Skip to main content

The ability of P700 oxidation in photosystem I reflects chilling stress tolerance in cucumber

Abstract

Low temperature inhibits photosynthesis and negatively affects plant growth. Cucumber (Cucumis sativus L.) is a chilling-sensitive plant, and its greenhouse production requires considerable energy during the winter. Therefore, a useful stress marker for selecting chilling-tolerant cucumber cultivars is desirable. In this study, we evaluated chilling-stress damage in different cucumber cultivars by measuring photosynthetic parameters. The majority of cultivars showed decreases in the quantum yield of photosystem (PS) II [Fv/Fm and Y(II)] and the quantity of active PS I (Pm) after chilling stress. In contrast, Y(ND)—the ratio of the oxidized state of PSI reaction center chlorophyll P700 (P700+)—differed among cultivars and was perfectly inversely correlated with Y(NA)—the ratio of the non-photooxidizable P700. It has been known that P700+ accumulates under stress conditions and protects plants to suppress the generation of reactive oxygen species. In fact, cultivars unable to induce Y(ND) after chilling stress showed growth retardation with reductions in chlorophyll content and leaf area. Therefore, Y(ND) can be a useful marker to evaluate chilling-stress tolerance in cucumber.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM (1992) Cytochrome b6f complex: dynamic molecular organization, function and acclimation. Photosynth Res 34:341–357

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    Article  CAS  PubMed  Google Scholar 

  • Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bi H, Li F, Wang H, Ai X (2019) Overexpression of transketolase gene promotes chilling tolerance by increasing the activities of photosynthetic enzymes, alleviating oxidative damage and stabilizing cell structure in Cucumis sativus L. Physiol Plant 167:502–515

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Shi Y, Yang S (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222:1690–1704

    Article  PubMed  Google Scholar 

  • Foyer C, Furbank R, Harbinson J, Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25:83–100

    Article  CAS  PubMed  Google Scholar 

  • Furutani R, Ohnishi M, Mori Y et al (2021) The difficulty of estimating the electron transport rate at photosystem I. J Plant Res. https://doi.org/10.1007/s10265-021-01357-6

    Article  PubMed  Google Scholar 

  • Garstka M, Drożak A, Rosiak M et al (2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll–protein complexes in bean thylakoid membranes. Biochim Biophys Acta (BBA) 1710:13–23

    Article  CAS  Google Scholar 

  • Garstka M, Venema JH, Rumak I et al (2007) Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll–protein complexes in pea and tomato: plants with a different susceptibility to non-freezing temperature. Planta 226:1165–1181

    Article  CAS  PubMed  Google Scholar 

  • Hanawa H, Ishizaki K, Nohira K et al (2017) Land plants drive photorespiration as higher electron-sink: Comparative study of post-illumination transient O2-uptake rates from liverworts to angiosperms through ferns and gymnosperms. Physiol Plant 161:138–149

    Article  CAS  PubMed  Google Scholar 

  • Harbinson J, Foyer CH (1991) Relationships between the efficiencies of photosystems I and II and stromal redox state in CO2-free air: evidence for cyclic electron flow in vivo. Plant Physiol 97:41–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heber U, Walker D (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol 100:1621–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heber U, Neimanis S, Siebke K et al (1992) Chloroplast energization and oxidation of P700/plastocyanin in illuminated leaves at reduced levels of CO2 or oxygen. Photosynth Res 34:433–447

    Article  CAS  PubMed  Google Scholar 

  • Heidarvand L, Amiri RM (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32:419–431

    Article  CAS  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L et al (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  CAS  PubMed  Google Scholar 

  • Helman Y, Barkan E, Eisenstadt D et al (2005) Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol 138:2292–2298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hope AB (2000) Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. Biochim Biophys Acta (BBA) 1456:5–26

    Article  CAS  Google Scholar 

  • Ivanov AG, Morgan RM, Gray GR et al (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292

    Article  CAS  PubMed  Google Scholar 

  • Kanazawa A, Ostendorf E, Kohzuma K et al (2017) Chloroplast ATP synthase modulation of the thylakoid proton motive force: implications for photosystem I and photosystem II photoprotection. Front Plant Sci 8:719

    Article  PubMed  PubMed Central  Google Scholar 

  • Karapetyan NV (2008) Protective dessipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters. Photosynth Res 97:195–204

    Article  CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    Article  CAS  Google Scholar 

