Photochemical functioning of Dracocephalum kotschyi ecotypes under UVB
محورهای موضوعی : Stress Physiology
Zahra Mottaki
1
,
Ghader Habibi
2
,
Abbas Gholipour
3
,
Tahmineh Lohrasebi
4
1 - . Department of Biology, Payame Noor University, Tehran, Iran
2 - . Department of Biology, Payame Noor University, Tehran, Iran
3 - Department of Biology, Payame Noor University, Tehran, Iran
4 - Plant Molecular Genetics, Plant Bioproducts Department, National Institute for Genetic Engineering
کلید واژه: altitudinal gradient, Dracocephalum kotschyi, photochemical activity, UVB radiation,
چکیده مقاله :
The objective of the present study was to determine the efficacy of chlorophyll fluorescence analysis and to understand the specific photosynthetic parameters for detection of UVB radiation and high light (HL)-induced stress in Dracocephalum kotschyi plants under low and high altitudes. Seeds of high (3,300 m) and low (2,600 m) altitude ecotypes of D. kotschyi were sown in a growth chamber. Following a 3-month acclimation period, independent pots were chosen and exposed to light intensities including 400 and HL (800 µmol m-2 s-1) as well as with two levels of UVB (15 and 30 kJ m-2 d-1) for further 10 days. High altitude plants displayed more protection to photoinhibition in comparison to low-altitude plants. Under combined stress, only in high altitude plants, the levels of carotenoids correlated well with the maximal quantum yield of photosystem II (Fv/Fm), suggesting that the accumulation of antioxidant metabolites including carotenoids play a key role in enhancing resistance to stresses. Under combined stress condition, low-altitude plants exhibited the occurrence of photoinhibition, which was assessed by the analysis of Fv/Fm. Additionally, in low-altitude plants, under combined stress, IP-phases from the OJIP curve decreased due to a decrease in electron transport towards PSI. To sum up, this study explored the key OJIP parameters that can be used for distinguishing primary mode of action of HL and UVB on photosystem II in different D. kotschyi populations.
The objective of the present study was to determine the efficacy of chlorophyll fluorescence analysis and to understand the specific photosynthetic parameters for detection of UVB radiation and high light (HL)-induced stress in Dracocephalum kotschyi plants under low and high altitudes. Seeds of high (3,300 m) and low (2,600 m) altitude ecotypes of D. kotschyi were sown in a growth chamber. Following a 3-month acclimation period, independent pots were chosen and exposed to light intensities including 400 and HL (800 µmol m-2 s-1) as well as with two levels of UVB (15 and 30 kJ m-2 d-1) for further 10 days. High altitude plants displayed more protection to photoinhibition in comparison to low-altitude plants. Under combined stress, only in high altitude plants, the levels of carotenoids correlated well with the maximal quantum yield of photosystem II (Fv/Fm), suggesting that the accumulation of antioxidant metabolites including carotenoids play a key role in enhancing resistance to stresses. Under combined stress condition, low-altitude plants exhibited the occurrence of photoinhibition, which was assessed by the analysis of Fv/Fm. Additionally, in low-altitude plants, under combined stress, IP-phases from the OJIP curve decreased due to a decrease in electron transport towards PSI. To sum up, this study explored the key OJIP parameters that can be used for distinguishing primary mode of action of HL and UVB on photosystem II in different D. kotschyi populations.
Caldwell, M. M. 1971. Solar UV irradiation and the growth and development of higher plants. Photophysiology, 6, 131-177.
Chen, C.-I., K.-H. Lin, T.-C. Lin, M.-Y. Huang, Y.-C. Chen, C.-C. Huang and C.-W. Wang. 2023. Responses of photosynthesis and chlorophyll fluorescence during light induction in different seedling ages of Mahonia oiwakensis. Botanical Studies, 64, (1) 5.
Chouhan, N., R. M. Yadav, J. Pandey and R. Subramanyam. 2023. High light-induced changes in thylakoid supercomplexes organization from cyclic electron transport mutants of Chlamydomonas reinhardtii. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1864, (1) 148917.
Demmig-Adams, B., J. J. Stewart, M. López-Pozo, S. K. Polutchko and W. W. Adams Iii. 2020. Zeaxanthin, a molecule for photoprotection in many different environments. Molecules, 25, (24) 5825.
