the lipid antioxidant characteristics in the desert plant Caryopteris mongolica Acta Ecol. Sin. 32 3 150 155 https://doi.org/10.1016/j.chnaes.2012.04.004

    • Search Google Scholar
    • Export Citation
  • Liu, M., Li, R., Fan, H. & Du, G.C. 2007 Effects of enhanced UV-B radiation on photosynthetic pigments and some enzymes in tobacco Xibei Zhiwu Xuebao 27 2 291 296 https://doi.org/10.1007/s10928-006-9043-z

    • Search Google Scholar
    • Export Citation
  • Luo, N.S., Liu, Y., Zhong, Z.C. & Zhou, Y.C. 2003 Effects of enhanced ultraviolet-B(UV-B) radiation on diurnal changes of photosynthesis and water use efficiency in Luffa cylindrica J South China Normal Univ. Nat. Sci. Ed. 28 3 436 439

    • Search Google Scholar
    • Export Citation
  • Ma, C.H., Chu, J.Z., Shi, X.F., Liu, C.Q. & Yao, X.Q. 2016 Effects of enhanced UV-B radiation on the nutritional and active ingredient contents during the floral development of medicinal chrysanthemum J. Photochem. Photobiol. B. 158 228 234 https://doi.org/10.1016/j.jphotobiol.2016.02.019

    • Search Google Scholar
    • Export Citation
  • Mao, B., Wang, Y., Zhao, T.H., Tian, R.R., Wang, W. & Ye, J.S. 2017 Combined effects of elevated O3 concentrations and enhanced UV-B radiation of the biometric and biochemical properties of soybean roots Front Plant Sci. 8 1568 https://doi.org/10.3389/fpls.2017.01568

    • Search Google Scholar
    • Export Citation
  • Mauzerall, D 1976 Chlorophyll and photosynthesis Philos. Trans. R. Soc. Lond. B Biol. Sci. 273 287 294 https://doi.org/10.1098/rstb.1976.0014

  • Mishra, V., Srivastava, G., Prasad, S.M. & Abraham, G. 2008 Growth, photosynthetic pigments and photosynthetic activity during seedling stage of cowpea (Vigna unguiculata) in response to UV-B and dimethoate Pestic. Biochem. Physiol. 92 1 30 37 https://doi.org/10.1016/j.pestbp.2008.05.003

    • Search Google Scholar
    • Export Citation
  • Miziorko, H.M. & Lorimer, G.H. 1983 Ribulose-1,5-bisphosphate carboxylase-oxygenase Annu. Rev. Biochem. 28 1 507 535 https://doi.org/10.1146/annurev.bi.52.070183.002451

    • Search Google Scholar
    • Export Citation
  • Neale, R.E., Barnes, P.W., Robson, T.M., Neale, P.J., Williamson, C.E., Zepp, R.G., Wilson, S.R., Madronich, S., Andrady, A.L., Heikkilä, A.M., Bernhard, G.H., Bais, A.F., Aucamp, P.J., Banaszak, A.T., Bornman, J.F., Bruckman, L.S., Byrne, S.N., Foereid, B., Häder, D.P., Hollestein, L.M., Hou, W.C., Hylander, S., Jansen, M.A.K., Klekociuk, A.R., Liley, J.B., Longstreth, J., Lucas, R.M., Martinez-Abaigar, J., McNeill, K., Olsen, C.M., Pandey, K.K., Rhodes, L.E., Robinson, S.A., Rose, K.C., Schikowski, T., Solomon, K.R., Sulzberger, B., Ukpebor, J.E., Wang, Q.W., Wängberg, S.Å., White, C.C., Yazar, S., Young, A.R., Young, P.J., Zhu, L. & Zhu, M. 2021 Environmental effects of stratospheric ozone depletion, UV radiation, and interactions with climate change: UNEP Environmental Effects Assessment Panel, Update 2020 Photochem. Photobiol. Sci. 20 1 1 67 https://doi.org/10.1007/s43630-020-00001-x

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    • Export Citation
  • Portis, A.R. Jr 1995 The regulation of Rubisco by Rubisco activase J. Expt. Bot. 46 1285 1291 https://doi.org/10.1093/jxb/46.special_issue.1285

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    • Export Citation
  • Rozema, J., van de Staaij, J., Björn, L.O. & Caldwell, M. 1997 UV-B as an environmental factor in plant life: Stress and regulation Trends Ecol. Evol. 12 1 22 28 https://doi.org/10.1016/S0169-5347(96)10062-8