  • Klughammer C, Schreiber U (2008a) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Klughammer C, Schreiber U (2008b) Saturation Pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14

    Google Scholar 

  • Kohzuma K, Cruz JA, Akashi K et al (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant Cell Environ 32:209–219

    Article  CAS  PubMed  Google Scholar 

  • Kono M, Yamori W, Suzuki Y, Terashima I (2017) Photoprotection of PSI by Far-red light against thefFluctuating light-induced photoinhibition in Arabidopsis thaliana and field-grown plants. Plant Cell Physiol 58:35–45

    CAS  PubMed  Google Scholar 

  • Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: Cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541–548

    Article  CAS  PubMed  Google Scholar 

  • Mehler AH (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Arch Biochem Biophys 33:65–77

    Article  CAS  PubMed  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Miyake C (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Miyake C (2020) Molecular Mechanism of oxidation of P700 and suppression of ROS production in photosystem I in response to elctron-sink limitations in C3 Plants. Antioxidants 9:230

    Article  CAS  PubMed Central  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  CAS  PubMed  Google Scholar 

  • Nishio JN, Whitmarsh J (1993) Dissipation of the proton electrochemical potential in intact chloroplasts (II. The pH gradient monitored by cytochrome f reduction kinetics). Plant Physiol 101:89–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh M-H, Safarova RB, Eu Y-J et al (2009) Loss of peripheral polypeptides in the stromal side of photosystem I by light-chilling in cucumber leaves. Photochem Photobiol Sci 8:535–541

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi M, Furutani R, Sohtome T et al (2021) Photosynthetic parameters show specific responses to essential mineral deficiencies. Antioxidants 10:996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oxborough K, Ort DR (1995) In situ evidence that chilling in the light does not cause uncoupling of photophosphorylation or detachment of coupling factor in chilling-sensitive plants. Photosynth Res 43:93–105

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (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 spectroscopy. Biochim Biophys Acta (BBA) 975:384–394

    Article  CAS  Google Scholar 

  • Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106

    Article  CAS  PubMed  Google Scholar 

  • Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188

    PubMed  PubMed Central  Google Scholar 

  • Schöttler MA, Tóth SZ, Boulouis A, Kahlau S (2015) Photosynthetic complex stoichiometry dynamics in higher plants: biogenesis, function, and turnover of ATP synthase and the cytochrome b6f complex. J Exp Bot 66:2373–2400

    Article  PubMed  CAS  Google Scholar 

  • Sejima T, Takagi D, Fukayama H et al (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193

    Article  CAS  PubMed  Google Scholar 

  • Sejima T, Hanawa H, Shimakawa G et al (2016) Post-illumination transient O2-uptake is driven by photorespiration in tobacco leaves. Physiol Plant 156:227–238

    Article  CAS  PubMed  Google Scholar 

  • Shaku K, Shimakawa G, Hashiguchi M, Miyake C (2016) Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. Plant Cell Physiol 57:1443–1453

    CAS  PubMed  Google Scholar 

  • Shen W, Nada K, Tachibana S (1999) Effect of cold treatment on enzymic and nonenzymic antioxidant activities in leaves of chilling-tolerant and chilling-sensitive cucumber (Cucumis sativus L.) cultivars. J Jpn Soc Hortic Sci 68:967–973

    Article  CAS  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa G, Miyake C (2018) Oxidation of P700 ensures robust photosynthesis. Front Plant Sci 9:1617

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Shaku K, Miyake C (2016) Oxidation of P700 in photosystem I is essential for the growth of cyanobacteria. Plant Physiol 172:1443–1450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Ishizaki K, Tsukamoto S et al (2017) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimakawa G, Shaku K, Miyake C (2018) Reduction-induced suppression of electron flow (RISE) is relieved by non-ATP-consuming electron flow in Synechococcus elongatus PCC 7942. Front Microbiol 9:886

    Article  PubMed  PubMed Central  Google Scholar 

  • Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K (1996a) Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species. Plant Sci 115:157–164

    Article  CAS  Google Scholar 

  • Sonoike K (1996b) Photoinhibition of photosystem I: Its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247

    Article  CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293

    Article  CAS  Google Scholar 

  • Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235–238

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K, Kamo M, Hihara Y et al (1997) The mechanism of the degradation of psaB gene product, one of the photosynthetic reaction center subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63