Dou, H., G. Niu and M. Gu. 2019. Pre-harvest UV-B radiation and photosynthetic photon flux density interactively affect plant photosynthesis, growth, and secondary metabolites accumulation in basil (Ocimum basilicum) plants. Agronomy, 9, (8) 434.
Faria-Silva, L., C. Gallon, P. Filgueiras and D. Silva. 2019. Irrigation improves plant vitality in specific stages of mango tree development according to photosynthetic efficiency. Photosynthetica, 57, (3) 820-829.
Guidi, L., E. Lo Piccolo and M. Landi. 2019. Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Frontiers in plant science, 10, 174.
Gupta, S. K., M. Sharma, F. Deeba and V. Pandey. 2017. Plant response: UV‐B avoidance mechanisms. UV‐B radiation: From environmental stressor to regulator of plant growth, 217-258.
Habibi, G. 2019. Effects of high light and chilling stress on photosystem II efficiency of aloe vera l. plants probing by chlorophyll a fluorescence measurements. Iranian Journal of Science and Technology, Transactions A: Science, 43, 7-13.
Habibi, G. and N. Ajory. 2015. The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low and high altitudes. Journal of plant research, 128, 987-994.
Habibi, G. and I. Turkan. 2021. Changes in crassulacean acid metabolism expression, chloroplast ultrastructure, photochemical and antioxidant activity in the Aloe vera during acclimation to combined drought and salt stress. Functional Plant Biology, 49, (1) 40-53.
Hamdani, S., M. Qu, C.-P. Xin, M. Li, C. Chu and X.-G. Zhu. 2015. Variations between the photosynthetic properties of elite and landrace Chinese rice cultivars revealed by simultaneous measurements of 820 nm transmission signal and chlorophyll a fluorescence induction. Journal of Plant Physiology, 177, 128-138.
Kalaji, H. M., K. Bosa, J. Kościelniak and K. Żuk-Gołaszewska. 2011. Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany, 73, 64-72.
Kalaji, H. M., A. Jajoo, A. Oukarroum, M. Brestic, M. Zivcak, I. A. Samborska, M. D. Cetner, I. Łukasik, V. Goltsev and R. J. Ladle. 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta physiologiae plantarum, 38, 1-11.
Kamran, M., K. Xie, J. Sun, D. Wang, C. Shi, Y. Lu, W. Gu and P. Xu. 2020. Modulation of growth performance and coordinated induction of ascorbate-glutathione and methylglyoxal detoxification systems by salicylic acid mitigates salt toxicity in choysum (Brassica parachinensis L.). Ecotoxicology and environmental safety, 188, 109877.
Kreslavski, V. D., V. V. Strokina, A. Y. Khudyakova, G. N. Shirshikova, A. A. Kosobryukhov, P. P. Pashkovskiy, S. Alwasel and S. I. Allakhverdiev. 2021. Effect of high-intensity light and UV-B on photosynthetic activity and the expression of certain light-responsive genes in A. thaliana phyA and phyB mutants. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1862, (8) 148445.
Küpper, H., Z. Benedikty, F. Morina, E. Andresen, A. Mishra and M. Trtílek. 2019. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant physiology, 179, (2) 369-381.
Liang, H.-Z., F. Zhu, R.-J. Wang, X.-H. Huang and J.-J. Chu. 2019. Photosystem II of Ligustrum lucidum in response to different levels of manganese exposure. Scientific Reports, 9, (1) 12568.
Lichtenthaler, H. K. and A. R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.
Lingwan, M., A. A. Pradhan, A. K. Kushwaha, M. A. Dar, L. Bhagavatula and S. Datta. 2023. Photoprotective role of plant secondary metabolites: Biosynthesis, photoregulation, and prospects of metabolic engineering for enhanced protection under excessive light. Environmental and Experimental Botany, 209, 105300.
Maxwell, K. and G. N. Johnson. 2000. Chlorophyll fluorescence—a practical guide. Journal of experimental botany, 51, (345) 659-668.
Muszyńska, E., K. M. Tokarz, M. Dziurka, M. Labudda, K. Dziurka and B. Tokarz. 2021. Photosynthetic apparatus efficiency, phenolic acid profiling and pattern of chosen phytohormones in pseudometallophyte Alyssum montanum. Scientific reports, 11, (1) 4135.
