Various antioxidant responses to hyperthermia in anatomically different species of the genus Rosa

Keywords: leaf anatomy; drought resistance; superoxide dismutase; peroxidase; pigments.


The heat and drought resistance of plants depend on their anatomical and biochemical features. In the present study, the adaptive features of three species of wild rose (Rosaceae, Rosales) under the short-term impact of high-temperature stress have been characterized. Plants of the species Rosa donetzica Dubovik, R. reversa Waldst. et Kit. and R. spinosissima L. were exposed to a temperature of 40 degrees C for 3 hours, following which peroxidase and superoxide dismutase activity, photosynthetic pigments and flavonoids’ content, and lipid peroxide oxidation level in the leaf were determined. In our investigation, the anatomical structure of leaves and drought resistance of three species of Rosa were studied. Xeromorphic features are the most expressed for R. reversa and R. spinosissima and almost absent for R. donetzica. It has been established that R. spinosissima is photophilous whereas R. donetzica is shade-tolerant. The relatively lower development of epidermic tissue in R. donetzica could probably contribute to more active destruction of the pigment complex under high temperature stress. The obtained data about changes in activity of peroxidase, superoxide dismutase, content of photosynthetic pigments and flavonoids, and level of lipid peroxidation indicate the low heat resistance of R. donetzica in comparison with the other two species. R. reversa, R. spinosissima were more tolerant to short-term hyperthermia. They showed faster antioxidant response, mainly due to the induction of peroxidase activity under stress. The species with the most expressed xerophytic features of anatomical structures have rapid antioxidant response and are more resistant to short-term hyperthermia. The induction of some activity of antioxidant enzymes "in reserve" is a less effective form of adaptation in wild roses. Such activation of enzymes is observed in plants with a more mesophytic structure. Flavonoids and superoxide dismutase were thermolabile to short-term influence of high temperature; therefore they play an insignificant role as antioxidants in the protecton against oxidative stress caused by high temperature stress in wild roses.


Abdel-Salam, E., Alatar, A., & El-Sheikh, M. A. (2018). Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on da­mask rose. Saudi Journal of Biological Sciences, 25(8), 1772–1780.

Ardelean, M., Cachita-Cosma, D., Aurel Ardelean, A., Ladasius, C., & Mihali, V. C. (2014). The effect of heat stress on hyperhydricity and guaiacol peroxidase activity (GPOX) at the foliar lamina of Sedum telephium L. ssp. maximum (L.) Krock. Vitroplantlets. Analele Ştiinţifice ale Universităţii „Al. I. Cuza” Iaşi s. II a. Biologie Vegetală, 60(2), 21–31.

Ashraf, M., & Harris, P. J. C. (2013). Photosynthesis under stressful environments: An overview. Photosynthetica, 51(2), 163–190.

Asrar, A. A., Abdel-Fattah, G. M., & Elhindi, K. M. (2012). Improving growth, flower yield, and water relations of snapdragon (Antirhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica, 50, 305–316.

Babenko, L. M., Kosakivska, I. V., Akimov, Y. A., Klymchuk, D. O., & Skater­nya, T. D. (2014). Effect of temperature stresses on pigment content, lipoxigenase activity and cell ultrastructure of winter wheat seedlings. Genetics and Plant Physiology, 4, 117–125.

Barkasdjieva, N. T., Chrostov, K. N., & Christina, K. N. (2000). Effect of calcium and zinc on the acivity and thermostability of superoxide dismuatse. Biologia Plantarum, 43, 73–78.

Barnabas, B., Jager, K., & Feher, A. (2008). Effect of drought and heat stress on reproductive processes in cereals. Plant Cell and Environment, 31, 11.

Bita, C. E., & Gerats, T. (2013). Plant tolerance to high temperature in a changing environment: Scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science, 4, 273.

