Photosynthetica 2020, 58(4):911-921 | DOI: 10.32615/ps.2020.044

Recovery of photosynthetic activity of resurrection plant Haberlea rhodopensis from drought- and freezing-induced desiccation

K. GEORGIEVA1, G. MIHAILOVA1, M. VELITCHKOVA2, A. POPOVA2
1 Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bonchev str., Bl. 21, 1113 Sofia, Bulgaria
2 Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev str., Bl. 21, 1113 Sofia, Bulgaria

The recovery of photosynthetic activity during rehydration of Haberlea rhodopensis from drought- and freezing-induced desiccation were investigated. The water uptake during the initial 15 h was slow thus preventing cellular damages. The results showed faster recovery of quantum efficiency of PSII in plants rehydrated after freezing stress (RAF) compared to plants rehydrated after drought stress (RAD) and the most significant differences between them were evident after 9-15 h of rehydration. Following rehydration, PSI activity recovered faster compared to PSII and in contrast to PSII, its activity was higher in RAD compared to RAF plants. During the first hours of rehydration, prominent alterations in energy transfer between photosynthetic complexes occurred as revealed by 77 K fluorescence of isolated thylakoids. High proportion of thermal energy dissipation in dry plants and during the first hours of rehydration protects them from photooxidation; the role of PSII reaction center quenching during the recovery was suggested.

Additional key words: 77 K fluorescence spectra; chlorophyll fluorescence; desiccation tolerance.

Received: March 20, 2020; Revised: May 22, 2020; Accepted: May 27, 2020; Prepublished online: June 22, 2020; Published: September 4, 2020  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
GEORGIEVA, K., MIHAILOVA, G., VELITCHKOVA, M., & POPOVA, A. (2020). Recovery of photosynthetic activity of resurrection plant Haberlea rhodopensis from drought- and freezing-induced desiccation. Photosynthetica58(4), 911-921. doi: 10.32615/ps.2020.044
Download citation