Sandmann, G. 2019. Antioxidant protection from UV-and light-stress related to carotenoid structures. Antioxidants, 8, (7) 219.
Takahashi, S. and M. R. Badger. 2011. Photoprotection in plants: a new light on photosystem II damage. Trends in plant science, 16, (1) 53-60.
Wu, X., B. Chen, J. Xiao and H. Guo. 2023. Different doses of UV-B radiation affect pigmented potatoes’ growth and quality during the whole growth period. Frontiers in Plant Science, 14, 1101172.
Yadav, A., D. Singh, M. Lingwan, P. Yadukrishnan, S. K. Masakapalli and S. Datta. 2020. Light signaling and UV‐B‐mediated plant growth regulation. Journal of Integrative Plant Biology, 62, (9) 1270-1292.
Zhang, Y., L. Feng, H. Jiang, Y. Zhang and S. Zhang. 2017. Different proteome profiles between male and female Populus cathayana exposed to UV-B radiation. Frontiers in Plant Science, 8, 320.
1405
Photochemical functioning of Dracocephalum kotschyi ecotypes under UVB
Zahra Mottaki1, Ghader Habibi1*, Abbas Gholipour1, Tahmineh Lohrasebi2
1. Department of Biology, Payame Noor University, Tehran, Iran
2. Plant Molecular Genetics, Plant Bioproducts Department, National Institute for Genetic Engineering
________________________________________________________________________________
Abstract
The objective of the present study was to determine the efficacy of chlorophyll fluorescence analysis and to understand the specific photosynthetic parameters for detection of UVB radiation and high light (HL)-induced stress in Dracocephalum kotschyi plants under low and high altitudes. Seeds of high (3,300 m) and low (2,600 m) altitude ecotypes of D. kotschyi were sown in a growth chamber. Following a 3-month acclimation period, independent pots were chosen and exposed to light intensities including 400 and HL (800 µmol m-2 s-1) as well as with two levels of UVB (15 and 30 kJ m-2 d-1) for further 10 days. High altitude plants displayed more protection to photoinhibition in comparison to low-altitude plants. Under combined stress, only in high altitude plants, the levels of carotenoids correlated well with the maximal quantum yield of photosystem II (Fv/Fm), suggesting that the accumulation of antioxidant metabolites including carotenoids play a key role in enhancing resistance to stresses. Under combined stress condition, low-altitude plants exhibited the occurrence of photoinhibition, which was assessed by the analysis of Fv/Fm. Additionally, in low-altitude plants, under combined stress, IP-phases from the OJIP curve decreased due to a decrease in electron transport towards PSI. To sum up, this study explored the key OJIP parameters that can be used for distinguishing primary mode of action of HL and UVB on photosystem II in different D. kotschyi populations.
Keywords: altitudinal gradient, Dracocephalum kotschyi, photochemical activity, UVB radiation
Mottaki, Z., Gh. Habibi, A. Gholipour, T. Lohrasebi. 2025. 'Photochemical functioning of Dracocephalum kotschyi ecotypes under UVB'. Iranian Journal of Plant Physiology 15 (2), 5473-5480.
|
To avoid the inhibitory effects of high light stress, plants have developed diverse morpho-physiological and biochemical adaptations which are defined as photoprotection mechanisms (Lingwan et al., 2023; Wu et al., 2023). Photoprotection mechanisms involved in minimizing photoinhibition of photosystem II (PSII) include the movement of chloroplasts, screening of photo radiation through changes in carotenoid and flavonoid biosynthesis, and the dissipation of absorbed light energy (Takahashi and Badger, 2011). Carotenoids, as a structural component of the light harvesting complexes (LHCs), are involved in light harvesting and photoprotection (Demmig-Adams et al., 2020). Under excess light, leaves accumulate carotenoids to alleviate photoinhibition of PSII which are associated with the dissipation of absorbed light energy via xanthophyll cycle (Habibi and Turkan, 2021).
