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.

Department of Biology University of Western Ontario 1151 Richmond Str N London N6A 5B7 Ontario Canada

Institute of Biophysics and Biomedical Engineering Bulgarian Academy of Sciences Acad G Bonchev Str Bl 21 1113 Sofia Bulgaria

Institute of Plant Physiology and Genetics Bulgarian Academy of Sciences Acad G Bonchev Str Bl 21 1113 Sofia Bulgaria

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Allen J.F.: Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. – Trends Plant Sci. 8: 15-19, 2003. https://www.sciencedirect.com/science/article/pii/S1360138502000067?via%3Dihub PubMed

Arnon D.I., Allen M.B., Whatley F.R.: Photosynthesis by isolated chloroplasts. – Nature 174: 394-396, 1954. https://www.nature.com/articles/174394a0 PubMed

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. https://www.annualreviews.org/doi/10.1146/annurev.arplant.50.1.601 PubMed DOI

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. https://academic.oup.com/pcp/article/33/7/927/1822209

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. https://academic.oup.com/pcp/article/34/1/39/1853089

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. https://link.springer.com/chapter/10.1007/978-3-642-76682-4_10 DOI

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. https://academic.oup.com/plphys/article/167/4/1554/6113757 PubMed PMC

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. https://royalsocietypublishing.org/doi/10.1098/rstb.2000.0705 PubMed DOI PMC

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. https://www.sciencedirect.com/science/article/pii/S0092867408000457?via%3Dihub PubMed

Demmig-Adams B., Adams W.W. III, 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. https://onlinelibrary.wiley.com/doi/abs/10.1034/j.1399-3054.1996.980206.x DOI

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. https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-3040.2007.01735.x PubMed DOI

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.

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. https://onlinelibrary.wiley.com/doi/10.1002/9780470376881.ch3 DOI

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. https://www.sciencedirect.com/science/article/pii/S0005272814005878?via%3Dihub PubMed

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. https://www.sciencedirect.com/science/article/pii/S0176161715002722?via%3Dihub PubMed

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. https://link.springer.com/article/10.1007/s11120-013-9892-4 PubMed DOI

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. https://academic.oup.com/pcp/article/52/5/885/1827954 PubMed

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. https://academic.oup.com/jxb/article/63/12/4349/640622?login=true PubMed

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. https://www.sciencedirect.com/science/article/pii/S0304416589800169?via%3Dihub

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. https://link.springer.com/article/10.1007/s12298-021-00998-0 PubMed DOI PMC

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. https://ps.ueb.cas.cz/artkey/phs-202004-0003_recovery-of-photosynthetic-activity-of-resurrection-plant-haberlea-rhodopensis-from-drought-and-freezing-induc.php

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. https://link.springer.com/article/10.1007/s00709-015-0932-0 PubMed DOI

Giarola V., Bartels D.: What can we learn from the transcriptome of the resurrection plant Craterostigma plantagineum? – Planta 242: 427-434, 2015. https://link.springer.com/article/10.1007/s00425-015-2327-z PubMed DOI

Giarola V., Hou Q., Bartels D.: Angiosperm plant desiccation tolerance: hints from transcriptomics and genome sequencing. – Trends Plant Sci. 22: 705-717, 2017. https://www.sciencedirect.com/science/article/pii/S1360138517301097?via%3Dihub PubMed

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. https://link.springer.com/article/10.1007/s00425-011-1544-3 PubMed DOI

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. https://www.sciencedirect.com/science/article/pii/S0176161716300360?via%3Dihub PubMed

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. https://febs.onlinelibrary.wiley.com/doi/abs/10.1016/S0014-5793%2898%2900681-4 PubMed DOI

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. https://link.springer.com/article/10.1007/s11120-012-9769-y PubMed DOI

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. https://link.springer.com/article/10.1007/s004250100522 PubMed DOI

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. https://www.degruyter.com/document/doi/10.1515/znc-1991-3-413/html DOI

Lichtenthaler H.K., Miehé J.A.: Fluorescence imaging as a diagnostic tool for plant stress. – Trends Plant Sci. 2: 316-320, 1997. https://www.sciencedirect.com/science/article/pii/S1360138597899542?via%3Dihub

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. https://www.tandfonline.com/doi/abs/10.1080/15476510.1988.10401466 DOI

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. https://www.frontiersin.org/articles/10.3389/fpls.2019.01067/full PubMed DOI PMC

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. https://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-018-1566-0 PubMed DOI PMC

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. https://onlinelibrary.wiley.com/doi/10.1111/j.1399-3054.2007.01000.x PubMed DOI

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. https://academic.oup.com/pcp/article/36/8/1589/1819678?login=true

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. https://pubs.acs.org/doi/abs/10.1021/bi00663a011 PubMed DOI

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. https://www.sciencedirect.com/science/article/pii/S0005272810007425?via%3Dihub PubMed

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. https://www.sciencedirect.com/science/article/pii/S0098847220301830?via%3Dihub

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. https://academic.oup.com/pcp/article/51/12/1951/1944496 PubMed

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. https://www.frontiersin.org/articles/10.3389/fpls.2015.00564/full PubMed DOI PMC

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. https://www.sciencedirect.com/science/article/pii/S1360138509000223?via%3Dihub PubMed

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. https://www.sciencedirect.com/science/article/pii/B9780123876928000096

Munekage Y., Hashimoto M., Miyake C. et al.: Cyclic electron flow around photosystem I is essential for photosynthesis. – Nature 429: 579-582, 2004. https://www.nature.com/articles/nature02598 PubMed

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. https://www.sciencedirect.com/science/article/pii/S009286740200867X?via%3Dihub PubMed

Peltier G., Cournac L.: Chlororespiration. – Annu. Rev. Plant Biol. 53: 523-550, 2002. https://www.annualreviews.org/doi/10.1146/annurev.arplant.53.100301.135242 PubMed DOI

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. https://link.springer.com/article/10.1007/BF00192538 DOI

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. https://www.pnas.org/content/97/26/14283 PubMed PMC

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. https://www.sciencedirect.com/science/article/pii/S0176161714001989?via%3Dihub PubMed

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. https://www.publish.csiro.au/fp/FP08093 PubMed

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. https://academic.oup.com/pcp/article/52/6/1042/1872739?login=true PubMed

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. https://academic.oup.com/pcp/article/51/9/1555/1826825?login=true PubMed

Shikanai T.: Cyclic electron transport around photosystem I: Genetic approaches. – Annu. Rev. Plant Biol. 58: 199-217, 2007. https://www.annualreviews.org/doi/10.1146/annurev.arplant.58.091406.110525 PubMed DOI

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. https://www.pnas.org/content/95/16/9705 PubMed PMC

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. https://www.sciencedirect.com/science/article/pii/S1674205216301654?via%3Dihub PubMed

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. https://academic.oup.com/plphys/article/149/2/1154/6107832?login=true PubMed PMC

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. https://www.pnas.org/content/49/4/567 PubMed PMC

van Kooten O., Snel J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. – Photosynth. Res. 25: 147-150, 1990. https://link.springer.com/article/10.1007/BF00033156 PubMed DOI

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. https://www.annualreviews.org/doi/10.1146/annurev-arplant-043015-111709 PubMed DOI

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. https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-313X.2011.04747.x PubMed DOI

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. https://www.nature.com/articles/s41467-019-13954-0 PubMed PMC

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. https://onlinelibrary.wiley.com/doi/full/10.1111/tpj.13227 PubMed DOI