    • Search Google Scholar
    • Export Citation
  • Saber, H., El-Sheekh, M.M., Ibrahim, A. & Alwaleed, E.A. 2020 Effect of UV-B radiation on amino acids profile, antioxidant enzymes and lipid peroxidation of some cyanobacteria and green algae Int. J. Radiat. 96 9 1 30 https://doi.org/10.1080/09553002.2020.1793025

    • Search Google Scholar
    • Export Citation
  • Surabhi, G.K., Reddy, K.R. & Singh, S.K. 2009 Photosynthesis, fluorescence, shoot biomass and seed weight responses of three cowpea [Vigna unguiculata (L.) Walp.] cultivars with contrasting sensitivity to UV-B radiation Environ. Exp. Bot. 66 2 160 171 https://doi.org/10.1016/j.envexpbot.2009.02.004

    • Search Google Scholar
    • Export Citation
  • Teramura, A.H., Ziska, L.H. & Sztein, A.E. 2010 Changes in growth and photosynthetic capacity of rice with increased UV-B radiation Physiol. Plant. 83 3 373 380 https://doi.org/10.1111/j.1399-3054.1991.tb00108.x

    • Search Google Scholar
    • Export Citation
  • Teramura, A.H 1983 Effects of ultraviolet-B radiation on the growth and yield of crop plants Physiol. Plant. 58 3 415 427 https://doi.org/10.1111/j.1399-3054.1983.tb04203.x

    • Search Google Scholar
    • Export Citation
  • Vassileva, V., Demirevska, K., Simova-Stoilova, L., Petrova, T. & Feller, U. 2011 Long-term field drought affects leaf protein pattern and chloroplast ultra structure of winter wheat in a cultivar-specific manner J. Agron. Crop Sci. 198 2 104 117 https://doi.org/10.1111/j.1439-037X.2011.00492.x

    • Search Google Scholar
    • Export Citation
  • Wang, H., Yang, C., Yue, K., Guo, Y. & Zhou, K 2020b The effects of different UV-B radiation on mango fruit quality and antioxidant properties Chinese J. Trop. Crops. 41 02 275 283 CNKI:SUN:RDZX.0.2020-02-011. (In Chinese)

    • Search Google Scholar
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  • Wang, H., Yue, K., Yang, C., Guo, Y. & Wang, P. 2020a 2020a. Physiological reasons for the inhibition of photosynthesis of mango leaves by enhanced UV-B radiation treatment Acta Hort. 47 02 242 252 https://doi.org/10.16420/j.issn.0513-353x.2019-0381

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    • Export Citation
  • Yang, Y., Guo, S., Yang, S., Zhang, Y., Bang, H., Meng, F., Duan, Y., Yang, Z., Yang, X., Yuan, J., Yue, X. & Fang, H. 2021 Effects of enhanced UV-B radiation on photosynthetic physiology and ultrastructure of mango leaves J. Fruit Trees. 38 09 1524 1539 https://doi.org/10.13925/j.cnki.gsxb.20200465. (In Chinese.)

    • Search Google Scholar
    • Export Citation
  • Yu, S. & Zheng, G. 1980 A preliminary study on the hill reaction activity of wheat chloroplasts J. Shandong Agricultural College. 02 45 52 https://kns.cnki.net/kcms/detail/detail.aspx?dbcode=CJFD&dbname=CJFD7984&filename=SCHO198002005&uniplatform=NZKPT&v=ZQik8OT8VJRboBWP0R_HmIXCQaKz66d_ lbTrpIYjqxtlhFlhKlQGZF33U9TqXukf

    • Search Google Scholar
    • Export Citation
  • Yuan, M., Yue, K., Wang, H., Guo, Y. & Zhou, K. 2019 Effects of enhanced UV-B radiation on photosynthesis, yield and quality of mango adult trees Guangxi Agric Sci. 49 05 930 937 https://doi.org/10.3969/j.issn.2095-1191.2018.05.15

    • Search Google Scholar
    • Export Citation
  • Yue, K., Wang, H., Guo, Y. & Zhou, K. 2019 Damage of enhanced UV-B radiation on photosynthetic structure of mango leaves J. South China Univ. Trop. Agric. 10 04 324 330 https://doi.org/10.15886/j.cnki.rdswxb.2019.04.004

    • Search Google Scholar
    • Export Citation
  • Zavafer, A., Koinuma, W., Chow, W.S., Cheah, M.H. & Mino, H. 2017 Mechanism of photodamage of the oxygen evolving Mn cluster of photosystem II by excessive light energy Sci. Rep. 7 1 7604 https://doi.org/10.1038/s41598-017-07671-1