Moreover, high-light stress is often accompanied by higher doses of UV. In addition, higher dosages of UV radiation on plants lead to accumulation of ROS and DNA damage associated with the changes in metabolites (Yadav et al., 2020). Leaf chlorophyll a fluorescence transient (O-J-I-P) provides detailed information associated with status and function of photosystem II (PSII) reaction centers under environmental stresses (Habibi, 2019). The JIP test provides the information about the energy flow in thylakoid membranes, the function of the photosynthetic structures and the trapping of excitation energy and electron transport, to identify plant stress in plant research (Habibi and Turkan, 2021).
Thus, long-term photoprotective mechanisms provide the survival of plants growing at high altitudes under different stresses in their natural habitats. Since previous studies were manipulated in response to individual UVB radiation and high light stress, we recorded, for the first time, the effects of combined stress (HL+UVB) on the regulation of photoprotective mechanisms in medicinal Dracocephalum kotschyi plants. There is no information about the possible differences in the role of UVB radiation in Dracocephalum kotschyi plants under low and high altitudes. Furthermore, we presumed that the significant difference in photoprotection mechanisms and condition of photosynthetic electron flux exists between low- and high-altitude plants. We, therefore, organized experiments to study the differences in the mechanisms involved in photoprotection of chloroplasts in low- and high- altitude Dracocephalum kotschyi plants, in order to recognize the population differentiation of photochemical functioning.
Materials and Methods
Plant material and treatments
High- and low-altitude ecotypes of Dracocephalum kotschyi were prepared from high (36°13′N, 51°27′W; 3,300 m) and low (36°13′N, 52°32′W; 2,600 m) altitude sites, located in Mazandaran (in central-northern part of Iran). Three to five seeds of Dracocephalum kotschyi were sown in plastic pots, which was prepared by mixing of sandy soil with peat moss and perlite, and were irrigated with distilled water every 7 days. Plants were grown under day/night temperature of 25 °C/14 °C, 16/8 h day/night cycle, and a daytime photon flux density of 400 μmol m–2 s–1 for a period of three months prior to the start of experiments. Following the 3 months acclimation period, independent pots were chosen randomly and allocated to measurements. The mature plants were then grown under irradiation with UVB and high-intensity light. Thereafter, plants were exposed to light intensities including 400 and high light (HL, 800 µmol m-2 s-1) as well as with two levels of ultraviolet-B irradiation (UVB 15 and 30 kJ m-2 d-1) for further 10 days. The photosynthetic active radiation (PAR, 400-700 nm) was supplied by cool white fluorescent lamps, and for UV radiation treatments, UVB fluorescent lamps (40 W, Philips, Germany) were used. The spectral outputs of the three lighting conditions were recorded using calibrated spectrophotometer and biologically effective UV doses employed were 15 and 30 kJ m-2 d-1 calculated according to Caldwell (1971). Fully expanded leaves were assigned to measurements of chlorophyll fluorescence and other analysis.
Measurements of total carotenoids, chlorophyll a and b
To estimate chlorophylls and carotenoids concentrations, after extraction of pigments in the cold acetone and permitting the samples to stand for 24 h in the dark at 4 °C, the homogenate was filtered, and then measurements were made spectrophotometrically at 400–700 nm (Lichtenthaler and Wellburn, 1983).
Determination of chlorophyll a fluorescence parameters
Fig. I. The effects of UVB radiation or high light alone and their combination on the chlorophyll contents in leaves of Dracocephalum kotschyi plants growing at low and high altitudes; bars indicated with the same letter within each altitude site are not significantly different (p<0.05, Tukey test). Values are the mean ± SD (n=4).
|
Fo: A parameter that describes minimum fluorescence, when all PSII reaction centers (RC) are open
Fm: A parameter that describes maximum fluorescence, when all PSII reaction centers are closed
Fv: Variable fluorescence
Fv/Fm: A parameter that characterizes the maximum quantum yield of PSII
Fv/Fo: The oxygen-evolving complex efficiency on the donor side of the PSII
φEo: A parameter that describes the quantum yield related to the reduction of end acceptors of PSI per photon absorbed
PIabs: A parameter that represents the performance index
Statistical Analysis
Experiments were performed using the completely randomized design with four independent replications. Analysis of variance (ANOVA) was employed to compare the data means at the same time point, and Tukey test (P<0.05) was used to record significant differences between means. The achieved data on Chl fluorescence were analyzed and conducted using the PEA Plus ver. 1.10 software. Correlation analysis using Spearman Rank Order Correlation in Sigma Stat (3.5) software was employed to assess the relationship between parameters.
