Assessment of the functioning of the photosynthetic apparatus of Olea europaea L. under freezing temperatures

Sergei Yu. Tsiupka; Valentina A. Tsiupka; Ilya V. Bulavin

doi:10.12731/2658-6649-2025-17-1-1058

Sergei Yu. Tsiupka Nikitsky Botanical Garden-National Scientific Center
Valentina A. Tsiupka Nikitsky Botanical Garden-National Scientific Center
Ilya V. Bulavin Nikitsky Botanical Garden-National Scientific Center

DOI: https://doi.org/10.12731/2658-6649-2025-17-1-1058

Keywords: olive, cultivar, frost resistance, photosynthetic activity

Abstract

Background. Olive (O. europaea) is a popular fruit crop, and is the second in the world by area after coffee. The main limiting factor for olive cultivation in regions located on the northern border of the subtropical zone, as well as in temperate climates, is their low frost resistance. So, the aim of the present study was to evaluate the degree of influence of low negative temperatures on the functional state of leaves of different O. europaea genotypes.

Materials and methods. The functioning of pigment apparatus, stability of chlorophyll-protein complex and membrane damage under freezing temperatures were evaluated on leaves of the following cultivars of olive: ‘Aglandau’, ‘Coreggiolo’, ‘Obilnaya’, ‘Tiflis’, ‘Dalmatica’, ‘Nikitskaya 2’, ‘Ascolano’, ‘Tossijskaya’, ‘Leccino’, ‘Razzo’. The studies were carried out under native conditions (control) and after exposure to low temperatures (immediately and after 24 hours of the stress factor influence). Four temperature effects were analyzed: -7°C, -10°C, -12°C and -14°C.

Results and conclusion. Exposure to sub-zero temperatures induced a different response both in the manifestation of visual lesions on leaves and in changes in their physiological parameters. At a low gradient of temperature exposure (-7... - 10°C), leaf tissues of the European selection varieties ‘Coreggiolo’, ‘Ascolano’, ‘Leccino’ and ‘Razzo’ were damaged: electrical conductivity reached 15%, chlorophyll stability index decreased, variable fluorescence and photosynthetic activity coefficients decreased, uncontrolled photon quenching was significantly higher than the effective photochemical quantum yield and non-photochemical quenching. Cultivars of crimean and caucasian breeding are characterised by increased frost resistance. Cultivars ‘Nikitskaya 2’, ‘Tossijskaya’ and ‘Tiflis’ demonstrate integrity of leaf cell membranes, preservation of stability of photosynthetic pigments content and work of photosystems at different levels of their organization at –14°C.

EDN: WTGVZM

Downloads

Download data is not yet available.

Author Biographies

Sergei Yu. Tsiupka, Nikitsky Botanical Garden-National Scientific Center

PhD, Senior Researcher

Valentina A. Tsiupka, Nikitsky Botanical Garden-National Scientific Center

PhD, Head of the Laboratory of Plant Genomics and Bioinformatics, Senior Researcher

Ilya V. Bulavin, Nikitsky Botanical Garden-National Scientific Center

PhD, Head of the Laboratory of Plant Cell Biology and Anatomy, Senior Researcher

References

Список литературы

Гольцев, В. Н., Каладжи, Х. М., Паунов, М., Баба, В., Хорачек, Т., Мойски, Я., Коцел, Х., & Аллахвердиев, С. И. (2016). Использование переменной флуоресценции хлорофилла для оценки физиологического состояния фотосинтетического аппарата растений. Физиология растений, 63(6), 881–907. https://doi.org/10.7868/S0015330316050055

Доманская, Э. Н. (1964). Изучение физиолого-биохимических показателей сравнительной морозостойкости сортов маслины. (кандидатская диссертация). Ялта.

Иванова, М. И., Бухаров, А. Ф., & Кашлева, А. И. (2022). Корреляционный анализ признаков, характеризующих урожайность и качество продукции представителей рода Allium (подрод Сера). Известия Саратовского университета. Новая серия. Серия: Химия. Биология. Экология, 22(1), 64–73. https://doi.org/10.18500/1816-9775-2022-22-1-64-73

Нестеренко, Т. В., Тихомиров, А. А., & Шихов, В. Н. (2007). Индукция флуоресценции хлорофилла и оценка устойчивости растений к неблагоприятным воздействиям. Журнал общей биологии, 68(6), 444–458.

