journal article·2023-02-27Open access

Comparative Analysis of Primary Photosynthetic Reactions Assessed by OJIP Kinetics in Three Brassica Crops after Drought and Recovery

Jasenka Antunović Dunić, Selma Mlinarić, Iva Pavlović, Hrvoje Lepeduš, Branka Salopek-Sondi

Applied Sciences· Volume 13· Issue 5

Abstract

Plant drought tolerance depends on adaptations of the photosynthetic apparatus to changing environments triggered by water deficit. The seedlings of three Brassica crops differing in drought sensitivity, Brassica oleracea L. var. capitata—white cabbage, Brassica oleracea L. var. acephala—kale, and Brassica rapa L. var. pekinensis—Chinese cabbage, were exposed to drought by withholding water. Detailed insight into the photosynthetic machinery was carried out when the seedling reached a relative water content of about 45% and after re-watering by analyzing the OJIP kinetics. The key objective of this study was to find reliable parameters for distinguishing drought−tolerant and drought-sensitive varieties before permanent structural and functional changes in the photosynthetic apparatus occur. According to our findings, an increase in the total performance index (PItotal) and structure–function index (SFI), positive L and K bands, total driving forces (ΔDF), and drought resistance index (DRI) suggest drought tolerance. At the same time, susceptible varieties can be distinguished based on negative L and K bands, PItotal, SFI, and the density of reaction centers (RC/CS0). Kale proved to be the most tolerant, Chinese cabbage was moderately susceptible, and white cabbage showed high sensitivity to the investigated drought stress. The genetic variation revealed among the selected Brassica crops could be used in breeding programs and high-precision crop management.
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Research context

OpenAlex topics: Plant Stress Responses and Tolerance · Photosynthetic Processes and Mechanisms · Plant responses to elevated CO2

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Biology, Josip Juraj Strossmayer University of Osijek, 31000 Osijek, Croatia

Laboratory of Growth Regulators, Faculty of Science of Palacký University & Institute of Experimental Botany of the Czech Academy of Sciences, 78371 Olomouc, Czech Republic

Laboratory for Chemical Biology, Department of Molecular Biology, Ruđer Bošković Institute, 10000 Zagreb, Croatia

Faculty of Humanities and Social Sciences, Josip Juraj Strossmayer University of Osijek, 31000 Osijek, Croatia

Faculty of Dental Medicine and Health, Josip Juraj Strossmayer University of Osijek, 31000 Osijek, Croatia

Funding

Croatian Science Foundation

References (100+)