Results
Fig. III. The effects of UVB radiation or high light alone and their combination on the maximum quantum yield (Fv/Fm) and oxygen-evolving complex efficiency of PSII (Fv/Fo) in leaves of Dracocephalum kotschyi plants growing at low and high altitudes; bars with the same letter within each altitude site are not significantly different (p<0.05, Tukey test). Values are the mean ± SD (n=4).
|
Fig. IV. The effects of UVB radiation or high light alone and their combination on the quantum yield of electron transport (φEo) and performance index (PIabs) in leaves of Dracocephalum kotschyi plants growing at low and high altitudes; bars with the same letter within each altitude site are not significantly different (p<0.05, Tukey test). Values are the mean ± SD (n=4).
|
In low-altitude plants, a clear reduction in the relative amplitude of the IP (Fm) phase was recorded in leaves treated with UVB or HL alone and their combination (Fig. V). However, the OJ part of the fluorescence rise was not affected by UVB and HL compared to IP part of the fluorescence rise. Similar results were found only after UVB15 or HL alone and their combination in high-altitude plants with respect to control plants. Interestingly, we observed that the UV-B irradiance at a dose of 30 caused an increase in the OJ phase of the fluorescence rise under both control and HL conditions (Fig. V).
Fig. VI. Correlation between values of total phenolic and malondialdehyde (MDA) recorded in Dracocephalum kotschyi plants growing at low and high altitudes under UVB radiation or high light stress; ns: non-significant, * and **: significant at the 5% and 1% levels of probability, respectively.
|
Fig. V. The effects of UVB radiation or high light alone and their combination on the chlorophyll a fluorescence induction curve of Dracocephalum kotschyi leaves growing at low and high altitudes; bars with the same letter within each altitude site are not significantly different (p<0.05, Tukey test). Values are the mean ± SD (n=8).
|
Discussion
Our results revealed that UVB stress caused further decreases in chlorophyll content of HL-exposed plants, which may lead to a decline in the photosynthetic capacity of low- and high-altitude plants. Dou et al., (2019)found similar results in basil (Ocimum basilicum) plants and observed a significant decrease in the chlorophyll content after UVB radiation, probably via degradation or retardation of enzymes involved in the chlorophyll biosynthesis (Yadav et al., 2020). In addition, priming of plants with UVB15 significantly increased the leaf content of carotenoids under the HL stress. However, in high altitude plants, the degree of increase in carotenoid contents was higher than the low altitude plants. Owing to the protective effects of carotenoids in the dissipation of absorbed light energy as thermal energy (Habibi, 2019; Habibi and Ajory, 2015), this higher accumulation of carotenoids plays a crucial role in plant photoprotection under HL and UVB stress (Demmig-Adams et al., 2020). In low altitude plants, the decrease in Fv/Fm showed the occurrence of photoinhibition of PSII (Chen et al., 2023; Guidi et al., 2019) under UVB+HL treatments, which was coincident with the largest decrease in Fv/Fo, quantum yield of ϕEo and PIabs. This decrease in Fv/Fo may reflect the decline in the water-splitting complex activity at the donor site of PSII (Habibi and Ajory, 2015; Kalaji et al., 2016). As compared to low altitude plants, the Fv/Fm and Fv/Fo were not affected by UVB+HL treatments in high altitude plants, characterizing proper functioning of PSII as well as more tolerance to photoinhibition. This intensification of photoprotection activity corresponded with a significant accumulation of carotenoids. High carotenoids content has a role in the light harvesting and photoprotection processes via xanthophyll cycle (Chouhan et al., 2023; Demmig-Adams et al., 2020; Faria-Silva et al., 2019). In fact, higher level of carotenoids can provide protection of chloroplasts under high light stress conditions (Sandmann, 2019).