Нестеров, Я. С. (1972). Методика определения зимостойкости и морозостойкости плодовых и ягодных культур. Мичуринск.

Рубин, А. Б. (2000). Биофизические методы в экологическом мониторинге. Соросовский образовательный журнал, (4), 7–13.

Щенникова, И. Н., Лисицын, Е. М., & Кокина, Л. П. (2010). Изменение пигментного комплекса флаговых листьев ячменя под действием эдафического стресса. Аграрная наука Евро-Северо-Востока, (1), 24–28.

Юшков, А. Н. (2017). Адаптивный потенциал и селекция плодовых растений на устойчивость к абиотическим стрессорам. (докторская диссертация). Мичуринск: Мичуринский государственный аграрный университет.

Alekseev, A. A., Osipov, V. A., & Matorin, D. N. (2006). Method for determining the functional state of plants by chlorophyll fluorescence. Yakut State University, Yakutsk, 65 p.

Antognozzi, E., Pilli, M., Proietti, P., & Romani, F. (1990). Analysis of some factors affecting frost resistance in olive trees. Paper presented at XXIII Int. Horticultural Congress, Firenze, Italy, 4280 p.

Arias, N. S., Scholz, F. G., Goldstein, G., & Bucci, S. J. (2021). Low-temperature acclimation and legacy effects of summer water deficits in olive freezing resistance. Tree Physiology, 41(10), 1836–1847. https://doi.org/10.1093/treephys/tpab040

Baker, N. R., & Oxborough, K. (2004). Chlorophyll fluorescence as a probe of photosynthetic productivity. In Chlorophyll a Fluorescence: A Signature of Photosynthesis (pp. 65–82). Dordrecht: Springer Netherlands. https://doi.org/10.1007/978-1-4020-3218-9_3

Bartolozzi, F., & Fontanazza, G. (1999). Assessment of frost tolerance in olive (Olea europaea L.). Scientia Horticulturae, 81, 309–319. https://doi.org/10.1016/S0304-4238(99)00019-9

Bartolozzi, F., Rocchi, P., Camerini, F., & Fontanazza, G. (1999). Changes of biochemical parameters in olive (Olea europaea L.) leaves during an entire vegetative season, and their correlation with frost resistance. Acta Horticulturae, 474, 435–440. https://doi.org/10.17660/ActaHortic.1999.474.89

Brajon, O. V., Korneev, D. Yu., Snegur, O. O., & Kitaev, O. I. (2000). Instrumental studies of the photosynthetic apparatus using the induction of chlorophyll fluorescence. Methodical instructions. Kyiv, Ukraine, 11 p.

D'Angeli, S., & Altamura, M. M. (2007). Osmotin induces cold protection in olive trees by affecting programmed cell death and cytoskeleton organization. Planta, 225, 1147–1163. https://doi.org/10.1007/s00425-006-0426-6

Deslauriers, A., Caron, L., & Rossi, S. (2015). Carbon allocation during defoliation: Testing a defense-growth trade-off in balsam fir. Frontiers in Plant Science, 6, 338. https://doi.org/10.3389/fpls.2015.00338

Fontanazza, G. (1986). Renovation of olive groves damaged by frost: technical guidelines. Giornale di Agricolture, 42, 45–47.

Food and Agriculture Organization (FAO) and Codex Alimentarius Commission. Available online: http://www.fao.org/. Accessed date: November 2023. https://doi.org/10.4337/9781786438935.00011

García-Mozo, H., Pérez-Badía, R., & Galán, C. (2008). Aerobiological and meteorological factors’ influence on olive (Olea europaea L.) crop yield in Castilla-La Mancha (central Spain). Aerobiologia, 24, 13–18. https://doi.org/10.1007/s10453-007-9075-x

Ghamary, B., Rajabipour, A., Borghei, A. M., & Sadeghi, H. (2010). Some physical properties of olive. Agricultural Engineering International, 12, 104–110. https://cigrjournal.org/index.php/Ejounral/article/view/1381

Gómez-del Campo, M., & Barranco, D. (2005). Field evaluation of frost tolerance in ten olive cultivars. Plant Genetic Resources, 3(3), 385–390. https://doi.org/10.1079/PGR200592

