Photosynthetica 2022, 60(1):136-146 | DOI: 10.32615/ps.2022.008

Limiting steps and the contribution of alternative electron flow pathways in the recovery of the photosynthetic functions after freezing-induced desiccation of Haberlea rhodopensis

K. GEORGIEVA1, A.V. POPOVA2, G. MIHAILOVA1, A.G. IVANOV2, 3, M. VELITCHKOVA2
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
3 Department of Biology, University of Western Ontario, 1151 Richmond Str. N, London, N6A 5B7 Ontario, Canada

Haberlea rhodopensis Friv. is unique with its ability to survive desiccation to an air-dry state during periods of extreme drought and freezing temperatures. To understand its survival strategies, it is important to examine the protective mechanisms not only during desiccation but also during rehydration. We investigated the involvement of alternative cyclic electron pathways during the recovery of photosynthetic functions after freezing-induced desiccation. Using electron transport inhibitors, the role of PGR5-dependent and NDH-dependent PSI-cyclic electron flows and plastid terminal oxidase were assessed during rehydration of desiccated leaves. Recovery of PSII and PSI, the capacity of PSI-driven cyclic electron flow, the redox state of plastoquinone pool, and the intersystem electron pool were analyzed. Data showed that the effect of alternative flows is more pronounced in the first hours of rehydration. In addition, the NDH-dependent cyclic pathway played a more determining role in the recovery of PSI than in the recovery of PSII.

Additional key words: alternative electron flow; chlorophyll fluorescence; cyclic electron flows; freezing-induced desiccation; rehydration.

Received: September 27, 2021; Revised: February 14, 2022; Accepted: February 16, 2022; Prepublished online: March 7, 2022; Published: March 18, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
GEORGIEVA, K., POPOVA, A.V., MIHAILOVA, G., IVANOV, A.G., & VELITCHKOVA, M. (2022). Limiting steps and the contribution of alternative electron flow pathways in the recovery of the photosynthetic functions after freezing-induced desiccation of Haberlea rhodopensis . Photosynthetica60(SPECIAL ISSUE 2022), 136-146. doi: 10.32615/ps.2022.008
Download citation

