Species-specific response to acute hyperthermal stress of Haworthia (Asphodelaceae) plants
AbstractAn increase in environmental temperature is one of the most common stress factors for plant organisms. The study of the plants’ adaptation to stress factors remains extremely important and relevant. This article presents the results of a acute short-term influence of hyperthermia on species of two subgenera of the genus Haworthia Duval. We investigated the different levels of antioxidant protection and damage degree of the members of two subgenera of the genus Haworthia at the biochemical level, measuring the lipid peroxidation, superoxide dismutase and peroxidase activities, total flavonoid content and content of photosynthetic pigments with a spectrophotometer. To determine the drought tolerance of plants, the water supply of tissues, water shortage and loss of water after an hour of wilting were measured. The values for different groups were compared by ANOVA followed by the Tukey multiple comparison test. The studied plants were warmed in a thermostat at temperatures of 40 °C and 50 °C for three hours under the conditions of natural light. The control group of plants was kept at 25 °C. The research has shown that H. attenuata, H. limifolia and H. cymbiformis are characterized with the increase of concentration of malonic dialdehyde at 40 °C and 50 °C, but a significant difference of values wasn’t received,which indicates the relative resistance of these plants to the influence of high temperatures. The sharp increase of temperature causes the highest level of lipid peroxidation in H. parksiana plants, along with which, warming to 50 °C launches a mechanism of activation and synthesis of superoxide dismutase and flavonoids for the plants. The studied species of the subgenus Haworthia have a photosynthetic system relatively resistant to thermal stress in comparison to the subgenus Hexangulares. H. limifolia plants have a slight inhibition of photosynthesis. The adaptation of H. cymbiformis to thermal stress is due to the strategy of accumulation of a pool of active enzymes, superoxide dismutase, peroxidase, flavonoids under normal conditions and the activation of new peroxidase enzymes as a result of stress. H. attenuata is characterized by activation of new enzymes of superoxide dismutase and peroxidase under stress. It was found that H. cymbiformis and H. attenuata are more heat resistant in comparison with the other two species. Acute short-term hyperthermia has a different influence on the antioxidant system of different species of Haworthia. H. limifolia has the highest drought tolerance, H. cymbiformis has the lowest, the other two species from different subgenera have similar drought tolerance indicators. We did not find any dependence of the mechanisms of action of the antioxidant system under hyperthermia on the type of adaptation to arid conditions at the anatomical level in plants of different subgenera of the genus Haworthia.
Ardelean, M., Cachita-Cosma, D., 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, Scientific Annals of „Alexandru Ioan Cuza” University of Iasi, Biology Series. 60(2), 21–31.
Ashraf, M., & Harris, P. J. C. (2013). Photosynthesis under stressful environments: An overview. Photosynthetica, 51(2), 163–190.
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.
Bayer, B. (1999). Haworthia revisied. A revision of genus. Umdaus Press, Pretoria.
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, 273–285.
Caverzan, G. Passaia, S., Rosa, S. B., Barcellos, R., Ribeiro, W. C., Lazzarotto, F., & Margis-Pinheiro, M. (2012) Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genetics and Molecular Biology, 35(4), 1011–1019.
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.
Chetti, M. B., & Nobel, P. S. (1988). Recovery of photosynthetic reactions after high-temperature treatments of a heat-tolerant cactus. Photosynthesis Research, 18(3), 277–286.
Didden-Zopfy, B., & Nobel, P. S. (1982). High temperature tolerance and heat acclimation of Opuntia bigelovii. Oecologia, 52(2), 176–180.
Eggli, U. (2001). Illustrated Handbook of succulent plants. Monocotyledones. Press: Springler-Verlag. Berlin, Heidelberg, 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, 1–42.
Giang, D., & Tokhtar’, V. K. (2011). Issledovanie zasuhoustoychivosti perspektivnyih vidov Momordica charantia L. i M. balsamina L. (Cucurbitaceae) [Drought resistance study of respective for introduction of Momordica charantia L. and M. balsamina L. Species (Cucurbitaceae)]. Nauchnyie Vedomosti. Seriya Estestvennyie Nauki, 9, 43–47 (in Russian).
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutase I. Occurrence in higher plants. Plant Physiology, 2, 309–314.
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 of Geophysical Research, 104, 30997–31022.
Harsh, A., Sharma, Y. K., Joshi, U., Rampuria, S., Singh, G., Kumarb, S., & Sharma, 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.