References

  1. Andrizhiyevskaya E.G., Chojnicka A., Bautista J.A. et al.: Origin of the F685 and F695 fluorescence in Photosystem II. -Photosynth. Res. 84: 173-180, 2005. Go to original source...
  2. Benina M., Obata T., Mehterov N. et al.: Comparative metabolic profiling of Haberlea rhodopensis, Thellungiella halophyla, and Arabidopsis thaliana exposed to low temperature. - Front. Plant Sci. 4: 499, 2013. Go to original source...
  3. Bernacchia G., Salamini F., Bartels D.: Molecular characteriza-tion of the rehydration process in the resurrection plant Craterostigma plantagineum. - Plant Physiol. 111: 1043-1050, 1996. Go to original source...
  4. Bewley J.D.: Physiological aspects of desiccation tolerance. - Ann. Rev. Plant Physio. 30: 195-238, 1979. Go to original source...
  5. Bewley J.D., Oliver M.J.: Desiccation tolerance in vegetative plant tissues and seeds: protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. - In: Somero G.N., Osmond C.B., Bolis C.L. (ed.): Water and Life. Pp. 141-160. Springer, Berlin-Heidelberg 1992. Go to original source...
  6. Bruce D., Samson G., Carpenter C.: The origins of non-photochemical quenching of chlorophyll in photosynthesis. Direct quenching by P680(+) in photosystem II enriched membranes at low pH. - Biochemistry-US 36: 749-755, 1997. Go to original source...
  7. Charuvi D., Nevo R., Shimoni E. et al.: Photoprotection conferred by changes in photosynthetic protein levels and organization during dehydration of a homoiochlorophyllous resurrection plant. - Plant Physiol. 167: 1554-1565, 2015. Go to original source...
  8. Cooper K., Farrant J.M.: Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. - J. Exp. Bot. 53: 1805-1813, 2002. Go to original source...
  9. Daskalova E., Dontcheva S., Yahoubian G. et al.: A strategy for conservation and investigation of the protected resurrection plant Haberlea rhodopensis Friv. - BioRisk 6: 41-60, 2011. Go to original source...
  10. Daskalova E., Dontcheva S., Yahubyan G. et al.: Ecological characteristics and conservation of the protected resurrection species Haberlea rhodopensis Friv. as in vitro plants through a modified micropropagation system. - Biotechnol. Biotec. Eq. 24: 213-217, 2010. Go to original source...
  11. Degl'Innocenti E., Guidi L., Stevanovic B., Navari F.: CO2 fixation and chlorophyll a fluorescence in leaves of Ramonda serbica during a dehydration-rehydration cycle. - J. Plant Physiol. 165: 723-733, 2008. Go to original source...
  12. Demmig-Adams B., Adams III W.W., Barker D.H. et al.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. - Physiol. Plantarum 98: 253-264, 1996. Go to original source...
  13. Deng X., Hu Z.A., Wang H.X. et al.: A comparison of photosynthetic apparatus of the detached leaves of the resurrection plant Boea hygrometrica with its non-tolerant relative Chirita heterotrichia in response to dehydration and rehydration. - Plant Sci. 165: 851-861, 2003. Go to original source...
  14. Djilianov D., Ivanov S., Moyankova D. et al.: 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, 2011. Go to original source...
  15. Farrant J.M.: Mechanisms of desiccation tolerance in angiosperm resurrection plants. - In: Jenks M., Wood A. (ed.): Plant Desiccation Tolerance. Pp. 51-90. Blackwell Publishing, Wallingford 2007. Go to original source...
  16. Farrant J.M., Brandt W.F., Lindsey G.G.: An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. - Plant Stress 1: 72-84, 2007.
  17. Farrant J.M., Cooper K., Kruger L.A., Sherwin H.W.: The effect of drying rate on the survival of three desiccation-tolerant angiosperm species. - Ann. Bot.-London 84: 371-379, 1999. Go to original source...
  18. Fernįndez-Marķn B., Nadal M., Gago J. et al.: Born to revive: molecular and physiological mechanisms of double tolerance in a paleotropical and resurrection plant. - New Phytol. 226: 741-759, 2020. Go to original source...
  19. Fernįndez-Marķn B., Neuner G., Kuprian E. et al.: First evidence of freezing tolerance in a resurrection plant: insights into molecular mobility and zeaxanthin synthesis in the dark. - Physiol. Plantarum 163: 472-489, 2018. Go to original source...
  20. Flores-Bavestrello A., Król M., Ivanov A.G. et al.: Two Hymenophyllaceae species from contrasting natural environ-ments exhibit a homoiochlorophyllous strategy in response to desiccation stress. - J. Plant Physiol. 191: 82-94, 2016. Go to original source...