    Article  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Suzuki Y, Nagao K, Takahashi Y et al (2021) Oxidation of the reaction center chlorophyll of photosystem I is induced via close cooperation of photosystems II and I with progress of drought stress in soybean seedlings. Soil Sci Plant Nutr. https://doi.org/10.1080/00380768.2021.2002124

    Article  Google Scholar 

  • Takagi D, Takumi S, Hashiguchi M et al (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi D, Amako K, Hashiguchi M et al (2017a) Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I. Plant J 91:306–324

    Article  CAS  PubMed  Google Scholar 

  • Takagi D, Ishizaki K, Hanawa H et al (2017b) Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. Physiol Plant 161:56–74

    Article  CAS  PubMed  Google Scholar 

  • Terashima I, Huang L-K, Osmond CB (1989) Effects of leaf chilling on thylakoid functions, measured at room temperature, in Cucumis sativus L. and Oryza sativa L. Plant Cell Physiol 30:841–850

    Article  CAS  Google Scholar 

  • Terashima I, Kashino Y, Katoh S (1991) Exposure of leaves of Cucumis sativus L. to low temperatures in the light causes uncoupling of thylakoids I. Studies with isolated thylakoids. Plant Cell Physiol 32:1267–1274

    CAS  Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    Article  CAS  Google Scholar 

  • Trissl H-W (1997) Determination of the quenching efficiency of the oxidized primary donor of Photosystem I, P700+: implications for the trapping mechanism. Photosynth Res 54:237–240

    Article  CAS  Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    Article  CAS  PubMed  Google Scholar 

  • Wada S, Takagi D, Miyake C et al (2019) Responses of the photosynthetic electron transport reactions stimulate the oxidation of the reaction center chlorophyll of photosystem I, P700, under drought and high temperatures in rice. Int J Mol Sci 20:2068

    Article  CAS  PubMed Central  Google Scholar 

  • Wada S, Suzuki Y, Miyake C (2020) Photorespiration enhances acidification of the thylakoid lumen, reduces the plastoquinone pool, and contributes to the oxidation of P700 at a lower partial pressure of CO2 in wheat leaves. Plants 9:319

    Article  CAS  PubMed Central  Google Scholar 

  • West KR, Wiskish JT (1968) Photosynthetic control by isolated pea chloroplasts. Biochem J 109:527–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson S, Clephan AL, Davies WJ (2001) Rapid low temperature-induced stomatal closure occurs in cold-tolerant Commelina communis leaves but not in cold-sensitive tobacco leaves, via a mechanism that involves apoplastic calcium but not abscisic acid. Plant Physiol 126:1566–1578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J-Q, Zhou Y-H, Huang L-F, Allen DJ (2002) Chill-induced inhibition of photosynthesis: genotypic variation within Cucumis sativus. Plant Cell Physiol 43:1182–1188

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z-S, Jin L-Q, Li Y-T et al (2016) Ultraviolet-B radiation (UV-B) relieves chilling-light-induced PSI photoinhibition and accelerates the recovery of CO2 assimilation in Cucumber (Cucumis sativus L.) leaves. Sci Rep 6:1–10

    CAS  Google Scholar 

  • Zhou YH, Yu JQ, Huang LF, Nogués S (2004) The relationship between CO2 assimilation, photosynthetic electron transport and water–water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant Cell Environ 27:1503–1514

    Article  Google Scholar 

  • Zhou Q, Wang C, Yamamoto H, Shikanai T (2021) PTOX-dependent safety valve does not oxidize P700 during photosynthetic induction in the Arabidopsis pgr5 mutant. Plant Physiol 188:1264–1276

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Mr. Shintaro Matsui, Takii Shubyo, Japan for his helpful suggestions.

Funding

This work was supported by JST, CREST, Japan, Grant Number JPMJCR15O3 and JPMJCR17O2 to Kentaro Ifuku and Chikahiro Miyake.

Author information

Authors and Affiliations

Authors

Contributions

KI, TN, and CM conceived the project; KT and YC performed the experiments; and KT and KI wrote the manuscript.

Corresponding author

Correspondence to Kentaro Ifuku.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Takeuchi, K., Che, Y., Nakano, T. et al. The ability of P700 oxidation in photosystem I reflects chilling stress tolerance in cucumber. J Plant Res 135, 681–692 (2022). https://doi.org/10.1007/s10265-022-01404-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-022-01404-w

Keywords

  • Chilling stress
  • Cucumber
  • Photoinhibition
  • Photosynthesis
  • Photosystem I
  • P700 oxidation