References

  1. Allen J.F.: Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. - Trends Plant Sci. 8: 15-19, 2003. Go to original source...
  2. Arnon D.I., Allen M.B., Whatley F.R.: Photosynthesis by isolated chloroplasts. - Nature 174: 394-396, 1954. Go to original source...
  3. Asada K.: The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. - Annu. Rev. Plant Phys. 50: 601-639, 1999. Go to original source...
  4. Asada K., Heber U., Schreiber U.: Pool size of electrons that can be donated to P700+, as determined in intact leaves: donation to P700+ from stromal components via the intersystem chain. - Plant Cell Physiol. 33: 927-932, 1992.
  5. Asada K., Heber U., Schreiber U.: Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as determined in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. - Plant Cell Physiol. 34: 39-50, 1993.
  6. 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...
  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. Cournac L., Josse E.M., Joët T. et al.: Flexibility in photosynthetic electron transport: a newly identified chloroplast oxidase involved in chlororespiration. - Philos. T. Roy. Soc. B 355: 1447-1454, 2000. Go to original source...
  9. DalCorso G., Pesaresi P., Masiero S. et al.: A Complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. - Cell 132: 273-285, 2008. Go to original source...
  10. 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...
  11. Díaz M., De Haro V., Muñoz R., Quiles M.J.: Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. - Plant Cell Environ. 30: 1578-1585, 2007. Go to original source...
  12. Endo T., Mi H., Shikanai T., Asada K.: Donation of electrons to plastoquinone by NAD(P)H dehydrogenase and by ferredoxin-quinone reductase in spinach chloroplasts. - Plant Cell Physiol. 38: 1272-1277, 1997. Go to original source...
  13. Farrant J.M.: Mechanisms of desiccation tolerance in angiosperm resurrection plants. - In: Jenks M.A., Wood A.J. (ed.): Plant Desiccation Tolerance. Pp. 51-90. Blackwell Publishing, Wallingford 2007. Go to original source...
  14. Fisher N., Kramer D.M.: Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: Relevance to cyclic electron flow around photosystem I? - BBA-Bioenergetics 1837: 1944-1954, 2014. Go to original source...
  15. Flores-Bavestrello A., Król M., Ivanov A.G. et al.: Two Hymenophyllaceae species from contrasting natural environments exhibit a homoiochlorophyllous strategy in response to desiccation stress. - J. Plant Physiol. 191: 82-94, 2016. Go to original source...
  16. Gao S., Niu J., Chen W. et al.: The physiological links of the increased photosystem II activity in moderately desiccated Porphyra haitanensis (Bangiales, Rhodophyta) to the cyclic electron flow during desiccation and re-hydration. - Photosynth. Res. 116: 45-54, 2013. Go to original source...
  17. Gao S., Shen S., Wang G. et al.: PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. - Plant Cell Physiol. 52: 885-893, 2011. Go to original source...
  18. 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...
  19. 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...
  20. Georgieva K., Mihailova G., Gigova L. et al.: The role of antioxidant defense in freezing tolerance of resurrection plant Haberlea rhodopensis. - Physiol. Mol. Biol. Pla. 27: 1119-1133, 2021. Go to original source...
  21. Georgieva K., Mihailova G., Velitchkova M., Popova A.: Recovery of photosynthetic activity of resurrection plant Haberlea rhodopensis from drought- and freezing-induced desiccation. - Photosynthetica 58: 911-921, 2020. Go to original source...
  22. 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, 2017. Go to original source...
  23. 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...
  24. 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...
  25. 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...
  26. Hüner N.P.A., Dahal K., Bode R. et al.: Photosynthetic acclimation, vernalization, crop productivity and 'the grand design of photosynthesis'. - J. Plant Physiol. 203: 29-43, 2016. Go to original source...
  27. Ivanov A.G., Morgan R.M., Gray G.R. et al.: Temperature/light dependence development of selective resistance to photoinhibition of photosystem I. - FEBS Lett. 430: 288-292, 1998. Go to original source...
  28. 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...
  29. Ivanov A.G., Sane P.V., Zeinalov Y. et al.: Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.). - Planta 213: 575-585, 2001. Go to original source...
  30. Klughammer C., Schreiber U.: Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated chloroplasts. - Z. Naturforsch. C 46: 233-244, 1991. Go to original source...
  31. Lichtenthaler H.K., Miehé J.A.: Fluorescence imaging as a diagnostic tool for plant stress. - Trends Plant Sci. 2: 316-320, 1997. Go to original source...
  32. Lichtenthaler H.K., Rinderle U.: The role of chlorophyll fluorescence in the detection of stress conditions in plants. - CRC Crit. Rev. Anal. Chem. 19: S29-S85, 1988. Go to original source...
  33. 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...
