Ramonda nathaliae and Ramonda serbica are resurrection plants belonging to homoiochlorophyllous desiccation-tolerant angiosperms. Chlorophyll biosynthesis is one of the most important metabolic pathways to tolerate desiccation in these plant species.
To better understand the early pathway steps of chlorophyll biosynthesis, we have analyzed the enzyme δ-aminolevulinic acid dehydratase (ALA-D) and contents of δ-aminolevulinic acid (ALA) and total chlorophyll as a final product during dehydration and rehydration stages for these plant species.
Our results showed that the activity of ALA-D in R. nathaliae and R. serbica plants rapidly decreased during dehydration and in the final stage of desiccation the activity of this enzyme was decreased by 79% and 86%, respectively. After rehydration of plants, the ALA-D activity was fully restored. In contrast, the ALA content of both plant species significantly increased during desiccation and decreased after 48 hr of rewatering. In each stage of dehydration or rehydration, a significant negative correlation was established between ALA-D activity and ALA content in both plant species.
Total chlorophyll content was preserved more in R. nathaliae than in R. serbica during desiccation. Moreover, ALA-D activity was decreased to a minimal level but preserved its function during desiccation, and this suggests one possible mechanism of desiccation tolerance to retain the chlorophyll of these plant species.
Alpert, P. (2000) The discovery, scope and puzzle of desiccation-tolerance in plants. Plant Ecol. 151, 5–17.
Augusti, A., Scartazza, A., Navari-Izzo, F., Sgherri, C. L. M., Stevanoviç, B., Brugnoli, E. (2001) Photosystem II photochemical efficiency, zeaxanthin and antioxidant contents in the poikilohydric Ramonda serbica during dehydration and rehydration. Photosynth. Res. 67, 79–88.
Daskalova, E., Dontcheva, S., Zekaj, Z., Bacu, A., Sota, V., Abdullai, K., Gashi, B., Minkov, I., Toneva, V., Kongjika, E. (2012) Initial determination of polymorphism and in vitro conservation of some Ramonda serbica and Ramonda nathaliae populations from Albania, Macedonia and Bulgaria. Biotechnol. Biotec. Eq. 26, 16–25.
Degl’Innocenti, E., Guidi, L., Stevanoviç, B., Navari, F. (2008) CO2 fixation and chlorophyll a fluorescence in leaves of Ramonda serbica during a dehydration–rehydration cycle. J. Plant Physiol. 165, 723–733.
Djilianov, D., Ivanov, S., Moyankova, D., Miteva, L., Kirova, E., Alexieva, V., Joudi, M., Peshev, D., Van den Ende, W. (2011) Sugar ratios, glutathione redox status and phenols in the resurrection species Haberlea rhodopensis and the closely related non-resurrection species Chirita eberhardtii. Plant Biol. 13, 767–776.
Dontcheva, S., Daskalova, E., Yahubyan, G., Denev, I., Minkov, I., Toneva, V. (2009) Conservation of the protected resurrection species Ramonda serbica Panc. – Habitat Montana district, Bulgaria as in vitro plants through a modified micropropagation system. Biotechnol. Biotec. Eq. 23(2), 369–372.
Drazic, G., Mihailovic, N., Stevanovic, B. (1999) Chlorophyll metabolism in leaves of higher poikilohidric plant Ramonda serbica Panc & Ramonda nathaliae Panc et Petrov during dehydration and rehydration. J. Plant Physiol. 154, 379–384.
Farrant, J. M. (2000) Comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plants. Plant Ecol. 151, 29–39.
Farrant, J. M., Brandt, W., Lindsey, G. G. (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1, 72–84.
Gaff, D. F. (1989) Responses of desiccation tolerant “resurrection” plants to water stress. In: Kreeb, K. H., Richter, H., Hinkley, T. M. (eds.) Structural and Functional Responses to Environmental Stresses. SPB Academic Publishing, The Hague, pp. 255–268.
Gaff, D. F., Oliver, M. (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct. Plant Biol. 40, 315–328.