Show source-provided references
1. El-Esawi, M.A. (2018). Brassica Germplasm—Characterization, Breeding and Utilization, InTech.10.5772/intechopen.71706 ↗
2. Pua, E.-C., and Douglas, C.J. (2004). Brassica, Springer.10.1007/978-3-662-06164-0 ↗
3. FAO (2022). FAOSTAT Analytical Brief Series No. 41, FAO.
4. Biondi, F., Balducci, F., Capocasa, F., Visciglio, M., Mei, E., Vagnoni, M., Mezzetti, B., and Mazzoni, L. (2021). Environmental Conditions and Agronomical Factors Influencing the Levels of Phytochemicals in Brassica Vegetables Responsible for Nutritional and Sensorial Properties. Appl. Sci., 11.10.3390/app11041927 ↗
5. Nutritional and Phytochemical Value of Brassica Crops from the Agri-food Perspective10.1111/aab.12318 ↗
6. Hedges, L., and Lister, C. (2006). Nutritional Attributes of Brassica Vegetables, New Zealand Institute for Crop & Food Research Ltd.
7. Kale (Brassica oleracea var. acephala) as a Superfood: Review of the Scientific Evidence behind the Statement10.1080/10408398.2018.1454400 ↗
8. Early Brassica Crops Responses to Salinity Stress: A Comparative Analysis between Chinese Cabbage, White Cabbage, and Kale10.3389/fpls.2019.00450 ↗
9. Pavlović, I., Petřík, I., Tarkowská, D., Lepeduš, H., Vujčić Bok, V., Radić Brkanac, S., Novák, O., and Salopek-Sondi, B. (2018). Correlations between Phytohormones and Drought Tolerance in Selected Brassica Crops: Chinese Cabbage, White Cabbage and Kale. Int. J. Mol. Sci., 19.10.3390/ijms19102866 ↗
10. Crop Photosynthesis for the Twenty-First Century10.1007/s11120-021-00869-5 ↗
11. Tripathi, D.K., Pratap Singh, V., Chauhan, D.K., Sharma, S., Prasad, S.M., Dubey, N.K., and Ramawat, N. (2020). Plant Life Under Changing Environment, Academic Press.
12. Climate Trends and Global Crop Production Since 198010.1126/science.1204531 ↗
13. Crop Production under Drought and Heat Stress: Plant Responses and Management Options10.3389/fpls.2017.01147 ↗
14. Drought Stress Tolerance in Plants: Interplay of Molecular, Biochemical and Physiological Responses in Important Development Stages10.3390/physiologia2040015 ↗
15. Drought-Induced Responses of Photosynthesis and Antioxidant Metabolism in Higher Plants10.1016/j.jplph.2004.01.013 ↗
16. Plant Responses to Drought and Stress
17. Plant Adaptations to the Combination of Drought and High Temperatures10.1111/ppl.12540 ↗
18. Improving Photosynthesis10.1104/pp.113.219006 ↗
19. Recent Progress in Drought and Salt Tolerance Studies in Brassica Crops10.1270/jsbbs.64.60 ↗
20. Adjustment of Photosynthetic Activity to Drought and Fluctuating Light in Wheat10.1111/pce.13756 ↗
21. Impact of Drought on Photosynthesis: Molecular Perspective10.1016/j.plgene.2017.04.003 ↗
22. Limitation to Photosynthesis in Water-stressed Leaves: Stomata vs. Metabolism and the Role of ATP10.1093/aob/mcf110 ↗
23. Mesophyll Conductance to CO2 and Rubisco as Targets for Improving Intrinsic Water Use Efficiency in C3 Plants10.1111/pce.12622 ↗
24. Energy Dissipation in C3 Plants under Drought10.1071/FP02015 ↗
25. Photosynthesis and Drought: Can We Make Metabolic Connections from Available Data?10.1093/jxb/erq340 ↗
26. Mechanisms Underlying Plant Resilience to Water Deficits: Prospects for Water-Saving Agriculture10.1093/jxb/erh269 ↗
27. Causes of Decreased Photosynthetic Rate and Metabolic Capacity in Water-Deficient Leaf Cells: A Critical Evaluation of Mechanisms and Integration of Processes10.1093/aob/mcn244 ↗
28. Photosynthetic Control of Electron Transport and the Regulation of Gene Expression10.1093/jxb/ers013 ↗
29. Reactive Oxygen Species Homeostasis and Signalling during Drought and Salinity Stresses10.1111/j.1365-3040.2009.02041.x ↗
30. Chloroplast ROS and Stress Signaling10.1016/j.xplc.2021.100264 ↗
31. Physiological and Anatomical Changes in Two Rapeseed (Brassica napus L.) Genotypes under Drought Stress Conditions10.1016/j.ocsci.2021.04.003 ↗
32. Physiological Response to Different Irradiation Regimes during Barley Seedlings Growth Followed by Drought Stress under Non-Photoinhibitory Light