    • Search Google Scholar
    • Export Citation
  • Zhang, Z., Zhu, Q., Hu, M., Gao, Z., An, F., Li, M. & Jiang, M. 2017 Low-temperature conditioning induces chilling tolerance in stored mango fruit Food Chem. 219 76 84 https://doi.org/10.1016/j.foodchem.2016.09.123

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    • Export Citation
  • Zhou, K., Li, S. & Yuan, M. 2019 Effects of enhanced UV-B radiation on mango plant yield, fruit quality and photosynthesis Redai Zuowu Xuebao 39 06 1102 1107 https://doi.org/10.3969/j.issn.1000-2561.2018.06.010

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Contributor Notes

K.Z. is the corresponding author. E-mail: zkb@hainanu.edu.cn.

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    Fig. 1.

    The mangoes were harvested 134 d after flowering.

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    Fig. 2.

    The effects of enhanced ultraviolet-B radiation on the mature fruit ratio. *Indicates a significant difference between the treatment and the control (P < 0.05), and the same as below.

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    Fig. 3.

    The effects of enhanced ultraviolet-B radiation on the net photosynthetic rate (Pn), Hill reaction activity, photochemical quenching coefficient, Rubisco activating enzyme, Rubisco, and relative expression of Rubisco large subunit and Rubisco small subunit genes in leaves. Note: The letters of the line chart indicate significant differences in the dynamic changes on different dates; different letters indicate significant differences, and the same letter indicates nonsignificant (P < 0.05).

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  • He, Y., Zhan, F., Zu, Y., Xu, W. & Li, Y. 2015 Effects of enhanced UV-B radiation on culm charateristics and lodging index of two local rice varieties in Yuanvang terraces under field condition J. Appl. Ecol. 26 1 39 45 https://doi.org/10.13287/j.1001-9332.20141208.002. (In Chinese)

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  • Kakani, V.G., Reddy, K.R., Zhao, D. & Mohammed, A.R. 2003 Effects of ultraviolet-B radiation on cotton (Gossypium hirsutum L.) morphology and anatomy Ann. Bot. 91 7 817 826 https://doi.org/10.1093/aob/mcg086

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  • Krizek, D.T 2004 Influence of PAR and UV-A in determining plant sensitivity and photomorphogenic responses to UV-B radiation Photochem. Photobiol. 9 4 307 315 https://doi.org/10.1111/j.1751-1097.2004.tb00013.x

    • Search Google Scholar
    • Export Citation
  • Li, H 2000 Principles and techniques of plant physiological and biochemical experiments 134 138 Beijing Higher Education Press https://xueshu.baidu.com/usercenter/paper/show?paperid=9451ba3beb65814b9b02a7667177c1b5&site=xueshu_se

    • Search Google Scholar
    • Export Citation
  • Li, T., Yamane, H. & Tao, R. 2021 Preharvest long-term exposure to UV-B radiation promotes fruit ripening and modifies stage-specific anthocyanin metabolism in highbush blueberry Hort. Res. 8 1 67 https://doi.org/10.1038/s41438-021-00503-4

    • Search Google Scholar
    • Export Citation
  • Liang, C.J., Huang, X.H. & Zhou, Q. 2006 Effect of cerium on photosynthetic characteristics of soybean seedling exposed to supplementary ultraviolet-B radiation J. Environ. Sci. (China) 18 6 1147 1151 https://doi.org/10.1016/S1001-0742(06)60053-3

    • Search Google Scholar
    • Export Citation
  • Liu, B., Liu, X.B., Li, Y.S. & Herbert, S.J. 2013 Effects of enhanced UV-B radiation on seed growth characteristics and yield components in soybean Field Crops Res. 154 3 158 163 https://doi.org/10.1016/j.fcr.2013.08.006

    • Search Google Scholar
    • Export Citation
  • Liu, M., Bo, C., Zhou, S. & Liu, Y. 2012 Responses of the flavonoid pathway to UV-B radiation stress and the correlation with the lipid antioxidant characteristics in the desert plant Caryopteris mongolica Acta Ecol. Sin. 32 3 150 155 https://doi.org/10.1016/j.chnaes.2012.04.004

    • Search Google Scholar
    • Export Citation
  • Liu, M., Li, R., Fan, H. & Du, G.C. 2007 Effects of enhanced UV-B radiation on photosynthetic pigments and some enzymes in tobacco Xibei Zhiwu Xuebao 27 2 291 296 https://doi.org/10.1007/s10928-006-9043-z