  34. Liu J., Moyankova D., Lin C.-T. et al.: Transcriptome reprogramming during severe dehydration contributes to physiological and metabolic changes in the resurrection plant Haberlea rhodopensis. - BMC Plant Biol. 18: 351, 2018. Go to original source...
  35. Losciale P., Oguchi R., Hendrickson L. et al.: A rapid, whole-tissue determination of the functional fraction of PSII after photoinhibition of leaves based on flash-induced P700 redox kinetics. - Physiol. Plantarum 132: 23-32, 2008. Go to original source...
  36. Mano J., Miyake C., Schreiber U., Asada K.: Photoactivation of electron flow from NADPH to plastoquinone in spinach chloroplasts. - Plant Cell Physiol. 36: 1589-1598, 1995.
  37. Maxwell P.C., Biggins J.: Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. - Biochemistry 15: 3975-3981, 1976. Go to original source...
  38. 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...
  39. Mihailova G., Solti Á., Sárvári É. et al.: Freezing tolerance of photosynthetic apparatus in the homoiochlorophyllous resurrection plant Haberlea rhodopensis. - Environ. Exp. Bot. 178: 104157, 2020. Go to original source...
  40. Miyake C.: Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. - Plant Cell Physiol. 51: 1951-1963, 2010. Go to original source...
  41. Mladenov P., Finazzi G., Bligny R. et al.: In vivo spectroscopy and NMR metabolite fingerprinting approaches to connect the dynamics of photosynthetic and metabolic phenotypes in resurrection plant Haberlea rhodopensis during desiccation and recovery. - Front. Plant Sci. 6: 564, 2015. Go to original source...
  42. Moore J.P., Le N.T., Brandt W.F. et al.: Towards a systems-based understanding of plant desiccation tolerance. - Trends Plant Sci. 14: 110-117, 2009. Go to original source...
  43. 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...
  44. Munekage Y., Hashimoto M., Miyake C. et al.: Cyclic electron flow around photosystem I is essential for photosynthesis. - Nature 429: 579-582, 2004. Go to original source...
  45. Munekage Y., Hojo M., Meurer J. et al.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. - Cell 110: 361-371, 2002. Go to original source...
  46. Peltier G., Cournac L.: Chlororespiration. - Annu. Rev. Plant Biol. 53: 523-550, 2002. Go to original source...
  47. Ravenel J., Peltier G., Havaux M.: The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. - Planta 193: 251-259, 1994. Go to original source...
  48. Sacksteder C.A., Kanazawa A., Jacoby M.E., Kramer D.M.: The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged. - P. Natl. Acad. Sci. USA 97: 14283-14288, 2000. Go to original source...
  49. Sárvári É., Mihailova G., Solti Á. et al.: Comparison of thylakoid structure and organization in sun and shade Haberlea rhodopensis populations under desiccation and rehydration. -J. Plant Physiol. 171: 1591-1600, 2014. Go to original source...
  50. Savitch L.V., Ivanov A.G., Gudynaite-Savitch L. et al.: Effects of low temperature stress on excitation energy partitioning and photoprotection in Zea mays. - Funct. Plant Biol. 36: 37-49, 2009. Go to original source...
  51. Savitch L.V., Ivanov A.G., Gudynaite-Savitch L. et al.: Cold stress effects on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. - Plant Cell Physiol. 52: 1042-1054, 2011. Go to original source...
  52. 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...
  53. Shikanai T.: Cyclic electron transport around photosystem I: Genetic approaches. - Annu. Rev. Plant Biol. 58: 199-217, 2007. Go to original source...
  54. Shikanai T., Endo T., Hashimoto T. et al.: Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. - P. Natl. Acad. Sci. USA 95: 9705-9709, 1998. Go to original source...
  55. Shikanai T., Yamamoto H.: Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. - Mol. Plant 10: 20-29, 2017. Go to original source...
  56. Stepien P., Johnson G.N.: Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis thaliana and the halophyte Tellungiella halophila. Role of the plastid terminal oxidase as an alternative electron sink. - Plant Physiol. 149: 1154-1165, 2009. Go to original source...
  57. Tagawa K., Tsujimoto H.Y., Arnon D.I.: Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. - P. Natl. Acad. Sci. USA 49: 567-572, 1963. Go to original source...
  58. van Kooten O., Snel J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  59. Walker B.J., VanLoocke A., Bernacchi C.J., Ort D.R.: The costs of photorespiration to food production now and in the future. - Annu. Rev. Plant Biol. 67: 107-129, 2016. Go to original source...
  60. Yamori W., Sakata N., Suzuki Y. et al.: Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. - Plant J. 68: 966-976, 2011. Go to original source...
  61. Yang Q., Blanco N.E., Hermida-Carrera C. et al.: Two dominant boreal conifers use contrasting mechanisms to reactivate photosynthesis in the spring. - Nat. Commun. 11: 128, 2020. Go to original source...
  62. Zia A., Walker B.J., Oung H.M.O. et al.: Protection of the photosynthetic apparatus against dehydration stress in the resurrection plant Craterostigma pumilum. - Plant J. 87: 664-680, 2016. Go to original source...