33. Reactions of Egyptian Landraces of Hordeum vulgare and Sorghum bicolor to Drought Stress, Evaluated by the OJIP Fluorescence Transient Analysis10.1007/s11738-012-1077-9 ↗
34. Implications of Intra-Seasonal Climate Variations on Chlorophyll a Fluorescence and Biomass in Winter Barley Breeding Program10.32615/ps.2020.053 ↗
35. Drought-Induced Modifications of Photosynthetic Electron Transport in Intact Leaves: Analysis and Use of Neural Networks as a Tool for a Rapid Non-Invasive Estimation10.1016/j.bbabio.2012.04.018 ↗
36. Impact of Drought, Heat, and Their Combination on Chlorophyll Fluorescence and Yield of Wild Barley (Hordeum spontaneum)
37. Can Chlorophyll-a Fluorescence Parameters Be Used as Bio-Indicators to Distinguish between Drought and Salinity Stress in Tilia cordata Mill?10.1016/j.envexpbot.2017.11.001 ↗
38. Drought-Induced Changes in Photosynthetic Electron Transport in Maize Probed by Prompt Fluorescence, Delayed Fluorescence, P700 and Cyclic Electron Flow Signals10.1016/j.envexpbot.2018.11.005 ↗
39. Jennings, R.C., Zucchelli, G., Ghetti, F., and Colombetti, G. (1996). Light as an Energy Source and Information Carrier in Plant Physiology, Springer US.10.1007/978-1-4613-0409-8 ↗
40. Chlorophyll Fluorescence, Photoinhibition and Abiotic Stress: Does It Make Any Difference the Fact to Be a C3 or C4 Species?10.3389/fpls.2019.00174 ↗
41. Moustakas, M., Sperdouli, I., and Moustaka, J. (2022). Early Drought Stress Warning in Plants: Color Pictures of Photosystem II Photochemistry. Climate, 10.10.3390/cli10110179 ↗
42. Chlorophyll a Fluorescence Analysis along a Vertical Gradient of the Crown in a Poplar (Oxford Clone) Subjected to Ozone and Water Stress10.1093/treephys/tps062 ↗
43. Mechanisms of Energy Dissipation in Peanut under Water Stress10.1007/s11099-006-0043-4 ↗
44. Variable Chlorophyll Fluorescence and Its Use for Assessing Physiological Condition of Plant Photosynthetic Apparatus10.1134/S1021443716050058 ↗
45. Delayed Chlorophyll Fluorescence as a Monitor for Physiological State of Photosynthetic Apparatus10.1080/13102818.2009.10818461 ↗
46. Chlorophyll a Fluorescence as a Tool to Monitor Physiological Status of Plants under Abiotic Stress Conditions10.1007/s11738-016-2113-y ↗
47. Strasser, R.J., Tsimilli-Michael, M., and Srivastava, A. (2004). Chlorophyll a Fluorescence, Springer.
48. Screening for Drought Tolerance in Mutant Germplasm of Sesame (Sesamum indicum) Probing by Chlorophyll a Fluorescence10.1016/j.envexpbot.2012.02.015 ↗
49. Physiological Insights on Soybean Response to Drought10.1016/j.agwat.2022.107620 ↗
50. Probing the Responses of Barley Cultivars (Hordeum vulgare L.) by Chlorophyll a Fluorescence OLKJIP under Drought Stress and Re-Watering10.1016/j.envexpbot.2007.01.002 ↗
51. PEG-Induced Physiological Drought for Screening Winter Wheat Genotypes Sensitivity—Integrated Biochemical and Chlorophyll a Fluorescence Analysis10.3389/fpls.2022.987702 ↗
52. Drought Tolerance in Brassica napus Is Accompanied with Enhanced Antioxidative Protection, Photosynthetic and Hormonal Regulation at Seedling Stage10.1111/ppl.13375 ↗
53. Potato Response to Drought Stress: Physiological and Growth Basis10.3389/fpls.2021.698060 ↗
54. Effects of Drought Stress on Photosynthetic and Physiological Parameters of Tomato10.21273/JASHS04725-19 ↗
55. Shin, Y.K., Bhandari, S.R., Jo, J.S., Song, J.W., and Lee, J.G. (2021). Effect of Drought Stress on Chlorophyll Fluorescence Parameters, Phytochemical Contents, and Antioxidant Activities in Lettuce Seedlings. Horticulturae, 7.10.3390/horticulturae7080238 ↗
56. Effect of Drought Length on the Performance of Cabbage (Brassica oleracea var. capitata) in the Forest-Savannah Transition Zone, Ghana10.1007/s40502-020-00541-5 ↗