Boskabady, M. H., Shafei, M. N., Saberi, Z., & Amini, S. (2011). Pharmacological effects of Rosa damascena. Iran Journal Basic Medical Sciences, 14(4), 295–307.

Cai, X., Starman, T., Niu, G., Hall, C., & Lombardini, L. (2012). Response of selected garden roses to drought stress. Journal American Society for Horticultural Science, 47(8), 1050–1055.

Capellades, M., Fontarnau, R., Carulla, C., & Debergh, P. (1990). Environment influences anatomy of stomata and epidermal cells in tissue-cultured Rosa multiflora. Journal of the American Society for Horticultural Science, 115, 141–145.

Caverzan, A., Casassola, A., & Brammer, S. P. (2016). Antioxidant responses of wheat plants under stress. Genetics and Molecular Biology, 39(1), 1–6.

Chen, W. R., Zheng, J. S., Li, Y. Q., & Guo, W. D. (2012). Effects of high temperature on photosynthesis, chlorophyll fluorescence, chloroplast ultrastructure, and antioxidant activities in fingered citron. Russian Journal of Plant Physiology, 59(6), 732–740.

Cruz, Z., Rodríguez, P., Galindo, A., Torrecillas, E., Ondoño, S., Mellisho, C., & Torrecillas, A. (2012). Leaf mechanisms for drought resistance in Zizyphus jujuba trees. Plant Science, 197, 77–83.

Di Ferdinando, M., Brunetti, C., Fini, A., & Tattini, M. (2011). Flavonoids as anti­oxidants in plants under abiotic stresses. In: Parvaiz Ahmad, M. N. V. P. (Ed.). Abiotic stress responses in plants. Springer. Pp. 159–179.

Essiett, U. A., & Iwok, E. S. (2014). Floral and leaf anatomy of Hibiscus species. American Journal of Medical and Biological Research, 2(5), 101–117.

Ezau, K. (1977). Anatomy of seed plants. 2nd ed., Wiley, New York.

Foyer, C. H., & Harbinson, J. (1994). Oxygen metabolism and the regulation of photosynthetic electron transport. In: Causes of photooxidative stress and amelioration of defense system in plants. CRC Press, Boca Ratón.

Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutase I. Occurrence in higher plants. Plant Physiology, 59(2), 309–314.

Gosavi, G. U., Jadhav, A. S., Kale, A. A., Gadakh, S. R., Pawar, B. D., & Chimote, V. P. (2014). Effect of heat stress on proline, chlorophyll content, heat shock proteins and antioxidant enzyme activity in sorghum (Sorghum bicolor) at seedlings stage. Indian Journal Biotechnol, 13, 356–363.

Grant, J. J. (2000). Role of active oxygen intermediates and cognate redox signa­ling in disease resistance. Plant Physiology, 124, 21–29.

Hansen, J., Ruedy, R., Glascoe, J., & Sato, M. (1999). GISS analysis of surface temperature change. Journal Geophysical Research, 104, 30997–31022.

Harsh, A., Sharma, Y. K., Joshi, U., Rampuria, S., Singh, G., Kumar, S., & Sharm, R. (2016). Effect of short-term heat stress on total sugars, proline and some antioxidant enzymes in moth bean (Vigna aconitifolia). Annals of Agricultural Sciences, 61(1), 57–64.

Hasanuzzaman, M., Fujita, M., Nahar, K., & Biswas, J. K. (2018). Advances in rice research for abiotic stress tolerance. Woodhead Publishing, Unated Kingdom.

Hasanuzzaman, M., Fujita, M., Oku, H., & Islam, M. T. (2019). Plant tolerance to envi­ronmental stress: Role of phytoprotectants, CRC Press, Taylor & Francis Group.

He, Y., & Huang, B. (2010). Differential responses to heat stress in activities and isozymes of four antioxidant enzymes for two cultivars of Kentucky Bluegrass contrasting in heat tolerance. Journal of the American Society for Horticultural Science, 135(2), 116–124.