Gashi, B., Abdullai, K., Mata, V., Kongjika, E. (2012) Effect of gibberellic acid and potassium nitrate on seed germination of the resurrection plants Ramonda serbica and Ramonda nathaliae. Afr. J. Biotech. 11(20), 4537–4542.
Gashi, B., Abdullai, K., Sota, V., Kongjika, E. (2015) Micropropagation and in vitro conservation of the rare and threatened plants Ramonda serbica and Ramonda nathaliae. Physiol. Mol. Biol. Plants 21, 123–136.
Gashi, B., Babani, F., Kongjika, E. (2013) Chlorophyll fluorescence imaging of photosynthetic activity and pigment contents of the resurrection plants Ramonda serbica and Ramonda nathaliae during dehydration and rehydration. Physiol. Mol. Biol. Plants 19, 333–341.
Georgieva, K., Sárvári, É., Keresztes, Á. (2010) Protection of thylakoids against combined light and drought by a luminal substance in the resurrection plant Haberlea rhodopensis. Ann. Bot. 105, 117–126.
Jaffe, E. K. (2000) The porphobilinogen synthase family of metalloenzymes. Acta Cryst. D. 56, 115–128.
Jain, M., Gadre, R. P. (2004) Inhibition of 5-aminolevulinic acid dehydratase activity by arsenic in excised etiolated maize leaf segments during greening. J. Plant Physiol. 161(3), 251–255.
Jovanoviç, Z., Rakic, T., Stevanovic, B., Radovic, S. (2011) Characterization of oxidative and antioxidative events during dehydration and rehydration of resurrection plant Ramonda nathaliae. J. Plant Growth Regul. 64, 231–240.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
Markovska, Y. K., Tonsev, T. D., Kimenov, G. P., Tutekova, A. A. (1994) Physiological changes in higher poikilohidric plants – Haberlea rhodopensis Friv. and Ramonda serbica Panc. during drought and rewatering at different light regimes. J. Plant Physiol. 144, 100–108.
Mihailova, G., Petkova, S., Buchel, C., Georgieva, K. (2011) Desiccation of the resurrection plant Haberlea rhodopensis at high temperature. Photosynth. Res. 108, 5–13.
Nagy-Deri, H., Peli, E. R., Georgieva, K., Tuba, Z. (2011) Changes in chloroplast morphology of different parenchyma cells in leaves of Haberlea rhodopensis Friv. during desiccation and following rehydration. Photosynthetica 49, 119–126.
Navari-Izzo, F., Pinzino, C., Quartacci, M. F., Sgherri, C. L. M., Izzo, R. (1994) Intracellular membranes: kinetics of superoxide production and changes in thylakoids of resurrection plants upon dehydration and rehydration. Proc. R. Soc. Edinburgh. 102B, 187–191.
Navari-Izzo, F., Rascio, N. (1999) Plant response to water deficit conditions. In: Pessarakli, M. (ed.) Handbook of Plant and Crop Stress. Marcel-Dekker, New York, NY, pp. 231–270.
Noriega, G. O., Balestrasse, K. B., Batlle, A., Tomaro, M. A. (2007) Cadmium induced oxidative stress in soybean plants also by the accumulation of δ-aminolevulinic acid. Biometals 20(6), 841–851.
Osmani, M., Tuna, M., Elezaj, I. R. (2018) Concentration of some metals in soil and plant organs and their biochemical profiles in Tulipa luanica, T. kosovarica and T. albanica native plant species. Physiol. Mol. Biol. Plants 24, 1117–1126.
Péli, E. R., Mihailova, G., Petkova, S., Tuba, Z., Georgieva, K. (2012) Differences in physiological adaptation of Haberlea rhodopensis Friv. leaves and roots during dehydration–rehydration cycle. Acta Physiol. Plant. 34, 947–955.
Porembski, S., Barthlott, W. (2000) Granitic and gneissic outcrops (inselbergs) as centres of diversity for desiccation-tolerant vascular plants. Plant Ecol. 151, 19–28.