57. He, J., Chang, C., Qin, L., and Lai, C.H. (2023). Impacts of Deficit Irrigation on Photosynthetic Performance, Productivity and Nutritional Quality of Aeroponically Grown Tuscan Kale (Brassica oleracea L.) in a Tropical Greenhouse. Int. J. Mol. Sci., 24.10.3390/ijms24032014 ↗
58. Photosynthetic and Growth Responses of Juvenile Chinese Kale (Brassica oleracea var. alboglabra) and Caisin (Brassica rapa subsp. parachinensis) to Waterlogging and Water Deficit10.1016/j.scienta.2006.10.017 ↗
59. Bauer, N., Tkalec, M., Major, N., Talanga Vasari, A., Tokić, M., Vitko, S., Ban, D., Ban, S.G., and Salopek-Sondi, B. (2022). Mechanisms of Kale (Brassica oleracea var. acephala) Tolerance to Individual and Combined Stresses of Drought and Elevated Temperature. Int. J. Mol. Sci., 23.10.3390/ijms231911494 ↗
60. Strasser, R.J., Srivastava, A., and Tsimilli-Michael, M. (2000). Probing Photosynthesis Mechanism, Regulation & Adaptation, CRC Press.
61. Overexpression of γ-Tocopherol Methyl Transferase Gene in Transgenic Brassica juncea Plants Alleviates Abiotic Stress: Physiological and Chlorophyll a Fluorescence Measurements10.1016/j.bbabio.2010.02.002 ↗
62. Dark Chilling Effects on Soybean Genotypes during Vegetative Development: Parallel Studies of CO2 Assimilation, Chlorophyll a Fluorescence Kinetics O-J-I-P and Nitrogen Fixation10.1034/j.1399-3054.2003.00056.x ↗
63. Imaging of Fast Chlorophyll Fluorescence Induction Curve (OJIP) Parameters, Applied in a Screening Study with Wild Barley (Hordeum spontaneum) Genotypes under Heat Stress10.1016/j.jphotobiol.2015.07.020 ↗
64. Revisiting JIP-Test: An Educative Review on Concepts, Assumptions, Approximations, Definitions and Terminology10.32615/ps.2019.150 ↗
65. Dąbrowski, P., Baczewska-Dąbrowska, A.H., Kalaji, H.M., Goltsev, V., Paunov, M., Rapacz, M., Wójcik-Jagła, M., Pawluśkiewicz, B., Bąba, W., and Brestic, M. (2019). Exploration of Chlorophyll a Fluorescence and Plant Gas Exchange Parameters as Indicators of Drought Tolerance in Perennial Ryegrass. Sensors, 19.10.3390/s19122736 ↗
66. Strasser, R.J., Tsimilli-Michael, M., Dangre, D., and Rai, M. (2007). Advanced Techniques in Soil Microbiology, Springer.
67. Inhibition of Photosystem II Activities in Soybean (Glycine max) Genotypes Differing in Chilling Sensitivity10.1016/j.sajb.2014.07.010 ↗
68. Effects of Drought Stress on Chlorophyll a Fluorescence in Two Rubber Tree Clones10.1016/j.scienta.2017.06.019 ↗
69. Variability of the Photosynthetic Machinery Tolerance When Imposed to Rapidly or Slowly Imposed Dehydration in Native Mediterranean Plants10.32615/ps.2022.003 ↗
70. Classification and Characteristics of Heat Tolerance in Ageratina Adenophora Populations Using Fast Chlorophyll a Fluorescence Rise OJIP10.1016/j.envexpbot.2015.09.011 ↗
71. Response of Photosynthesis in Maize to Drought and Re-Watering10.1134/S1021443719030105 ↗
72. Adaptation of Amorpha fruticosa to Different Habitats Is Enabled by Photosynthetic Apparatus Plasticity
73. Drought Tolerance of Passion Fruit Plants Assessed by the OJIP Chlorophyll a Fluorescence Transient10.1016/j.scienta.2012.04.026 ↗
74. Simultaneous in Vivo Recording of Prompt and Delayed Fluorescence and 820 nm Reflection Changes during Drying and after Rehydration of the Resurrection Plant Haberlea rhodopensis10.1016/j.bbabio.2010.03.008 ↗
75. Zagorchev, L., Atanasova, A., Albanova, I., Traianova, A., Mladenov, P., Kouzmanova, M., Goltsev, V., Kalaji, H.M., and Teofanova, D. (2021). Functional Characterization of the Photosynthetic Machinery in Smicronix galls on the Parasitic Plant Cuscuta campestris by JIP-Test. Cells, 10.10.3390/cells10061399 ↗
76. The Polyphasic Chlorophyll a Fluorescence Rise Measured under High Intensity of Exciting Light10.1071/FP05095 ↗
77. Šrajer Gajdošik, M., Vicić, A., Gvozdić, V., Galić, V., Begović, L., and Mlinarić, S. (2022). Effect of Prolonged Photoperiod on Light-Dependent Photosynthetic Reactions in Cannabis. Int. J. Mol. Sci., 23.10.3390/ijms23179702 ↗