Hernández, I., Alegre, J., van Bresugem, F., & Munné-Bosch, S. (2009). How relevant are flavonoids as antioxidants in plants. Trends in Plant Science, 14, 125–132.

Hickey, M., & King, C. (2001). Xeromorphic. The Cambridge Illustrated Glossary of Botanical Terms. Cambridge.

Huang, B. (2004). Recent advances in drought and heat stress physiology of turf­grass: A review. Acta Horticulturae, 661, 185–192.

Huseynova, I. M., Aliyeva, D. R., & Aliyev, J. A. (2014). Subcellular localization and responses of superoxide dismutase isoforms in local wheat varieties subject­ted to continuous soil drought. Plant Physiology and Biochemistry, 81, 54–60.

Jones, P. D., & Moberg, A. (2003). Hemispheric and large-scale surface air temperature variations: An extensive revision and an update to 2001. Journal of Climate, 16, 206–223.

Khromykh, N., Lykholat, Y., Shupranova, L., Kabar, A., Didur, O., Lykholat, T., & Kulbachko, Y. (2018). Interspecific differences of antioxidant ability of introduced Chaenomeles species with respect to adaptation to the steppe zone conditions. Biosystems Diversity, 26(2), 132–138.

Kong, L., Wang, F., Si, J., Feng, B., Zhang, B., Li, S., & Wang, Z. (2014). Increa­sing in ROS levels and callose deposition in peduncle vascular bundles of wheat (Triticum aestivum L.) grown under nitrogen deficiency. Journal Plant Interact, 8, 109–116.

Kumar, G. N. M., & Knowles, N. R. (1993). Changes in lipid peroxidation and lipolitic and free radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed-tubers. Plant Physiology, 102, 115–124.

Levitt, J. (1972). Responses of plants to environmental stress. New York.

Lichtenthaller, H. K. (1987). Chlorophylls and carotenoids, pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382.

Mittler, R., Vanderauwera, S., Gollery, M., & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.

Mori, K., Goto-Yamamoto, N., Kitayama, M., & Hashizume, K. (2007). Loss of anthocyanins in red-wine grape under high temperature, Journal of Experimental Botany, 58, 1935–1945.

Niu, G., & Rodriguez, D. (2009). Growth and physiological responses of four rose rootstocks to drought stress. Journal of the American Society for Horticultural Science, 134(2), 202–209.

Nuzhyna, N., Baglay, K., Golubenko, A., & Lushchak, O. (2018). Anatomically distinct representatives of Cactaceae Juss. family have different response to acute heat shock stress. Flora, 242, 137–145.

Olmos, E., Sánchez-Blanco, M. J., Ferrández, T., & Alarcón, J. J. (2007). Subcellular effects of dought stress in Rosmarinus officinalis. Plant Biology, 9, 77–84.

Pshibytko, N. L., Zhavoronkova, N. B., & Kabashnikova, L. F. (2005). Vliyanie gipertermii na strukturno-funkcional'noe sostoyanie fotosinteticheskih membran yachmenya s modificirovannym pigmentnym aparatom [The effect of hyperthermia on the structural and functional state of the photosynthetic membranes of barley with a modified nutritional apparatus]. Biologicheskie Membrany, 22(6), 444–449 (in Russian).

Raghuwanshi, A., Dudeja, S., & Khurana, A. (1994). Effect of temperature on fla­vonoid production in pigeonpea (Cajanus cajan (L) Millsp.) in relation to nodulation. Biology and Fertility of Soils, 17(4), 314–316.

Rai, N., Rai, K. K., Tiwari, G., & Singh, P. K. (2015). Changes in free radical generation, metabolites and antioxidant defense machinery in hyacinth bean (Lablab purpureus L.) in response to high temperature stress. Acta Physiologiae Plantarum, 37, 46–57.

Rizhsky, L., Hongjian, L., & Mittler, R. (2002). The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology, 130, 1143–1151.

