Acclimation of the Resurrection Plant Haberlea rhodopensis to Changing Light Conditions
Abstract
:1. Introduction
2. Results
2.1. Changes in Electrolyte Leakage and Malondialdehyde and Proline Content as Stress Markers
2.2. Photochemical Activity of PSII and Pigment Content
2.3. Effect of Light on the Activity of Antioxidant Enzymes During Desiccation
3. Discussion
3.1. Response of Sun and Shade Plants to Desiccation
3.2. Shade and Sun H. rhodopensis Plants Showed High Acclimation Capacity When Desiccated at Opposite Light Intensities
4. Materials and Methods
4.1. Desiccation and Rehydration of Plants
4.2. Determination of RWC
4.3. Pigment Content Determination
4.4. Electrolyte Leakage
4.5. Malondialdehyde Content (MDA)
4.6. Determination of Proline Content
4.7. Chlorophyll a Fluorescence Induction
4.8. Enzyme Activities
4.9. Statistics
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Daskalova, E.; Dontcheva, S.; Yahubyan, G.; Minkov, I.; Toneva, V. Ecological characteristics and conservation of the protected resurrection species Haberlea rhodopensis Friv. as in vitro plants through a modified micropropagation system. Biotechnol. Biotechnol. Equip. 2010, 24, 213–217. [Google Scholar] [CrossRef]
- Zia, A.; Walker, B.J.; Oung, H.M.O.; Charuvi, D.; Jahns, P.; Cousins, A.B.; Farrant, J.M.; Reich, Z.; Kirchhoff, H. Protection of the photosynthetic apparatus against dehydration stress in the resurrection plant Craterostigma pumilum. Plant J. 2016, 87, 664–680. [Google Scholar] [CrossRef] [PubMed]
- Sherwin, H.W.; Pammenter, N.W.; February, E.D.; Vander Willigen, C.; Farrant, J.M. Xylem hydraulic characteristics, water relations and wood anatomy of the resurrection plant Myrothamnus flabellifolius Welw. Ann. Bot. 1998, 81, 567–575. [Google Scholar] [CrossRef]
- Muslin, L.E.H.; Homann, P.H. Light as a hazard for the desiccationresistant ‘resurrection’ fern Polypodium polypodioides. Plant Cell Environ. 1992, 15, 81–89. [Google Scholar] [CrossRef]
- Seel, W.; Baker, N.R.; Lee, J.A. Analysis of the decrease in photosynthesis on desiccation of mosses from xeric and hydric environments. Physiol. Plant. 1992, 86, 451–458. [Google Scholar] [CrossRef]
- Georgieva, K.; Maslenkova, L. Thermostability and photostability of PSII in leaves of resurrection plant Haberlea rhodopensis studied by means of chlorophyll fluorescence. Z. Naturfor. C 2006, 61, 234–240. [Google Scholar] [CrossRef]
- Georgieva, K.; Lenk, S.; Buschmann, C. Responses of the resurrection plant Haberlea rhodopensis to high irradiance. Photosynthetica 2008, 46, 208–215. [Google Scholar] [CrossRef]
- Sárvári, É.; Mihailova, G.; Solti, Á.; Keresztes, Á.; Velitchkova, M.; Georgieva, K. Comparison of thylakoid structure and organization in sun and shade Haberlea rhodopensis populations under desiccation and rehydration. J. Plant Physiol. 2014, 171, 1591–1600. [Google Scholar] [CrossRef] [PubMed]
- Sherwin, H.W.; Farrant, J.M. Protection mechanism against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul. 1998, 24, 203–210. [Google Scholar] [CrossRef]
- Farrant, J.M. A comparison of mechanisms of desiccation-tolerance among three angiosperm resurrection plant species. Plant Ecol. 2000, 151, 29–39. [Google Scholar] [CrossRef]
- Smirnoff, N. Role of active oxygen in the response of plants to water deficits and desiccation. New Phytol. 1993, 125, 27–58. [Google Scholar] [CrossRef] [PubMed]
- Farrant, J.M.; Bartsch, S.; Loffell, D.; van der Willigen, C.; Whittaker, A. An investigation into the effects of light on the desiccation of three resurrection plants species. Plant Cell Environ. 2003, 26, 1275–1286. [Google Scholar] [CrossRef]