To further study the effects of HL and UVB on photosystem II (PSII) electron transport chain components of leaves, we assayed the typical OJIP chlorophyll a fluorescence transient. We also recorded changes in the OJIP curve in response to environmental stress, to record the status of the electron transport activity (Liang et al., 2019; Maxwell and Johnson, 2000). The changes in OJIP transient reflect differences in the efficiency of the chlorophyll antenna involved in capturing light energy and conduct to the electron acceptor, plastoquinone QA (Küpper et al., 2019). In both low- and high-altitude plants, after exposure of the leaves to HL alone, UVB15 alone, or their combination, a clear reduction in the IP (Fm) phase was recorded, which may be due to the suppression of the content of reaction centers in PSI (Gupta et al., 2017). Interestingly, UVB30 either with or without HL increased the IP phase only in high altitude plants. Indeed, the IP phase may be related to the electron transport carriers to the (electron) acceptor side of PSI (Hamdani et al., 2015; Muszyńska et al., 2021) as well as to the amount of PSI (Muszyńska et al., 2021). Here, we showed that there is a higher IP phase in high-altitude plants in comparison to low-altitude plants , which may correlate to the higher PSI/PSII ratio in high-altitude plants in comparison with low-altitude plants (Zhang et al., 2017); however, a higher IP phase could have multiple causes, and further analyses are required to understand the effects of altitude on the chlorophyll a fluorescence transient. In the high-altitude leaves, we assume that the prevention of stress-induced reduction of photosynthetic activity under HL and UVB conditions was due to the increased content of carotenoids and UV-absorbing pigments (Kreslavski et al., 2021)as compared with the low-altitude plants. Indeed, high-altitude plants exhibited more tolerance to combined stress through maintenance non-enzymatic antioxidant pools, and this may lead to the conservation of Fv/Fm and Fv/Fo, as indices of photochemical activity (Kamran et al., 2020).
Conclusion
In conclusion, significant variation in stress tolerance was detected between low- and high-altitude plants, which was probably due to their altitudinal distributions. The exposure of low altitude plants to combined stress resulted in the occurrence of photoinhibition, which was correlated with the largest decrease in Fv/Fo, ϕEo and PIabs. In comparison, when high-altitude plants were exposed to stress conditions (UVB+HL), photoprotective mechanisms were activated, leading to acclimation to excess light through the accumulation of antioxidant metabolites including carotenoids and consequently, higher photochemical functioning. Since in low-altitude plants, under HL and UVB stress, the OJIP curve has been flattened because of reduction of electron transport towards PSI, we explored the key OJIP parameters that can be used for distinguishing primary mode of action of HL and UVB on photosystem II in different D. kotschyi populations.
References
Caldwell, M. M. 1971. Solar UV irradiation and the growth and development of higher plants. Photophysiology, 6, 131-177.
Chen, C.-I., K.-H. Lin, T.-C. Lin, M.-Y. Huang, Y.-C. Chen, C.-C. Huang and C.-W. Wang. 2023. Responses of photosynthesis and chlorophyll fluorescence during light induction in different seedling ages of Mahonia oiwakensis. Botanical Studies, 64, (1) 5.
Chouhan, N., R. M. Yadav, J. Pandey and R. Subramanyam. 2023. High light-induced changes in thylakoid supercomplexes organization from cyclic electron transport mutants of Chlamydomonas reinhardtii. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1864, (1) 148917.
Demmig-Adams, B., J. J. Stewart, M. López-Pozo, S. K. Polutchko and W. W. Adams Iii. 2020. Zeaxanthin, a molecule for photoprotection in many different environments. Molecules, 25, (24) 5825.
Dou, H., G. Niu and M. Gu. 2019. Pre-harvest UV-B radiation and photosynthetic photon flux density interactively affect plant photosynthesis, growth, and secondary metabolites accumulation in basil (Ocimum basilicum) plants. Agronomy, 9, (8) 434.
Faria-Silva, L., C. Gallon, P. Filgueiras and D. Silva. 2019. Irrigation improves plant vitality in specific stages of mango tree development according to photosynthetic efficiency. Photosynthetica, 57, (3) 820-829.
Guidi, L., E. Lo Piccolo and M. Landi. 2019. Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Frontiers in plant science, 10, 174.
Gupta, S. K., M. Sharma, F. Deeba and V. Pandey. 2017. Plant response: UV‐B avoidance mechanisms. UV‐B radiation: From environmental stressor to regulator of plant growth, 217-258.
Habibi, G. 2019. Effects of high light and chilling stress on photosystem II efficiency of aloe vera l. plants probing by chlorophyll a fluorescence measurements. Iranian Journal of Science and Technology, Transactions A: Science, 43, 7-13.