    • Search Google Scholar
    • Export Citation
  • Luo, N.S., Liu, Y., Zhong, Z.C. & Zhou, Y.C. 2003 Effects of enhanced ultraviolet-B(UV-B) radiation on diurnal changes of photosynthesis and water use efficiency in Luffa cylindrica J South China Normal Univ. Nat. Sci. Ed. 28 3 436 439

    • Search Google Scholar
    • Export Citation
  • Ma, C.H., Chu, J.Z., Shi, X.F., Liu, C.Q. & Yao, X.Q. 2016 Effects of enhanced UV-B radiation on the nutritional and active ingredient contents during the floral development of medicinal chrysanthemum J. Photochem. Photobiol. B. 158 228 234 https://doi.org/10.1016/j.jphotobiol.2016.02.019

    • Search Google Scholar
    • Export Citation
  • Mao, B., Wang, Y., Zhao, T.H., Tian, R.R., Wang, W. & Ye, J.S. 2017 Combined effects of elevated O3 concentrations and enhanced UV-B radiation of the biometric and biochemical properties of soybean roots Front Plant Sci. 8 1568 https://doi.org/10.3389/fpls.2017.01568

    • Search Google Scholar
    • Export Citation
  • Mauzerall, D 1976 Chlorophyll and photosynthesis Philos. Trans. R. Soc. Lond. B Biol. Sci. 273 287 294 https://doi.org/10.1098/rstb.1976.0014

  • Mishra, V., Srivastava, G., Prasad, S.M. & Abraham, G. 2008 Growth, photosynthetic pigments and photosynthetic activity during seedling stage of cowpea (Vigna unguiculata) in response to UV-B and dimethoate Pestic. Biochem. Physiol. 92 1 30 37 https://doi.org/10.1016/j.pestbp.2008.05.003

    • Search Google Scholar
    • Export Citation
  • Miziorko, H.M. & Lorimer, G.H. 1983 Ribulose-1,5-bisphosphate carboxylase-oxygenase Annu. Rev. Biochem. 28 1 507 535 https://doi.org/10.1146/annurev.bi.52.070183.002451

    • Search Google Scholar
    • Export Citation
  • Neale, R.E., Barnes, P.W., Robson, T.M., Neale, P.J., Williamson, C.E., Zepp, R.G., Wilson, S.R., Madronich, S., Andrady, A.L., Heikkilä, A.M., Bernhard, G.H., Bais, A.F., Aucamp, P.J., Banaszak, A.T., Bornman, J.F., Bruckman, L.S., Byrne, S.N., Foereid, B., Häder, D.P., Hollestein, L.M., Hou, W.C., Hylander, S., Jansen, M.A.K., Klekociuk, A.R., Liley, J.B., Longstreth, J., Lucas, R.M., Martinez-Abaigar, J., McNeill, K., Olsen, C.M., Pandey, K.K., Rhodes, L.E., Robinson, S.A., Rose, K.C., Schikowski, T., Solomon, K.R., Sulzberger, B., Ukpebor, J.E., Wang, Q.W., Wängberg, S.Å., White, C.C., Yazar, S., Young, A.R., Young, P.J., Zhu, L. & Zhu, M. 2021 Environmental effects of stratospheric ozone depletion, UV radiation, and interactions with climate change: UNEP Environmental Effects Assessment Panel, Update 2020 Photochem. Photobiol. Sci. 20 1 1 67 https://doi.org/10.1007/s43630-020-00001-x

    • Search Google Scholar
    • Export Citation
  • Portis, A.R. Jr 1995 The regulation of Rubisco by Rubisco activase J. Expt. Bot. 46 1285 1291 https://doi.org/10.1093/jxb/46.special_issue.1285

    • Search Google Scholar
    • Export Citation
  • Rozema, J., van de Staaij, J., Björn, L.O. & Caldwell, M. 1997 UV-B as an environmental factor in plant life: Stress and regulation Trends Ecol. Evol. 12 1 22 28 https://doi.org/10.1016/S0169-5347(96)10062-8

    • Search Google Scholar
    • Export Citation
  • Saber, H., El-Sheekh, M.M., Ibrahim, A. & Alwaleed, E.A. 2020 Effect of UV-B radiation on amino acids profile, antioxidant enzymes and lipid peroxidation of some cyanobacteria and green algae Int. J. Radiat. 96 9 1 30 https://doi.org/10.1080/09553002.2020.1793025

    • Search Google Scholar
    • Export Citation
  • Surabhi, G.K., Reddy, K.R. & Singh, S.K. 2009 Photosynthesis, fluorescence, shoot biomass and seed weight responses of three cowpea [Vigna unguiculata (L.) Walp.] cultivars with contrasting sensitivity to UV-B radiation Environ. Exp. Bot. 66 2 160 171 https://doi.org/10.1016/j.envexpbot.2009.02.004