- Morse, M.; Rafudeen, M.S.; Farrant, J.M. An overview of the current understanding of desiccation tolerance in the vegetative tissues of higher plants. Adv. Bot. Res. 2011, 57, 319–347. [Google Scholar] [CrossRef]
- Georgieva, K.; Dagnon, S.; Gesheva, E.; Bojilov, D.; Mihailova, G.; Doncheva, S. Antioxidant defense during desiccation of the resurrection plant Haberlea rhodopensis. Plant Physiol. Biochem. 2017, 114, 51–59. [Google Scholar] [CrossRef]
- Georgieva, K.; Rapparini, F.; Bertazza, G.; Mihailova, G.; Sárvári, É.; Solti, Á.; Keresztes, Á. Alterations in the sugar metabolism and in the vacuolar system of mesophyll cells contribute to the desiccation tolerance of Haberlea rhodopensis ecotypes. Protoplasma 2017, 254, 193–201. [Google Scholar] [CrossRef]
- Moore, J.; Westall, K.; Ravenscroft, N.; Farrant, J.M.; Lindsey, G.; Brandt, W. The predominant polyphenol in the leaves of the resurrection plant Myrothamnus flabellifolius, 3,4,5 tri-O-galloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochem. J. 2005, 385, 301–308. [Google Scholar] [CrossRef]
- Pacifico, S.; D’Abrosca, B.; Pascarella, M.T.; Letizia, M.; Uzzo, P.; Piscopo, V.; Fiorentino, A. Antioxidant efficacy of iridoid and phenylethanoid glycosides from the medicinal plant Teucrium chamaedris in cell-free systems. Bioorg. Med. Chem. 2009, 17, 6173–6179. [Google Scholar] [CrossRef]
- Hoekstra, F.A.; Golovina, E.A.; Buitink, J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 2001, 6, 431–438. [Google Scholar] [CrossRef]
- Ghasempour, H.R.; Gaff, D.F.; Williams, R.D.; Gianello, R.D. Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul. 1998, 24, 185–191. [Google Scholar] [CrossRef]
- Nishizawa, A.; Yabuta, Y.; Shigeoka, S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008, 147, 1251–1263. [Google Scholar] [CrossRef]
- Rapparini, F.; Neri, L.; Mihailova, G.; Petkova, S.; Georgieva, K. Growth irradiance affects the photoprotective mechanisms of the resurrection angiosperm Haberlea rhodopensis Friv. in response to desiccation and rehydration at morphological, physiological and biochemical levels. Environ. Exp. Bot. 2015, 113, 67–79. [Google Scholar] [CrossRef]
- Mihailova, G.; Abakumov, D.; Büchel, C.; Dietzel, L.; Georgieva, K. Drought-responsive gene expression in sun and shade plants of Haberlea rhodopensis under controlled environment. Plant Mol. Biol. Rep. 2017, 35, 313–322. [Google Scholar] [CrossRef]
- Georgieva, K.; Doncheva, S.; Mihailova, G.; Petkova, S. Response of sun- and shade- adapted plants of Haberlea rhodopensis to desiccation. Plant Growth Regul. 2012, 67, 121–132. [Google Scholar] [CrossRef]
- Garab, G.; Cseh, Z.; Kovács, L.; Rajagopal, S.; Várkonyi, Z.; Wentworth, M.; Mustárdy, L.; Dér, A.; Ruban, A.V.; Papp, E.; et al. Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: Thermo-optic mechanism. Biochemistry 2002, 41, 15121–15129. [Google Scholar] [CrossRef] [PubMed]
- Kranner, I.; Birtić, S. A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 2005, 45, 734–740. [Google Scholar] [CrossRef] [PubMed]
- Radermacher, A.L.; du Toit, S.F.; Farrant, J.M. Desiccation-driven senescence in the resurrection plant Xerophyta schlechteri (Baker) N.L. Menezes: Comparison of anatomical, ultrastructural and metabolic responses between senescent and non-senescent tissues. Front. Plant Sci. 2019, 10, 1396. [Google Scholar] [CrossRef]
- Vieira, E.A.; Gaspar, M.; Caldeira, C.F.; Munné-Bosch, S.; Braga, M.R. Desiccation tolerance in the resurrection plant Barbacenia graminifolia involves changes in redox metabolism and carotenoid oxidation. Front. Plant Sci. 2024, 15, 1344820. [Google Scholar] [CrossRef]