Rodríguez, V. M., Soengas, P., Alonso-Villaverde, V., Sotelo, T., Cartea, M. E., & Velasco, P. (2015). Effect of temperature stress on the early vegetative deve­lopment of Brassica oleracea L. BMC Plant Biology, 15, 145.

Romeis, B. (1948). Mikroskopische Technik [Microscopic technique]. München, R. Oldenbourg (in German).

Savicka, M., & Škute, N. (2010). Effects of high temperature on malondialdehyde content, superoxide production and growth changes in wheat seedlings (Triticum aestivum L.). Ekologija, 56(1–2), 26–33.

Scandalios, J. G. (2005). Oxidative stress: Molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research, 38, 995–1014.

Sharifi, G., & Ebrahimzadeh, H. (2010). Changes of antioxidant enzyme activities and isoenzyme profiles during in vitro shoot formation in saffron (Crocus sativus L.). Acta Biologica Hungarica, 61(1), 73–89.

Sunkar, R. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell, 18(6), 2051–2065.

Tabuchi, T., Hiramatsu, N., & Hida, Y. (2010). Anatomical characteristics of leaf mesophyll on Rosa rugosa and their hybrid plant. Acta Horticulturae, 870, 137–142.

Talaat, N. B., & Shawky, B. T. (2014). Modulation of the ROSscavenging system in salt-stressed wheat plants inoculated with arbuscular mycorrhizal fungi. Journal Plant Nutrition Soil Science, 177, 199–207.

Torre, S., Fjeld, T., Gislerod, H. R., & Moe, R. (2003). Leaf anatomy and stomatal morphology of greenhouse rose grown at moderate or high air humidity. Journal of the American Society for Horticultural Science, 128(4), 598–602.

Trineeva, O. V., Slivkin, A. I., & Voropaeva, S. S. (2014). Razrabotka i validaciya metodiki kolichestvennogo opredeleniya flavonoidov v list'yah krapivy dvudomnoj [Development and validation of a technique of quantitative definition flavonoids in nettle leaves a two-blast furnace]. Vestnik VGU, Himiya, Biologiya, Farmaciya, 1, 138–144 (in Russian).

Tuteja, N., Gill, S. S., & Tuteja, R. (2013). Improving crop productivity in sustainable agriculture. Wiley VCH, Weinheim.

Wang, G., Cao, F., Wang, G., & El-Kassaby, Y. A. (2015). Role of temperature and soil moisture conditions on flavonoid production and biosynthesis-rela­ted genes in ginkgo (Ginkgo biloba L.) leaves. Open Natural Products Chemistry and Research, 3(1), 1000162.

Warburg, O., & Christian, W. (1941). Isolierung und kristallisation des garungsferments enolase [Isolation and crystallization of the fermentation enzyme enolase]. Biochemistry, 310, 384–421 (in German).

Zandalinas, S. I., Rivero, R. M., Martínez, V., Gómez-Cadenas, A., & Arbona, V. (2016). Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biology, 16, 105.

Zhang, D. H., & Tohtar, V. K. (2011). Issledovanie zasuhoustojchivosti perspektivnyh vidov Momordica charantia L. i M. balsamina L. (Cucurbitaceae) [Drought resistence study of respective for introduction of Momordica charantia L. and M. balsamina L. species (Cucurbitaceae)]. Nauchnye Vedomosti, Seriya Estestvennye Nauki, 104(15), 43–47 (in Russian).

Zhang, J., & Kirkham, M. (1994). Drought-stress induced changes in activities of superoxide dismutase, catalase and peroxidases in wheat leaves. Plant Cell Physiology, 35, 785–791.

Zhang, X., Wang, K., & Ervin, E. H. (2010). Optimizing dosages of seaweed extract-based cytokinins and zeatin riboside for improving creeping bentgrass heat tolerance. Crop Science, 50, 316–320.