Gordeev, R. V., Pyzhev, A. I., & Zander, E. V. (2022). Does climate change influence Russian agriculture? Evidence from panel data analysis. Sustainability, 14, 718. https://doi.org/10.3390/su14020718

Gubanova, T. B. (2019a). Resistance of Olea europaea L. varieties and forms to unfavorable winter conditions on the southern coast of Crimea. Pomiculture and Small Fruit Culture in Russia, 57, 32–41. https://doi.org/10.31676/2073-4948-2019-57-32-41

Gubanova, T. B. (2019b). The influence of negative temperatures on photosynthetic activity in some evergreen species of Oleaceae family. Subtropical and Decorative Gardening, 70, 158–167. https://doi.org/10.31360/2225-3068-2019-70-158-167

Gubanova, T. B., & Paliy, A. E. (2020). Physiological and biochemical aspects of frost resistance in Olea europaea L. Russian Journal of Plant Physiology, 67, 671–679. https://doi.org/10.1134/S1021443720030103

Ivashchenko, Y., Ivashchenko, I., & Tsiupka, S. (2021). Evaluation of olive cultivars with different photosynthetic activity of leaves. Acta Horticulturae, 1308, 99–104. https://doi.org/10.17660/ActaHortic.2021.1308.16

Kramer, D. M., Johnson, G., Kirats, O., & Edwards, G. E. (2004). New flux parameters for the determination of Qa redox state and excitation flux. Photosynthesis Research, 79, 209–218. https://doi.org/10.1023/B:PRES.0000015391.99477.0d

La Porta, N., Zacchini, M., Bartolini, S., Viti, R., & Roselli, G. (1994). The frost hardiness of some clones of olive cv. Leccino. Journal of Horticultural Science, 69(3), 433–435. https://doi.org/10.1080/14620316.1994.11516472

Lichtenthaler, H. K. (2004). Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In H. K. Lichtenthaler & F. Babani (Eds.), Chlorophyll a Fluorescence: A Signature of Photosynthesis (pp. 713–736). Dordrecht: Springer Netherlands.

Lichtenthaler, H. K., & Rinderle, U. (1988). The role of chlorophyll fluorescence in the detection of stress conditions in plants. CRC Critical Reviews in Analytical Chemistry, 19(1), 29–85. https://doi.org/10.1080/15476510.1988.10401466

Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591–592. https://doi.org/10.1042/bst0110591

Martin, G. C., Denney, J. O., Ketchie, D. O., Osgood, J. W., Connel, J. H., Sibbett, G. S., Kammereck, R., Krueger, W. H., & Nour, G. A. (1993). Freeze damage and cold hardiness in olive: Findings from the 1990 freeze. California Agriculture, 47(1), 1–12. https://www.cabidigitallibrary.org/doi/full/10.5555/19930325238

Maxwell, K., & Johnson, G. N. (2000). Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany, 51(345), 659–668. https://doi.org/10.1093/jexbot/51.345.659

Moreno-Alias, I., Leon, L., de la Rosa, R., & Rapoport, H. F. (2009). Morphological and anatomical evaluation of adult and juvenile leaves of olive plants. Trees, 23, 181–187. https://doi.org/10.3390/agriculture13061137

Rezaei, M., & Rohani, A. (2023). Estimating freezing injury on olive trees: A comparative study of computing models based on electrolyte leakage and tetrazolium tests. Agriculture, 13, 1137. https://doi.org/10.3390/agriculture13061137

Rinderle, U., & Lichtenthaler, H. K. (1988). The chlorophyll fluorescence ratio F690/F735 as a possible stress indicator. In H. K. Lichtenthaler (Ed.), Applications of Chlorophyll Fluorescence (pp. 189–196). Dordrecht: Kluwer Academic Publishers. https://doi.org/10.1007/978-94-009-2823-7_23

Rodrigo-Comino, J., Salvia, R., Quaranta, G., Cudlin, P., Salvati, L., & Gimenez-Morera, A. (2021). Climate aridity and the geographical shift of olive trees in a Mediterranean northern region. Climate, 9, 64. https://doi.org/10.3390/cli9040064

Roselli, G., La Porta, N., & Morelli, D. (1992). Evaluations of olive germplasm for cold-stress tolerance. Atti Convegno Germoplasma Frutticolo: Alghero, Settembre, pp. 107–112.