  21. Gaff D.F., Oliver M.: The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. - Funct. Plant Biol. 40: 315, 2013. Go to original source...
  22. Gao S., Wang G.: The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). - J. Exp. Bot. 63: 4349-4358, 2012. Go to original source...
  23. Gashi B., Babani F., Kongjika E.: 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. Pla. 19: 333-341, 2013. Go to original source...
  24. Gashi B., Kongjika E., Osmani M., Luma V.: Activity of δ-aminolevulinic acid dehydratase at Ramonda nathaliae and Ramonda serbica plants during dehydration and rehydration. - Biol. Futur. 70: 210-217, 2019. Go to original source...
  25. Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - BBA-Gen. Subjects 990: 87-92, 1989. Go to original source...
  26. Georgieva K., Dagnon S., Gesheva E. et al.: Antioxidant defense during desiccation of the resurrection plant Haberlea rhodopensis. - Plant Physiol. Bioch. 114: 51-59, 2017a. Go to original source...
  27. Georgieva K., Maslenkova L., Peeva V. et al.: Comparative study on the changes in photosynthetic activity of the homoiochlorophyllous desiccation-tolerant Haberlea rhodo-pensis and desiccation-sensitive spinach leaves during desiccation and rehydration. - Photosynth. Res. 85: 191-203, 2005. Go to original source...
  28. Georgieva K., Mihailova G.: Drought tolerance of photosyn-thesis. - In: Pessarakli M. (ed.): Handbook of Photosynthesis. 3rd Edition. Pp. 683-695. CRC Press, Boca Raton 2016. Go to original source...
  29. Georgieva K., Mihailova G., Gigova L. et al.: Freezing tolerance of resurrection plant Haberlea rhodopensis.- In: FEBS Advanced Courses - Resurrection Plants: Hope for Crop Drought Tolerance (ReHOPE) (Abstract Book). Pp. 13. 20-22 September, Plovdiv, Bulgaria 2018. https://rehope2018.febsevents.org/
  30. Georgieva K., Rapparini F., Bertazza G. et al.: Alterations in the sugar metabolism and in the vacuolar system of mesophyll cells contribute to the desiccation tolerance of Haberlea rhodopensis ecotypes. - Protoplasma 254: 193-201, 2017b. Go to original source...
  31. Georgieva K., Röding A., Büchel C.: Changes in some thylakoid membrane proteins and pigments upon desiccation of the resurrection plant Haberlea rhodopensis. - J. Plant Physiol. 166: 1520-1528, 2009. Go to original source...
  32. Georgieva K., Szigeti Z., Sarvari E. et al.: Photosynthetic activity of homoiochlorophyllous desiccation tolerant plant Haberlea rhodopensis during dehydration and rehydration. - Planta 225: 955-964, 2007. Go to original source...
  33. Giarola V., Bartels D.: What can we learn from the transcriptome of the resurrection plant Craterostigma plantagineum? - Planta 242: 427-434, 2015. Go to original source...
  34. Giarola V., Hou Q., Bartels D.: Angiosperm plant desiccation tolerance: hints from transcriptomics and genome sequencing. - Trends Plant Sci. 22: 705-717, 2017. Go to original source...
  35. Heber U.: Photoprotection of green plants: a mechanism of ultra-fast thermal energy dissipation in desiccated lichens. - Planta 228: 641-650, 2008. Go to original source...
  36. Heber U., Azarkovich M., Shuvalov V.: Activation of mechanisms of photoprotection by desiccation and by light: poikilohydric photoautotrophs. - J. Exp. Bot. 58: 2745-2759, 2007. Go to original source...
  37. Heber U., Bilger W., Shuvalov V.A.: Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. - J. Exp. Bot. 57: 2993-3006, 2006b. Go to original source...
  38. Heber U., Lange O.L., Shuvalov V.A.: Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. - J. Exp. Bot. 57: 1211-1223, 2006a. Go to original source...
  39. Heber U., Shuvalov V.A.: Photochemical reactions of chlorophyll in dehydrated photosystem II: two chlorophyll forms (680 and 700 nm). - Photosynth. Res. 84: 85-91, 2005. Go to original source...
  40. Horton P., Ruban A.: Regulation of Photosystem II. - Photosynth. Res. 34: 375-385, 1992. Go to original source...
  41. Huang W., Yang S.J., Zhang S.B. et al.: Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. - Planta 235: 819-828, 2012. Go to original source...
  42. Hundal T., Virgin I., Styring S., Andersson B.: Changes in the organization of photosystem II following light-induced D1-protein degradation. - BBA-Bioenergetics 1017: 235-241, 1990. Go to original source...
  43. Hüner N.P., Öquist G., Melis A.: Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes. - In: Green B.R., Parson W.W. (ed.): Light-Harvesting Antennas in Photosynthesis. Advances in Photosynthesis and Respiration. Vol. 13. Pp. 401-421. Springer, Dordrecht 2003. Go to original source...