Habibi, G. and N. Ajory. 2015. The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low and high altitudes. Journal of plant research, 128, 987-994.
Habibi, G. and I. Turkan. 2021. Changes in crassulacean acid metabolism expression, chloroplast ultrastructure, photochemical and antioxidant activity in the Aloe vera during acclimation to combined drought and salt stress. Functional Plant Biology, 49, (1) 40-53.
Hamdani, S., M. Qu, C.-P. Xin, M. Li, C. Chu and X.-G. Zhu. 2015. Variations between the photosynthetic properties of elite and landrace Chinese rice cultivars revealed by simultaneous measurements of 820 nm transmission signal and chlorophyll a fluorescence induction. Journal of Plant Physiology, 177, 128-138.
Kalaji, H. M., K. Bosa, J. Kościelniak and K. Żuk-Gołaszewska. 2011. Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany, 73, 64-72.
Kalaji, H. M., A. Jajoo, A. Oukarroum, M. Brestic, M. Zivcak, I. A. Samborska, M. D. Cetner, I. Łukasik, V. Goltsev and R. J. Ladle. 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta physiologiae plantarum, 38, 1-11.
Kamran, M., K. Xie, J. Sun, D. Wang, C. Shi, Y. Lu, W. Gu and P. Xu. 2020. Modulation of growth performance and coordinated induction of ascorbate-glutathione and methylglyoxal detoxification systems by salicylic acid mitigates salt toxicity in choysum (Brassica parachinensis L.). Ecotoxicology and environmental safety, 188, 109877.
Kreslavski, V. D., V. V. Strokina, A. Y. Khudyakova, G. N. Shirshikova, A. A. Kosobryukhov, P. P. Pashkovskiy, S. Alwasel and S. I. Allakhverdiev. 2021. Effect of high-intensity light and UV-B on photosynthetic activity and the expression of certain light-responsive genes in A. thaliana phyA and phyB mutants. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1862, (8) 148445.
Küpper, H., Z. Benedikty, F. Morina, E. Andresen, A. Mishra and M. Trtílek. 2019. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant physiology, 179, (2) 369-381.
Liang, H.-Z., F. Zhu, R.-J. Wang, X.-H. Huang and J.-J. Chu. 2019. Photosystem II of Ligustrum lucidum in response to different levels of manganese exposure. Scientific Reports, 9, (1) 12568.
Lichtenthaler, H. K. and A. R. Wellburn. 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.
Lingwan, M., A. A. Pradhan, A. K. Kushwaha, M. A. Dar, L. Bhagavatula and S. Datta. 2023. Photoprotective role of plant secondary metabolites: Biosynthesis, photoregulation, and prospects of metabolic engineering for enhanced protection under excessive light. Environmental and Experimental Botany, 209, 105300.
Maxwell, K. and G. N. Johnson. 2000. Chlorophyll fluorescence—a practical guide. Journal of experimental botany, 51, (345) 659-668.
Muszyńska, E., K. M. Tokarz, M. Dziurka, M. Labudda, K. Dziurka and B. Tokarz. 2021. Photosynthetic apparatus efficiency, phenolic acid profiling and pattern of chosen phytohormones in pseudometallophyte Alyssum montanum. Scientific reports, 11, (1) 4135.
Sandmann, G. 2019. Antioxidant protection from UV-and light-stress related to carotenoid structures. Antioxidants, 8, (7) 219.
Takahashi, S. and M. R. Badger. 2011. Photoprotection in plants: a new light on photosystem II damage. Trends in plant science, 16, (1) 53-60.
Wu, X., B. Chen, J. Xiao and H. Guo. 2023. Different doses of UV-B radiation affect pigmented potatoes’ growth and quality during the whole growth period. Frontiers in Plant Science, 14, 1101172.
Yadav, A., D. Singh, M. Lingwan, P. Yadukrishnan, S. K. Masakapalli and S. Datta. 2020. Light signaling and UV‐B‐mediated plant growth regulation. Journal of Integrative Plant Biology, 62, (9) 1270-1292.
Zhang, Y., L. Feng, H. Jiang, Y. Zhang and S. Zhang. 2017. Different proteome profiles between male and female Populus cathayana exposed to UV-B radiation. Frontiers in Plant Science, 8, 320.