78. Botyanszka, L., Zivcak, M., Chovancek, E., Sytar, O., Barek, V., Hauptvogel, P., Halabuk, A., and Brestic, M. (2020). Chlorophyll Fluorescence Kinetics May Be Useful to Identify Early Drought and Irrigation Effects on Photosynthetic Apparatus in Field-Grown Wheat. Agronomy, 10.10.3390/agronomy10091275 ↗
79. Drought Stress Effects on Photosystem I Content and Photosystem II Thermotolerance Analyzed Using Chl a Fluorescence Kinetics in Barley Varieties Differing in Their Drought Tolerance10.1111/j.1399-3054.2009.01273.x ↗
80. Screening of Tomato Landraces for Drought Tolerance Based on Growth and Chlorophyll Fluorescence Analyses10.1007/s13580-020-00328-5 ↗
81. Probing the Photosynthetic Efficiency of Some European and Anatolian Scots Pine Populations under UV-B Radiation Using Polyphasic Chlorophyll a Fluorescence Transient10.32615/ps.2019.151 ↗
82. Preservation of Photosynthetic Electron Transport from Senescence-Induced Inactivation in Primary Leaves after Decapitation and Defoliation of Bean Plants10.1016/j.jplph.2008.05.003 ↗
83. Identification of Nutrient Deficiency in Maize and Tomato Plants by in vivo Chlorophyll a Fluorescence Measurements10.1016/j.plaphy.2014.03.029 ↗
84. The Alternation between PSII and PSI in Ivy (Hedera nepalensis) Demonstrated by in Vivo Chlorophyll a Fluorescence and Modulated 820 nm Reflection10.1016/j.plaphy.2016.08.018 ↗
85. Differential Heat Sensitivity Index in Barley Cultivars (Hordeum vulgare L.) Monitored by Chlorophyll a Fluorescence OKJIP10.1016/j.plaphy.2016.04.015 ↗
86. Performance Index and PSII Connectivity under Drought and Contrasting Light Regimes in the CAM Orchid Phalaenopsis10.3389/fpls.2019.01012 ↗
87. Energetic Flux and Performance Index in Copaiba (Copaifera multijuga Hayne) and Mahogany (Swietenia macrophylla King) Seedlings Grown under Two Irradiance Environments10.1590/S1677-04202007000300001 ↗
88. Selenium Uptake, Dynamic Changes in Selenium Content and Its Influence on Photosynthesis and Chlorophyll Fluorescence in Rice (Oryza sativa L.)10.1016/j.envexpbot.2014.05.005 ↗
89. Close Relationship between the State of the Oxygen Evolving Complex and Rice Cold Stress Tolerance10.1016/j.plantsci.2020.110488 ↗
90. Regulation of Photosystem II Heterogeneity and Photochemistry in Two Cultivars of C4 Crop Sugarcane under Chilling Stress10.3389/fpls.2021.627012 ↗
91. Photosynthetic Proton and Electron Transport in Wheat Leaves under Prolonged Moderate Drought Stress10.1016/j.jphotobiol.2014.01.007 ↗
92. Thermal Phase and Excitonic Connectivity in Fluorescence Induction10.1007/s11120-013-9915-1 ↗
93. Development of Photosystems 2 and 1 during Leaf Growth in Grapevine Seedlings Probed by Chlorophyll a Fluorescence Transient and 820 Nm Transmission in vivo10.1007/s11099-006-0050-5 ↗
94. Phenotyping of Dark and Light Adapted Barley Plants by the Fast Chlorophyll a Fluorescence Rise OJIP10.1016/S0254-6299(15)30246-5 ↗
95. PSII Photochemistry in Vegetative Buds and Needles of Norway Spruce (Picea abies L. Karst.) Probed by OJIP Chlorophyll a Fluorescence Measurement10.1556/ABiol.63.2012.2.5 ↗
96. Exogenously Spermidine Alleviates Damage from Drought Stress in the Photosystem II of Tall Fescue10.17221/236/2021-PSE ↗
97. The Oxygen-Evolving Complex: A Super Catalyst for Life on Earth, in Response to Abiotic Stresses10.1080/15592324.2020.1824721 ↗
98. Photobiological and Lipidic Responses Reveal the Drought Tolerance of Aster tripolium Cultivated under Severe and Moderate Drought: Perspectives for Arid Agriculture in the Mediterranean10.1016/j.plaphy.2020.06.019 ↗
99. Special Issue in Honour of Prof. Reto J. Strasser—Chlorophyll a Fluorescence Parameters as Indicators of a Particular Abiotic Stress in Rice10.32615/ps.2019.147 ↗
100. Song, Y.G., Hwang, J.E., An, J., Kim, P.B., Park, H.B., Park, H.J., Kim, S., Lee, C.W., Lee, B.D., and Kim, N.Y. (2022). The Growth and Physiological Characteristics of the Endangered CAM Plant, Nadopungnan (Sedirea japonica), under Drought and Climate Change Scenarios. Forests, 13.10.3390/f13111823 ↗