  44. Ivanov A.G., Rosso D., Savitch L.V. et al.: Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold acclimated Arabidopsis thaliana. - Photosynth. Res. 113: 191-206, 2012. Go to original source...
  45. Jovanovię ®., Rakię T., Stevanovię B., Radovię S.: Charac-terization of oxidative and antioxidative events during dehydration and rehydration of resurrection plant Ramonda nathaliae. - Plant Growth Regul. 64: 231-240, 2011. Go to original source...
  46. Kappen L.: [The influence of water content on the resistance of plants to high and low temperatures, examined on leaves of some ferns and Ramonda myconi.] - Flora 156: 427-445, 1966. https://doi.org/10.1016/S0367-1836(17)30278-1 [In German] Go to original source...
  47. Krause G.H., Weis E.: Chlorophyll fluorescence and photo-synthesis. The basics. - Annu. Rev. Plant Phys. 42: 313-349, 1991. Go to original source...
  48. Lawlor D.W., Cornic G.: Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. - Plant Cell Environ. 25: 275-294, 2002. Go to original source...
  49. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
  50. Liu J., Moyankova D., Djilianov D., Deng X.: Common and specific mechanisms of desiccation tolerance in two Gesneriaceae resurrection plants. Multiomics evidences. - Front. Plant Sci. 10: 1067, 2019. Go to original source...
  51. McDonald A.E., Ivanov A.G., Bode R. et al.: Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). - BBA-Bioenergetics 1807: 954-967, 2011. Go to original source...
  52. Morse M., Rafudeen M.S., Farrant J.M.: An overview of the current understanding of desiccation tolerance in the vegetative tissues of higher plants. - In: Turkan I. (ed.): Advances in Botanical Research. Vol. 57. Pp. 319-347. Elsevier, Amsterdam 2011. Go to original source...
  53. Oliver M.J., Tuba Z., Mishler B.D.: The evolution of vegetative desiccation tolerance in land plants. - Plant Ecol. 151: 85-100, 2000. Go to original source...
  54. Peeva V., Cornic G.: Leaf photosynthesis of Haberlea rhodo-pensis before and during drought. - Environ. Exp. Bot. 65: 310-318, 2009. Go to original source...
  55. Péli E.R., Mihailova G., Petkova S. et al.: Differences in physiological adaptation of Haberlea rhodopensis Friv. leaves and roots during dehydration-rehydration cycle. - Acta Physiol. Plant. 34: 947-955, 2012. Go to original source...
  56. Petrova G., Moyankova D., Nishii K. et al.: The European paleoendemic Haberlea rhodopensis (Gesneriaceae) has an Oligocene origin and a Pleistocene diversification and occurs in a long-persisting refugial area in Southeastern Europe. - Int. J. Plant Sci. 176: 499-514, 2015. Go to original source...
  57. Popova A.V., Dobrev K, Velitchkova M., Ivanov A.G.: Differential temperature effects on dissipation of excess light energy and energy partitioning in lut2 mutant of Arabodopsis thaliana under photoinhibitory conditions. - Photosynth. Res. 139: 367-385, 2019. Go to original source...
  58. Rakię T., Lazarevię M., Jovanovię ®.S. et al.: 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: 550, 2014. Go to original source...
  59. Savitch L.V., Ivanov A.G., Krol M. et al.: Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. - Plant Cell Physiol. 51: 1555-1570, 2010. Go to original source...
  60. Sgherri C., Stevanovię B., Navari-Izzo F.: Role of phenolic in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. - Physiol. Plantarum 112: 478-485, 2004. Go to original source...
  61. Tan T., Sun Y., Luo S. et al.: Efficient modulation of photosynthetic apparatus confers desiccation tolerance in the resurrection plant Boea hygrometrica. - Plant Cell Physiol. 58: 1976-1990, 2017. Go to original source...
  62. van Kooten O., Snel J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  63. Velitchkova M., Popova A.: High light-induced changes of 77 K fluorescence emission of pea thylakoid membranes with altered membrane fluidity. - Bioelectrochemistry 67: 81-90, 2005. Go to original source...
  64. Vertucci C.W., Farrant J.M.: Acquisition and loss of desiccation tolerance. - In: Kigel J., Galili G. (ed.): Seed Development and Germination. Pp. 237-271. Marcel Dekker, New York 1995. Go to original source...
  65. ®ivkovię T., Quartacci M.F., Stevanovię B. et al.: Low-molecular weight substances in the poikilohydric plant Ramonda serbica during dehydration and rehydration. - Plant Sci. 168: 105-111, 2005. Go to original source...