- Mundree, S.G.; Baker, B.; Mowla, S.; Peters, S.; Marais, S.; Vander Willigen, C.; Govender, K.; Maredza, A.; Muyanga, S.; Farrant, J.M.; et al. Physiological and molecular insights into drought tolerance. Afr. J. Biotechnol. 2002, 1, 28–38. [Google Scholar]
- Mihailova, G.; Kocheva, K.; Goltsev, V.; Kalaji, H.M.; Georgieva, K. Application of a diffusion model to measure ion leakage of resurrection plant leaves undergoing desiccation. Plant Physiol. Biochem. 2018, 125, 185–192. [Google Scholar] [CrossRef]
- Georgieva, K.; Mihailova, G.; Petkova, S. Photochemical efficiency of photosystem II during desiccation of shade-and sun-adapted plants of Haberlea rhodopensis. Proc. Bulg. Acad. Sci. 2012, 65, 631–638. [Google Scholar]
- Genty, B.; Harbinson, J.; Cailly, A.L.; Rizza, F. Fate of excitation at PS II in leaves: The non-photochemical side. In Proceedings of the Third BBSRC Robert Hill Symposium on Photosynthesis, Sheffield, UK, 31 March–3 April 1996. [Google Scholar]
- Charuvi, D.; Nevo, R.; Aviv-Sharon, E.; Gal, A.; Kiss, V.; Shimoni, E.; Farrant, J.M.; Kirchhoff, H.; Reich, Z. Chloroplast breakdown during dehydration of a homoiochlorophyllous resurrection plant proceeds via senescence-like processes. Environ. Exp. Bot. 2019, 157, 100–111. [Google Scholar] [CrossRef]
- Farrant, J.M.; Brandt, W.; Lindsey, G. An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 2007, 1, 72–84. [Google Scholar]
- Challabathula, D.; Puthur, J.T.; Bartels, D. Surviving metabolic arrest: Photosynthesis during desiccation and rehydration in resurrection plants. Ann. N. Y. Acad. Sci. 2016, 1365, 89–99. [Google Scholar] [CrossRef] [PubMed]
- Mihailova, G.; Büchel, C.; Dietzel, L.; Georgieva, K. Desiccation induced changes in photosynthesis related proteins of shade and sun Haberlea rhodopensis plants. Proc. Bulg. Acad. Sci. 2016, 69, 37–44. [Google Scholar]
- Tan, T.; Sun, Y.; Luo, S.; Zhang, C.; Zhou, H.; Lin, H. Efficient modulation of photosynthetic apparatus confers desiccation tolerance in the resurrection plant Boea hygrometrica. Plant Cell Physiol. 2017, 58, 1976–1990. [Google Scholar] [CrossRef]
- Charuvi, D.; Nevo, R.; Shimoni, E.; Naveh, L.; Zia, A.; Zach, A.; Farrant, J.M.; Kirchhoffd, H.; Reich, Z. Photoprotection conferred by changes in photosynthetic protein levels and organization during dehydration of a homoiochlorophyllous resurrection plant. Plant Physiol. 2015, 167, 1554–1565. [Google Scholar] [CrossRef]
- Dinakar, C.; Bartels, D. Light response, oxidative stress management and nucleic acid stability in closely related Linderniaceae species differing in desiccation tolerance. Planta 2012, 236, 541–555. [Google Scholar] [CrossRef]
- Solti, Á.; Mihailova, G.; Sárvári, É.; Georgieva, K. Antioxidative defence mechanism contributes to desiccation tolerance in Haberlea rhodopensis population naturally exposed to high irradiation. Acta Biol. Szeged. 2014, 58, 11–14. [Google Scholar]
- Jovanović, Ž.; Rakić, T.; Stevanović, B.; Radović, S. Characterization of oxidative and antioxidative events during dehydration and rehydration of resurrection plant Ramonda nathaliae. Plant Growth Regul. 2011, 64, 231–240. [Google Scholar] [CrossRef]
- Pandey, V.; Ranjan, S.; Deeba, F.; Pandey, A.K.; Singh, R.; Shirke, P.; Pathre, U. Desiccation-induced physiological and biochemical changes in resurrection plant, Selaginella bryopteris. J. Plant Physiol. 2010, 167, 1351–1359. [Google Scholar] [CrossRef]