Porra, R. J., Thompson, W. A., Kriedemann, P. E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim. Biophys. Acta 975, 384–394.
Quartacci, M. F., Glisic, O., Stevanovic, B., Navari-Izzo, F. (2002) Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration. J. Exp. Bot. 53, 2159–2166.
Rakic, T., Lazarevic, M., Jovanovic, Z. S., Radovic, S., Siljak-Yakovlev, S., Stevanovic, B., Stevanovic, V. (2014) Resurrection plants of the genus Ramonda: prospective survival strategies – unlock further capacity of adaptation, or embark on the path of evolution? Front Plant Sci. 4, 1–9.
Rakic, T., Quartacci, M. F., Cardelli, R., Navari-Izzo, F., Stevanovic, B. (2009) Soil properties and their effect on water and mineral status of resurrection Ramonda serbica. Plant Ecol. 203, 13–21.
Rocha, J. B. T., Pereira, M. E., Emanuelli, T., Christofari, R. S., Souza, D. (1995) Effects of methylmercury exposure during the second stage of rapid postnatal brain growth on delta-aminolevulinic acid dehydratase (ALA-D) activity in brain, liver, kidney and blood of suckling rats. Toxicology 100, 27–37.
Schiller, P., Heilmeier, H., Hartung, W. (1998) Uptake of amino acids by the aquatic resurrection plant Chamaegigas intrepidus and its implication for N nutrition. Oecologia 117, 63–69.
Schwab, K. B., Gaff, D. F. (1990) Influence of compatible solutes on soluble enzymes from desiccation-tolerant Sporobolus stapfianus and desiccation-sensitive Sporobolus pyramidalis. J. Plant Physiol. 137, 208–215.
Schwab, K. B., Schreiber, U., Heber, U. (1989) Response of photosynthesis and respiration of resurrection plants to desiccation and rehydration. Planta 177, 217–227.
Sgherri, C., Stevanovic, B., Navari-Izzo, F. (2004) Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol. Plant. 122, 478–485.
Sgherri, C. L. M., Loggini, B., Puliga, S., Navari-Izzo, F. (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35, 561–565.
Siljak-Yakovlev, S., Stevanoviç, V., Tomaseviç, M., Brown, C. S., Stevanoviç, B. (2008) Genome size variation and polyploidy in the resurrection plant genus Ramonda: cytogeography of living fossils. Environ. Exp. Bot. 62, 101–112.
Stevanovic, V., Niketic, M., Stevanovic, B. (1991) Chorological differentiation of endemo-relic species Ramonda serbica Panc. and R. nathaliae Panc. et Petrov. (Gesneriaceae) on the Balkan Peninsula. Bot. Chron. 10, 507–515.
Tanaka, R., Tanaka, A. (2007) Tetrapyrrole biosynthesis in higher plants. Annu. Rev. Plant Biol. 58, 321–346.
Tewari, A. K., Tripathy, S. (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol. 117, 851–858.
Toldi, O., Tuba, Z., Scott, P. (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci. 176, 187–199.
Tuba, Z., Proctor, M. C. F., Csintalan, Z. (1998) Ecophysiological responses of homoichlorophyllous and poikilochlorophyllous desiccation-tolerant plant Xerophyta scabrida at present day CO2 concentration. Plant Physiol. Biochem. 35, 381–386.
Veljovic-Jovanoviç, S., Kukavica, B., Stevanoviç, B., Navari-Izzo, F. (2006) Senescence- and drought-related changes in peroxidase and superoxide dismutase isoforms in leaves of Ramonda serbica. J. Exp. Bot. 57, 1759–1768.
Zhang, Q., Song, X., Bartels, D. (2016) Enzymes and metabolites in carbohydrate metabolism of desiccation tolerant plants. Proteomes 40, 1–14.
Zivkoviç, T., Quartacci, M. F., Stevanoviç, B., Marinone, F., Navari-Izzo, F. (2005) Low molecular weight substances in the poikilohydric plant Ramonda serbica during dehydration and rehydration. Plant Sci. 168, 105–111.