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 Horticular Science. 135(2), 116–124.
Hernandez, J. A., Jiménez, A., Mullineaux, P., & Sevilia, F. (2000). Tolerance of pea (Pisum sativum L.) to long term stress is associated with induction of antioxidant defences. Plant Cell and Environment, 23, 583–862.
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.
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.
Lichtenthaller, H. K. (1987). Chlorophylls and carotenoids, pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382.
Mansoor, S., & Naqvi, F. N. (2013). Effect of heat stress on lipid peroxidation and antioxidant enzymes in mung bean (Vigna radiata L.) seedlings. African Journal of Biotechnology, 12(21), 3196–3203.
Martinazzo, E. G., Ramm, A., & Bacarin, M. A. (2013). The chlorophyll a fluorescence as an indicator of the temperature stress in the leaves of Prunus persica. Brazilian Journal of Plant Physiology, 24(4).
Mittler, R., Vanderauwera, S., Gollery, M., & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in Plant Science, 9, 490–498.
Nepliy, L., Babayants, O., Molodchenkova, O., & Lyashuk, N. L. (2013). Vplyv VZhKYa na kil’kisnyy vmist khlorofiliv, karotynoyidiv ta zahal’nykh tsukri u lystkakh ozymoyi pshenytsi v pivdennomu stepu Ukrayiny [Influence of HPLC on the quantitative content of chlorophylls, carotenoids and common sugars in leaves of winter wheat in the Southern Steppe of Ukraine]. Visnyk Kyyivs’koho Natsional’noho Universytetu Ukrayiny. Seriya Biolohiya], 63, 29–33. (in Ukrainian).
Nuzhyna, N. V., & Gaydarzhy, M. N. (2015). Comparative characteristics of anatomical and morphological adaptations of plants of two subgenera Haworthia Duval (Asphodelaceae) to arid environmental conditions. Acta Agrobotanika, 68(1), 23–31.
Nuzhyna, N., Bahlay, K., & Avyekin, Y. (2016). Dynamika pihmentnoho kompleksu Echinocactus grusonii Hildm., Mammillaria bocasana Pos., Aylostera flavistyla Ritt. za umov hipertermiyi [Dynamics of the pigment complex Echinocactus grusonii Hildm., Mammillaria bocasana Pos., Aylostera flavistyla Ritt. under hyperthermia]. Visnyk Kyyivskogo Universytetu imeni Tarasa Shevchenka. Introduktsiya ta Zberezhennya Roslynnoho Riznomanittya, 34, 66–68 (in Ukrainian).
Panda, S. K., & Khan, M. H. (2004). Changes in growth and superoxide dismutase activity in Hydrilla verticillata L. under abiotic stress. Brazilian Journal of Plant Physiology, 2, 115–118.
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(3), 46–57.
Red List of South Africa Plants. Pretoria, (2009).
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.
Rosas, U., Zhou, R. W., Castillo, G., & Collazo-Ortega, M. (2012). Developmental reaction norms for water stressed seedlings of succulent cacti. PLoS ONE, 7(3).
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.
Sibgatullina, G. V., Haertdinova, L. R., Gumerova, E. A., Akulov, A. N., Kostyukova, Y. A., Nikonorova, N. A., & Rumyantsev, N. I. (2011). [Metody opredelenia redox-statusa kul’tiviruemyh kletok rasteniy] Methods for determining the redox status of cultured plant cells. Kazan Federal University, Kazan (in Russian).
Smirnoff, N. (1993) The role of active oxygen in response to water deficit and dessication. New Phytology, 125, 27–58.
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, 2051–2065.
Trineeva, O. V., Slivkin, A. I., & Voropayeva, S. (2014). Razrabotka i validatsiya metodiki kolichestvennogo opredeleniya flavonoidov v listyah krapivyi dvudomnoy. [Development and validation of a technique of quantitative definition flavonoids in nettle leaves a two-blast furnace]. Vestnik VGU, Himiya, Biologiya, Farmatsiya, 1, 138–144 (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.
Zutta, B. R., Nobel, P. S., Aramians, A. M., & Sahaghian, A. (2011). Low-and high-temperature tolerance and acclimation for chlorenchyma versus meristem of the cultivated cacti Nopalea cochenillifera, Opuntia robusta, and Selenicereus megalanthus. Journal of Botany, Article ID 347168.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.