Roselli, G., & Venora, G. (1989). Relationship between stomatal size and winter hardiness in the olive. International Symposium on Olive Growing, 286, 89–92. https://doi.org/10.17660/ActaHortic.1990.286.15

Roselli, G., & Venora, G. (1990). Relationship between stomatal size and winter hardiness in the olive. Acta Horticulturae, 286, 89–92. https://doi.org/10.17660/ActaHortic.1990.286.15

Schreiber, U., Schliwa, U., & Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research, 10, 51–62. https://doi.org/10.1007/BF00024185

Stirbet, A., & Govindjee, G. (2011). On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology, 104(1–2), 236–257. https://doi.org/10.1016/j.jphotobiol.2010.12.010

Tanentzap, F. M., Stempel, A., & Ryser, P. (2015). Reliability of leaf relative water content (RWC) measurements after storage: consequences for in situ measurements. Botany, 93, 535–541. https://doi.org/10.1139/cjb-2015-0065

Tsiupka, S. (2018). Historical review of olive germplasm evaluation and cultivar development in Crimea. Acta Horticulturae, 1208, 97–104. https://doi.org/10.17660/ActaHortic.2018.1208.13

van Kooten, O., & Snel, J. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25, 147–150. https://doi.org/10.1007/BF00033156

Xu, Z., Zhou, G., & Li, H. (2004). Responses of chlorophyll fluorescence and nitrogen level of Leymus chinensis seedling to changes of soil moisture and temperature. Journal of Environmental Sciences, 16(4), 666–669.

Yoshida, S., & Uemura, M. (1990). Responses of the plasma membrane to cold acclimation and freezing stress. In The Plant Plasma Membrane (pp. 293–320). Berlin: Springer. https://doi.org/10.1007/978-3-642-74522-5_13

Zhang, B. B., Xu, J. L., Zhou, M., Yan, D. H., & Ma, R. J. (2018). Effect of light quality on leaf photosynthetic characteristics and fruit quality of peach (Prunus persica L. Batch). Photosynthetica, 56, 1113–1122. https://doi.org/10.1007/s11099-018-0820-x

References

Gol'tsev, V. N., Kaladzhi, Kh. M., Paunov, M., Baba, V., Khorachek, T., Moyski, Ya., Kotsel, Kh., & Allahverdiev, S. I. (2016). Using variable chlorophyll fluorescence to evaluate the physiological state of the photosynthetic apparatus of plants. Fiziologiya rasteniy, 63(6), 881–907. https://doi.org/10.7868/S0015330316050055

Domanskaya, E. N. (1964). Study of physiological and biochemical indicators of comparative frost resistance of olive varieties. Unpublished doctoral dissertation, Yalta.

Ivanova, M. I., Bukharov, A. F., & Kashleva, A. I. (2022). Correlation analysis of traits characterizing yield and product quality of Allium (subgenus Sera) representatives. Izvestiya Saratovskogo universiteta. Novaya seriya. Seriya: Khimiya. Biologiya. Ekologiya, 22(1), 64–73. https://doi.org/10.18500/1816-9775-2022-22-1-64-73

Nesterenko, T. V., Tikhomirov, A. A., & Shikhov, V. N. (2007). Induction of chlorophyll fluorescence and assessment of plant resistance to adverse influences. Zhurnal obshchey biologii, 68(6), 444–458.

Nesterov, Ya. S. (1972). Methodology for assessing winter hardiness and frost resistance of fruit and berry crops. Michurinsk.

Rubin, A. B. (2000). Biophysical methods in ecological monitoring. Sorosovskiy Obrazovatel'nyy Zhurnal, (4), 7–13.

Shchennikova, I. N., Lisitsyn, E. M., & Kokina, L. P. (2010). Changes in the pigment complex of barley flag leaves under the influence of edaphic stress. Agrarnaya nauka Euro-Severo-Vostoka, (1), 24–28.

Yushkov, A. N. (2017). Adaptive potential and breeding of fruit plants resistant to abiotic stresses. Unpublished doctoral dissertation, Michurinsk: Michurinsky State Agrarian University.