- Gechev, T.S.; Benina, M.; Obata, T.; Tohge, T.; Sujeeth, N.; Minkov, I.; Hille, J.; Temanni, M.-R.; Marriott, A.S.; Bergström, E.; et al. Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell Mol. Life Sci. 2013, 70, 689–709. [Google Scholar] [CrossRef] [PubMed]
- Mittler, R.; Vanderauwera, S.; Suzuki, N.; Miller, G.A.D.; Tognetti, V.B.; Vandepoele, K.; Gollery, M.; Shulaev, V.; Van Breusegem, F. ROS signaling: The new wave? Trends Plant Sci. 2011, 16, 300–309. [Google Scholar] [CrossRef] [PubMed]
- Ashraf, M.F.M.R.; Foolad, M.R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 2007, 59, 206–216. [Google Scholar] [CrossRef]
- Reddy, A.; Chaitanya, K.; Vivekanandan, M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 2004, 161, 1189–1202. [Google Scholar] [CrossRef]
- Živković, T.; Quartacci, M.; Stevanović, B.; Marinone, F.; Navari-Izzo, F. Low-molecular weight substances in the poikilohydric plant Ramonda serbica during dehydration and rehydration. Plant Sci. 2005, 168, 105–111. [Google Scholar] [CrossRef]
- Mihailova, G.; Petkova, S.; Büchel, C.; Georgieva, K. Desiccation of the resurrection plant Haberlea rhodopensis at high temperature. Photosynth. Res. 2011, 108, 5–13. [Google Scholar] [CrossRef] [PubMed]
- Su, Y.; Yang, H.; Wu, Y.; Gong, W.; Gul, H.; Yan, Y.; Yang, W. Photosynthetic Acclimation of Shade-Grown Soybean Seedlings to a High-Light Environment. Plants 2023, 12, 2324. [Google Scholar] [CrossRef] [PubMed]
- Sano, S.; Takemoto, T.; Ogihara, A.; Suzuki, K.; Masumura, T.; Satoh, S.; Takano, K.; Mimura, Y.; Morita, S. Stress Responses of Shade-Treated Tea Leaves to High Light Exposure after Removal of Shading. Plants 2020, 9, 302. [Google Scholar] [CrossRef]
- Lichtenthaler, K.H. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 1987, 148, 350–382. [Google Scholar] [CrossRef]
- Esterbauer, H.; Cheeseman, K.H. Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods Enzymol. 1990, 186, 407–421. [Google Scholar] [CrossRef]
- Bates, L.S.; Waldren, R.P.; Teare, I.D. Rapid determination of free proline for water-stress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
- Genty, B.; Briantais, J.-M.; Baker, N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 1989, 990, 87–92. [Google Scholar] [CrossRef]
- van Kooten, O.; Snel, J. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 1990, 25, 147–150. [Google Scholar] [CrossRef] [PubMed]
- Brennan, T.; Frenkel, C. Involvement of Hydrogen Peroxide in the Regulation of Senescence in Pear. Plant Physiol. 1977, 59, 411–416. [Google Scholar] [CrossRef] [PubMed]
- Nakano, Y.; Asada, K. Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant Cell Physiol. 1981, 22, 867–880. [Google Scholar] [CrossRef]
- Beyer, W.F.; Fridovich, I. Assaying for Superoxide Dismutase Activity: Some Large Consequences of Minor Changes in Conditions. Anal. Biochem. 1987, 161, 559–566. [Google Scholar] [CrossRef]
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Georgieva, K.; Mihailova, G. Acclimation of the Resurrection Plant Haberlea rhodopensis to Changing Light Conditions. Plants 2024, 13, 3147. https://doi.org/10.3390/plants13223147
Georgieva K, Mihailova G. Acclimation of the Resurrection Plant Haberlea rhodopensis to Changing Light Conditions. Plants. 2024; 13(22):3147. https://doi.org/10.3390/plants13223147
Chicago/Turabian StyleGeorgieva, Katya, and Gergana Mihailova. 2024. "Acclimation of the Resurrection Plant Haberlea rhodopensis to Changing Light Conditions" Plants 13, no. 22: 3147. https://doi.org/10.3390/plants13223147
APA StyleGeorgieva, K., & Mihailova, G. (2024). Acclimation of the Resurrection Plant Haberlea rhodopensis to Changing Light Conditions. Plants, 13(22), 3147. https://doi.org/10.3390/plants13223147