    • Search Google Scholar
    • Export Citation
  • Teramura, A.H., Ziska, L.H. & Sztein, A.E. 2010 Changes in growth and photosynthetic capacity of rice with increased UV-B radiation Physiol. Plant. 83 3 373 380 https://doi.org/10.1111/j.1399-3054.1991.tb00108.x

    • Search Google Scholar
    • Export Citation
  • Teramura, A.H 1983 Effects of ultraviolet-B radiation on the growth and yield of crop plants Physiol. Plant. 58 3 415 427 https://doi.org/10.1111/j.1399-3054.1983.tb04203.x

    • Search Google Scholar
    • Export Citation
  • Vassileva, V., Demirevska, K., Simova-Stoilova, L., Petrova, T. & Feller, U. 2011 Long-term field drought affects leaf protein pattern and chloroplast ultra structure of winter wheat in a cultivar-specific manner J. Agron. Crop Sci. 198 2 104 117 https://doi.org/10.1111/j.1439-037X.2011.00492.x

    • Search Google Scholar
    • Export Citation
  • Wang, H., Yang, C., Yue, K., Guo, Y. & Zhou, K 2020b The effects of different UV-B radiation on mango fruit quality and antioxidant properties Chinese J. Trop. Crops. 41 02 275 283 CNKI:SUN:RDZX.0.2020-02-011. (In Chinese)

    • Search Google Scholar
    • Export Citation
  • Wang, H., Yue, K., Yang, C., Guo, Y. & Wang, P. 2020a 2020a. Physiological reasons for the inhibition of photosynthesis of mango leaves by enhanced UV-B radiation treatment Acta Hort. 47 02 242 252 https://doi.org/10.16420/j.issn.0513-353x.2019-0381

    • Search Google Scholar
    • Export Citation
  • Yang, Y., Guo, S., Yang, S., Zhang, Y., Bang, H., Meng, F., Duan, Y., Yang, Z., Yang, X., Yuan, J., Yue, X. & Fang, H. 2021 Effects of enhanced UV-B radiation on photosynthetic physiology and ultrastructure of mango leaves J. Fruit Trees. 38 09 1524 1539 https://doi.org/10.13925/j.cnki.gsxb.20200465. (In Chinese.)

    • Search Google Scholar
    • Export Citation
  • Yu, S. & Zheng, G. 1980 A preliminary study on the hill reaction activity of wheat chloroplasts J. Shandong Agricultural College. 02 45 52 https://kns.cnki.net/kcms/detail/detail.aspx?dbcode=CJFD&dbname=CJFD7984&filename=SCHO198002005&uniplatform=NZKPT&v=ZQik8OT8VJRboBWP0R_HmIXCQaKz66d_ lbTrpIYjqxtlhFlhKlQGZF33U9TqXukf

    • Search Google Scholar
    • Export Citation
  • Yuan, M., Yue, K., Wang, H., Guo, Y. & Zhou, K. 2019 Effects of enhanced UV-B radiation on photosynthesis, yield and quality of mango adult trees Guangxi Agric Sci. 49 05 930 937 https://doi.org/10.3969/j.issn.2095-1191.2018.05.15

    • Search Google Scholar
    • Export Citation
  • Yue, K., Wang, H., Guo, Y. & Zhou, K. 2019 Damage of enhanced UV-B radiation on photosynthetic structure of mango leaves J. South China Univ. Trop. Agric. 10 04 324 330 https://doi.org/10.15886/j.cnki.rdswxb.2019.04.004

    • Search Google Scholar
    • Export Citation
  • Zavafer, A., Koinuma, W., Chow, W.S., Cheah, M.H. & Mino, H. 2017 Mechanism of photodamage of the oxygen evolving Mn cluster of photosystem II by excessive light energy Sci. Rep. 7 1 7604 https://doi.org/10.1038/s41598-017-07671-1

    • Search Google Scholar
    • Export Citation
  • Zhang, Z., Zhu, Q., Hu, M., Gao, Z., An, F., Li, M. & Jiang, M. 2017 Low-temperature conditioning induces chilling tolerance in stored mango fruit Food Chem. 219 76 84 https://doi.org/10.1016/j.foodchem.2016.09.123

    • Search Google Scholar
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  • Zhou, K., Li, S. & Yuan, M. 2019 Effects of enhanced UV-B radiation on mango plant yield, fruit quality and photosynthesis Redai Zuowu Xuebao 39 06 1102 1107 https://doi.org/10.3969/j.issn.1000-2561.2018.06.010

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